Documenting the impacts of increasing salinity in freshwater and coastal ecosystems: Introduction to the special issue

Freshwater salinization is the process of changing ion concentrations (e.g., Na+, Mg2+, K+, Cl−, CO 3 2 − , SO 4 2 − ) relative to background levels due to human activities (e.g., agriculture, application of road de-icing salts, water and resource extraction, climate change, and sea-level rise; Williams 2001; Cañedo-Argüelles et al. 2016). Although considerably less studied than other environmental issues (Cañedo-Argüelles 2020), salinization is widely accepted as presenting major challenges to freshwater and coastal biodiversity (Cunillera-Montcusí et al. 2022). Existing data and research show a clear rise in freshwater salinization worldwide (Dugan et al. 2017; Cañedo-Argüelles 2020; Jeppesen et al. 2020; Kaushal et al. 2021), yet key knowledge gaps and management challenges remain due to the complexity (Kaushal et al. 2018) and prevalence of the problem (Cañedo-Argüelles 2020; Jeppesen et al. 2020). Current literature has neglected to provide unbiased geographic coverage (Cunillera-Montcusí et al. 2022), and ecosystem-level responses (e.g., functions and services) are rarely assessed (Herbert et al. 2015). Compelling calls for research agendas that address the need for salinization research at multiple scales (e.g., global, regional, local) are well timed (Cunillera-Montcusí et al. 2022). One identified research gap points to the need for networks of researchers working together at regional scales using experimental approaches to identify impacts on biodiversity, community salinity thresholds, and landscape-scale drivers. Here, we document the results of a networked Global Salt Initiative (GSI) that performed in situ experiments on lakes to look at ecosystem-level impacts: their findings suggest that North American and European water quality guidelines for salt are far too low to prevent ecosystem-level impacts. The further purpose of this Special Issue (SI) is to document the results of ecosystem-level impacts of increasing salinity on lake and coastal area biodiversity and ecosystem functioning from a variety of perspectives. Salinity is an important environmental parameter, like temperature and light, that directly affects freshwater organisms via osmotic stress (Silver and Donini 2021). Despite the rise in freshwater salinization worldwide, however, from a socioeconomic perspective, salts are perhaps still viewed as a natural component of ecosystems with negligible impacts on biodiversity and ecosystem functioning (Gorostiza and Saurí 2019). Moreover, current management solutions are technically challenging and expensive (Cañedo-Argüelles 2020), making salinization a seemingly unavoidable consequence of many human activities. We have witnessed a substantial increase in research on freshwater salinization worldwide, including some high profile papers and reviews (Dugan et al. 2017; Kaushal et al. 2018; Hintz and Relyea 2019; Arnott et al. 2020; Dugan et al. 2020; Thorslund et al. 2021; Cunillera-Montcusí et al. 2022; Hintz et al. 2022a,b), scientific data papers (Dugan et al. 2017; Thorslund and van Vliet 2020), and three SIs devoted to the topic: (1) SI in Philosophical Transactions B (2018) on “Salt in freshwaters: causes, ecological consequences and future prospects” (Cañedo-Argüelles et al. 2019); (2) SI in Water (coming in 2022) focused on “Salinization of water resources: ongoing and future trends” (Colombani 2022); and (3) SI in Hydrobiologia (coming in 2023) focused on “Effects of induced changes in salinity on inland and coastal water ecosystems,” edited by Jeppesen, Cañedo-Argüelles, Entrekin, Padisák, and Sarma. What makes this SI in Limnology and Oceanography Letters unique is the principal focus on determining impacts of salinization on lakes and coastal ecosystems worldwide (as stated above). When faced with trying to understand the complexity of what happens when a mixture of salt ions interacts with other anthropogenically derived substances in aquatic ecosystems, experts refer to the result as a “freshwater salinization syndrome” (FSS; Kaushal et al. 2018). Like any syndrome, the combination of complex factors (chemical, biological, geological, environmental, and social) associated with freshwater salinization can result in extreme consequences like unsafe drinking water (Ehmar Khan et al. 2014; Kaushal 2016); mobilized contaminants (Herbert et al. 2015; Kaushal et al. 2022); changes in the toxicity and bioaccumulation of co-occurring pollutants such as pesticides (Saranjampour et al. 2017; Hutton et al. 2021; Xing et al. 2022); and a loss of freshwater biodiversity (James et al. 2003; Castillo et al. 2018; Hintz and Relyea 2019; Hébert et al. 2022). FSS is expected to progress in five distinct stages as outlined here (this SI) for the first time (Kaushal et al. 2022). As a result of inadequate salinity regulations (Huling and Hollocher 1972; Jackson and Jobbàgy 2005; Gorostiza and Saurí 2019; Schuler et al. 2019; Arnott et al. 2020; Hintz et al. 2022b), salinization continues to impact freshwater biodiversity and ecosystem function, as well as freshwater ecosystem services such as sector-specific water withdrawals in many regions of the world (e.g., irrigation agriculture; drinking water; van Vliet et al. 2017). The global scale and complexity of freshwater ecosystem salinization and the seemingly irreconcilable demands of various anthropogenic practices (e.g., agriculture, road-de-icing, mining) help to explain the recent increase in scientific research in this area. International teams working on freshwater salinization recently published calls for networked research approaches (e.g., coordinated mesocosm experiments across regions) that focus on the most urgent knowledge gaps (Hintz and Relyea 2019; Jeppesen et al. 2020; Cunillera-Montcusí et al. 2022). All three guest editors of this SI are a part of the networked GSI, which began with the design of a Global Salt Experiment (GSE) conceived at a GLEON (Global Lakes Ecological Observatory Network) meeting in Mohonk (New York) 2017. Interdisciplinary researchers led by Drs Shelley Arnott and William Hintz designed a large-scale, simultaneous mesocosm experiment that was performed in 16 lakes within Canada (CA), Europe (EU), and the United States (US) in the summer of 2018. The experiment was performed under natural conditions and was designed to address a lack of experimental research on the direct impacts of road de-icing salt on pristine lake zooplankton, outside of laboratory tests. The results of these regional lake mesocosm experiments are published in Hintz et al. (2022b) and in this SI as a series of six papers that either combine data to evaluate cross-regional impacts (Arnott et al. 2022) or examine unique regional effects of salt and other stressors on communities at the base of the food chain (Moffett et al. 2020; Greco et al. 2021; Astorg et al. 2022). The GSE results (i) are complemented by 14 selected research papers that examine what is known about effects of freshwater salinization on zooplankton communities worldwide; (ii) document and predict trends of ongoing increases in lake salinity in North America caused predominantly by road salt; (iii) examine complex impacts of salinity on lake associated freshwater ecosystems (e.g., urban wetlands, streams, and ponds); (iv) examine impacts of increased human land-water usage patterns causing saltwater intrusion and nutrient loadings in coastal marine areas; and (v) document the need to consider community-level impacts and the freshwater salinization syndrome. The contributions in this SI provide depth and scope in support of GSI's recent overarching paper that explains how zooplankton abundances will be lost in lakes due to current water quality guidelines (Hintz et al. 2022b). Currently, freshwater salinization is regulated through recommendations (i.e., non-legally enforced standards) that are based on laboratory toxicity tests, and the focus is on total salinity and/or chloride concentrations (e.g., chronic chloride [Cl−] guidelines for Canada and the United States are 120 and 230 mg L−1, respectively). Addressing the problem of freshwater salinization will require more rigorous guidelines that capture the complexity of ecosystems and consider the toxicity of different ion mixtures and chemical cocktails (Cañedo-Argüelles et al. 2016; Schuler et al. 2019). Recently, Hintz et al.'s (2022b) paper created heightened scientific appreciation, with over 2300 comments and 69,100 upvotes in the New Reddit Journal of Science (NRJS 2022). Such appreciation included the need for investigations into microbes that use road salt for energy; the need for knowledge about how products affect ecosystems; or the use of different substances for safe roads, such as beet juice, gravel (Finland), or sand. Without knowledge and evidence, legislative changes are unlikely. We provide a brief overview in this SI to enhance the probability of legislative change. The most important finding of our coordinated, mesocosm, experiments (on impacts of increasing salt on lake zooplankton communities) was the precipitous loss of zooplankton biomass (e.g., 50% reductions) at salt concentrations below existing chronic concentration guidelines in CA, US, and EU (Hintz et al. 2022b). Vitally, Hébert et al. (2022) showed that the loss in abundance was accompanied by a loss in zooplankton biodiversity with fewer species, reduced community diversity, and a consistent trophic shift in algal communities (dominance) across all lakes, demonstrated by increasing chlorophyll a (Chl a). Arnott et al. (2022) were unable to link sensitivity of zooplankton communities (i.e., intraspecific variation in community-level salt responses) to their original species pool or local environmental conditions. Yet, some lakes had more robust zooplankton community responses, possibly due to evolutionary adaptation (Moffett et al. 2020). Nonetheless, even the most robust zooplankton communities were lost at upper Cl− concentrations leading to a proliferation of algae released from grazing pressure. The paper by Astorg et al. (2022) uniquely investigated shifts in the algal and fungal eukaryotic plankton community using DNA metabarcoding with 18 S rRNA. They found massive compositional shifts in plankton communities with increasing salinity among diverse groups of fungal dominants and unicellular algae. Eventually, high Cl− concentrations combined with high nutrient loadings are expected to favor cyanobacteria (Porter-Goff et al. 2013), but this is not universally the case for lakes wherein cyanobacteria are absent and other groups of phytoplankton are favored in the phytoplankton community (Astorg et al. 2022). More research on effects of multiple stressors is needed. Examining interactions between Cl− and nutrients, Greco et al. (2021) exposed zooplankton communities in their mesocosms to either ambient or high nutrient levels (~ 3–4× ambient), concluding that although higher nutrients increased food availability, there was no concomitant increase in zooplankton tolerance to salt. Temperature is another key variable expected to interact with salinity, and McClymont et al. (2022) found that algae were more responsive to changes in temperature than zooplankton when subjected to interactions with Cl− as a stressor. Despite the losses in zooplankton abundance and diversity that we found in our GSI mesocosm experiments, Wersebe et al. (2021) found only slight changes in the relative abundance of Daphnia ephippia in response to increasing suburban lake salinization over 170 years (with changing [Cl−] from 1 to 150 mg L−1) in a paleolimnological study of ephippial densities in lake sediments. This ecological response in zooplankton may be explained by the possible attenuating effects of calcium and water hardness (Elphick et al. 2011). However, more research is needed to address ecological and evolutionary responses to freshwater salinization in lakes with different environmental conditions as previous studies have focused on soft water, boreal shield lakes. Dugan's research group focused on quantifying and modeling the increases in lake salinity levels across North America over the past 50 years (Dugan et al. 2017; Dugan et al. 2020). In this special issue, the group presents their most recent findings in a series of three original papers: (1) Dugan and Rock (2021) model increasing salinity in a distinctive groundwater fed seepage lake located next to a highway in Northern Wisconsin. By adjusting an outdated box model (Bowser 1992) to account for increasing Cl− reservoirs in the soil, the authors demonstrate why previously predicted 2020 Cl− concentrations in Sparking Lake were surpassed by 50%, highlighting the need to consider soil as a long-term reservoir of salt. (2) In a second paper, they demonstrate how Lake Michigan annually receives more than 1 million metric tonnes of Cl− from five main urbanized rivers (i.e., the Grand, St. Joseph, Fox, Kalamazoo, and Milwaukee Rivers, Dugan et al. 2021). If these trends continue, they predict that Lake Michigan could reach 18 mg L−1 Cl− by 2050, a concentration known to decrease reproduction and increase mortality of Daphnia for lakes within the Canadian Shield (Arnott et al. 2020). (3) Ladwig et al. (2021) investigate the understudied impact of increasing lake salinities on lake depth stratification for north temperate lakes. They show delays in spring turnover, prolonged summer stratification periods, and increases in water column stability during spring, summer, and winter, which could have critical impacts like anoxic conditions in the hypolimnion during summer. Impacts of increasing dissolved salts extend to muddled lake deltas that may once have persisted as unique ecosystems (Richardson et al. 2021). The associated complexity of salt impacted streams, ponds, and wetlands are covered in a series of three SI papers by Shattuck et al. (2022); Bolotin et al. (2022); and Kinsman-Costello et al. (2022). Decades of data are needed to understand prolonged salinity trends in stream surface waters outside of seasonal hydrologic variability. Shattuck et al. (2022) used long-term data for New Hampshire streams combined with insights from high-frequency sensors (15-min intervals) to elucidate influences of groundwater Cl− sources and extreme flooding events. Chloride concentrations increased threefold since 1953 in an urban site, and urban streams often exceed relatively lax (230 mg L−1) chronic chloride guidelines in all seasons, but surprisingly an extreme flood event reset Cl− levels for up to a decade. Bolotin et al. (2022) provide a predictive salinity classification model based on key drivers (e.g., precipitation, slope, and soil salinity), which may help managers track salinity across and within basins of the central and western US. Predictive modeling characterizing stream salinization patterns are needed across the globe to use as reference and management tools. Kinsman-Costello et al. (2022) provide an important review of salinization syndrome impacts on urban wetlands. They identify a knowledge gap that limits our understanding of how urban wetland salinization impacts biogeochemical processing (e.g., N & P nutrient removal) in urban wetlands, which is an ecosystem service that many urban wetlands are designed to perform. Most research on trends in freshwater salinization focuses on inland freshwater ecosystems such as rivers (Cañedo-Argüelles et al. 2013; Kaushal et al. 2022) and lakes (Dugan et al. 2017). However, coastal ecosystems also face severe salinization due mainly to a combination of water withdrawal—for irrigation and human consumption—and sea-level rise (Oude Essink et al. 2010; Mahmuduzzaman et al. 2014; Dasgupta et al. 2015; Mabrouk et al. 2018). To elucidate problems facing sensitive groundwater dependent coastal ecosystems in the Pacific and beyond, Dulai et al. (2021) use Hawaii as a case study to show how changes in groundwater nutrient and salinity discharge levels modify native marine macroalgal growth rates, branching patterns, and ostensibly weaken ensuing competitive interactions with invasive macroalgae. Tidal freshwater marsh communities are significantly affected by sea-level rise and seawater intrusion. Mobilian et al. (2020) conducted a large-scale, multiyear, field manipulation to address how in situ microbial community diversity and carbon cycling activity are more affected by the consistent press of seawater intrusion (i.e., by long-term sea-level rise—than by pulses of high salinity due to episodic seawater intrusion). Osburn et al. (2022) employed a laboratory experiment to understand the implications of what may happen at the mouth of coastal estuaries when toxic cyanobacterial blooms, such as those that occur in upstream eutrophic reservoirs, encounter salinity when they are flushed downstream to the ocean. Their results indicate that such practices may magnify the harmful effects of cyanobacterial blooms when they mix with ocean water. Changes in macroalgae and microbial communities along coastal salinity continua lead to predictable shifts in phytoplankton community diversity with a minimum diversity at intermediate salinity levels (i.e., at a salinity of 8 g L−1; Olli et al. 2022). However, when phytoplankton chlorophyll (Chl a) relative to total nitrogen was measured as an indicator of resource use efficiency (RUE), Olli et al. (2022) found functional redundancy in RUE likely due to fewer trophic interactions (i.e., lower resource competition and reduced grazing). We know that species occur within communities and ecosystems, and that the interaction between them can modulate the sensitivity of individual species to stressors (Baillard et al. 2020; Thompson et al. 2021). Kefford et al. (2021) and Arnott et al. (2022) call for more community-based toxicity tests and coordinated mesocosm studies that account for species interactions rather than single species toxicity tests performed in laboratories when salinity standards for the protection of aquatic ecosystems are developed. Results reported in this SI provide new knowledge about how lake and coastal ecosystems, zooplankton, plankton and microbial (algal, bacterial, and fungal) communities will likely respond to increasing salinity, not only with reductions in zooplankton abundance, but also with fewer species of zooplankton, and a consistent trophic shift towards primary producers and microbiota. Regional differences and high intra- and inter-specific variation in species responses to changing salinity are to be expected, and it may be difficult to link variable responses to drivers in multistressor environments. We conclude that the need to better understand lake and coastal salinization impacts on plankton communities will intensify with global climate change in most parts of the world (Jeppesen et al. 2015), and impacts will vary regionally. For example, in regions receiving large freshwater inputs from melting glaciers, salinity will decrease (Garcia-Eidell et al. 2019). In the search for solutions to FSS impacts, effective management practices that adjust for regional variability (e.g., calcium levels, additional contaminant pressures, changing climate and precipitation patterns) in ecosystem and community responses will help prevent costly impacts. The authors thank Jim Cloern, Gesa Weyhenmeyer, Steven Perez, and the Wiley editorial team for their vital and judicious assistance. The authors thank all the reviewers who graciously gave their time, expertise, and advice in helping review and improve special issue manuscripts. This study is part of the Global Salt Initiative, a working group formed during the Global Lake Ecological Observatory Network (GLEON) meeting held in 2017. The authors acknowledge the following funding sources for supporting our research, writing, and editing: Natural Sciences and Engineering Research Council (NSERC) Discovery Grant program (DG 03834-2015 to SJM and DG 05143-2016 to AMD). MC was supported by a Ramón y Cajal contract funded by the Spanish Ministry of Science and Innovation (RYC2020-029829-I). None declared.