Studying interactions among anthropogenic stressors in freshwater ecosystems: A systematic review of 2396 multiple-stressor experiments.

Understanding the interactions among anthropogenic stressors is critical for effective conservation and management of ecosystems. Freshwater scientists have invested considerable resources in conducting factorial experiments to disentangle stressor interactions by testing their individual and combined effects. However, the diversity of stressors and systems studied has hindered previous syntheses of this body of research. To overcome this challenge, we used a novel machine learning framework to identify relevant studies from over 235,000 publications. Our synthesis resulted in a new dataset of 2396 multiple-stressor experiments in freshwater systems. By summarizing the methods used in these studies, quantifying trends in the popularity of the investigated stressors, and performing co-occurrence analysis, we produce the most comprehensive overview of this diverse field of research to date. We provide both a taxonomy grouping the 909 investigated stressors into 31 classes and an open-source and interactive version of the dataset (https://jamesaorr.shinyapps.io/freshwater-multiple-stressors/). Inspired by our results, we provide a framework to help clarify whether statistical interactions detected by factorial experiments align with stressor interactions of interest, and we outline general guidelines for the design of multiple-stressor experiments relevant to any system. We conclude by highlighting the research directions required to better understand freshwater ecosystems facing multiple stressors.

Reconstructing historical time-series of cyanobacteria in lake sediments: Integrating technological innovation to enhance cyanobacterial management.

The global rise of cyanobacterial blooms emphasizes the need to develop tools to manage water bodies prone to cyanobacterial dominance. Reconstructing cyanobacterial baselines and identifying environmental drivers that favour cyanobacterial dominance are important to guide management decisions. Conventional techniques for estimating cyanobacteria in lake sediments require considerable resources, creating a barrier to routine reconstructions of cyanobacterial time-series. Here, we compare a relatively simple technique based on spectral inferences of cyanobacteria using visible near-infrared reflectance spectroscopy (VNIRS) with a molecular technique based on real-time PCR quantification (qPCR) of the 16S rRNA gene conserved in cyanobacteria in 30 lakes across a broad geographic gradient. We examined the sedimentary record from two perspectives: 1) relationships throughout the entire core (without radiometric dating); 2) relationships post-1900s with the aid of radiometric dating (i.e., 210Pb). Our findings suggest that the VNIRS-based cyanobacteria technique is best suited for reconstructing cyanobacterial abundance in recent decades (i.e., circa 1990 onwards). The VNIRS-based cyanobacteria technique showed agreement with those generated using qPCR, with 23 (76%) lakes showing a strong or very strong positive relationship between the results of the two techniques. However, five (17%) lakes showed negligible relationships, suggesting cyanobacteria VNIRS requires further refinement to understand where VNIRS is unsuitable. This knowledge will help scientists and lake managers select alternative cyanobacterial diagnostics where appropriate. These findings demonstrate the utility of VNIRS, in most instances, as a valuable tool for reconstructing past cyanobacterial prevalence.

Chemical Mixtures and Multiple Stressors: Same but Different?

Ecosystems are strongly influenced by multiple anthropogenic stressors, including a wide range of chemicals and their mixtures. Studies on the effects of multiple stressors have largely focussed on nonchemical stressors, whereas studies on chemical mixtures have largely ignored other stressors. However, both research areas face similar challenges and require similar tools and methods to predict the joint effects of chemicals or nonchemical stressors, and frameworks to integrate multiple chemical and nonchemical stressors are missing. We provide an overview of the research paradigms, tools, and methods commonly used in multiple stressor and chemical mixture research and discuss potential domains of cross-fertilization and joint challenges. First, we compare the general paradigms of ecotoxicology and (applied) ecology to explain the historical divide. Subsequently, we compare methods and approaches for the identification of interactions, stressor characterization, and designing experiments. We suggest that both multiple stressor and chemical mixture research are too focused on interactions and would benefit from integration regarding null model selection. Stressor characterization is typically more costly for chemical mixtures. While for chemical mixtures comprehensive classification systems at suborganismal level have been developed, recent classification systems for multiple stressors account for environmental context. Both research areas suffer from rather simplified experimental designs that focus on only a limited number of stressors, chemicals, and treatments. We discuss concepts that can guide more realistic designs capturing spatiotemporal stressor dynamics. We suggest that process-based and data-driven models are particularly promising to tackle the challenge of prediction of effects of chemical mixtures and nonchemical stressors on (meta-)communities and (meta-)food webs. We propose a framework to integrate the assessment of effects for multiple stressors and chemical mixtures. Environ Toxicol Chem 2023;42:1915-1936. © 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Local stressors mask the effects of warming in freshwater ecosystems.

Climate warming is a ubiquitous stressor in freshwater ecosystems, yet its interactive effects with other stressors are poorly understood. We address this knowledge gap by testing the ability of three contrasting null models to predict the joint impacts of warming and a range of other aquatic stressors using a new database of 296 experimental combinations. Despite concerns that stressors will interact to cause synergisms, we found that net impacts were usually best explained by the effect of the stronger stressor alone (the dominance null model), especially if this stressor was a local disturbance associated with human land use. Prediction accuracy depended on stressor identity and how asymmetric stressors were in the magnitude of their effects. These findings suggest we can effectively predict the impacts of multiple stressors by focusing on the stronger stressor, as habitat alteration, nutrients and contamination often override the biological consequences of higher temperatures in freshwater ecosystems.

Identifying factors that affect mountain lake sensitivity to atmospheric nitrogen deposition across multiple scales.

Increased nitrogen (N) deposition rates over the past century have affected both North American and European mountain lake ecosystems. Ecological sensitivity of mountain lakes to N deposition varies, however, because chemical and biological responses are modulated by local watershed and lake properties. We evaluated predictors of mountain lake sensitivity to atmospheric N deposition across North American and European mountain ranges and included as response variables dissolved inorganic N (DIN = NNH4+ + NNO3-) concentrations and phytoplankton biomass. Predictors of these responses were evaluated at three different spatial scales (hemispheric, regional, subregional) using regression tree, random forest, and generalized additive model (GAM) analysis. Analyses agreed that Northern Hemisphere mountain lake DIN was related to N deposition rates and smaller scale spatial variability (e.g., regional variability between North American and European lakes, and subregional variability between mountain ranges). Analyses suggested that DIN, N deposition, and subregional variability were important for Northern Hemisphere mountain lake phytoplankton biomass. Together, these findings highlight the need for finer-scale, subregional analyses (by mountain range) of lake sensitivity to N deposition. Subregional analyses revealed differences in predictor variables of lake sensitivity. In addition to N deposition rates, lake and watershed features such as land cover, bedrock geology, maximum lake depth (Zmax), and elevation were common modulators of lake DIN. Subregional phytoplankton biomass was consistently positively related with total phosphorus (TP) in Europe, while North American locations showed variable relationships with N or P. This study reveals scale-dependent watershed and lake characteristics modulate mountain lake ecological responses to atmospheric N deposition and provides important context to inform empirically based management strategies.

Using a lake sediment record to infer the long-term history of cyanobacteria and the recent rise of an anatoxin producing Dolichospermum sp.

Lakes that experience recurrent toxic cyanobacterial harmful algae blooms (cyanoHABS) are often subject to cultural eutrophication, where landscape development and upland activities increase the nutrient inputs to the water column and fuel cyanoHABS. Few studies have focused on the response of a lake to nutrient inputs for which the natural geomorphic setting predisposes a nutrient-rich water column to already support abundant cyanobacteria. Here, we present a sediment core record from a lake surrounded by parkland that experiences recurrent cyanoHABs which produce dangerous levels of the neurotoxin, anatoxin-a, impacting the recreational use of the lake and park. Using photoautotrophic pigments in the sediment record, we establish cyanobacteria have long been part of the diverse and abundant phytoplankton community within the lake. Despite this long record, shotgun metagenome and other DNA analyses of the sediment record suggest that the current anatoxin-a producer Dolichospermum sp. WA102 only emerged to dominate the cyanobacterial community in the mid-1990s. A period of lakeshore farming that finished in the 1950s-1960s and possibly the stocking of rainbow trout fry (1970-2016) coincide with a progressive shift in primary production, together with a change in bacterial communities. Based on the history of the lake and contemporary ecology of Dolichospermum, we propose that the legacy of nutrient inputs and changes in nutrient cycling within the lake has encouraged the development of an ecosystem where the toxin producing Dolichospermum sp WA102 is highly competitive. Understanding the historical presence of cyanobacteria in the lake provides a context for current-day management strategies of cyanoHABs.

Towards a unified study of multiple stressors: divisions and common goals across research disciplines.

Anthropogenic environmental changes, or 'stressors', increasingly threaten biodiversity and ecosystem functioning worldwide. Multiple-stressor research is a rapidly expanding field of science that seeks to understand and ultimately predict the interactions between stressors. Reviews and meta-analyses of the primary scientific literature have largely been specific to either freshwater, marine or terrestrial ecology, or ecotoxicology. In this cross-disciplinary study, we review the state of knowledge within and among these disciplines to highlight commonality and division in multiple-stressor research. Our review goes beyond a description of previous research by using quantitative bibliometric analysis to identify the division between disciplines and link previously disconnected research communities. Towards a unified research framework, we discuss the shared goal of increased realism through both ecological and temporal complexity, with the overarching aim of improving predictive power. In a rapidly changing world, advancing our understanding of the cumulative ecological impacts of multiple stressors is critical for biodiversity conservation and ecosystem management. Identifying and overcoming the barriers to interdisciplinary knowledge exchange is necessary in rising to this challenge. Division between ecosystem types and disciplines is largely a human creation. Species and stressors cross these borders and so should the scientists who study them.

Multiscale drivers of phytoplankton communities in north-temperate lakes.

Multiple factors operating across different spatial and temporal scales affect ß-diversity, the variation in community composition among sites. Disentangling the relative influence of co-occurring ecological drivers over broad biogeographic gradients and time is critical to developing mechanistic understanding of community responses to natural environmental heterogeneity as well as predicting the effects of anthropogenic change. We partitioned taxonomic ß-diversity in phytoplankton communities across 75 north-temperate lakes and reservoirs in Alberta, Canada, using data-driven, spatially constrained null models to differentiate between spatially structured, spatially independent, and spuriously correlated associations with a suite of biologically relevant environmental variables. Phytoplankton ß-diversity was largely independent of space, indicating spatial processes (e.g., dispersal limitation) likely play a minor role in structuring communities at the regional scale. Our analysis also identified seasonal differences in the importance of environmental factors, suggesting a general shift toward greater relevance of local, in-lake (e.g., nutrients and Secchi depth) over regional, atmospheric and catchment-level (e.g., monthly solar radiation and grassland coverage) drivers as the open-water growing season progressed. Several local and regional variables explained taxonomic variation jointly, reflecting climatic and land-use linkages (e.g., air temperature and water column stability or pastureland and nutrient enrichment) that underscore the importance of understanding how phytoplankton communities integrate, and may serve as sentinels of, broader anthropogenic changes. We also discovered similar community composition in natural and constructed water bodies, demonstrating rapid filtering of regional species to match local environmental conditions in reservoirs comparable to those in natural habitats. Finally, certain factors related to human footprint (e.g., cropland development) explained the composition of bloom-forming and/or toxic cyanobacteria more than the overall phytoplankton community, suggesting their heightened importance to integrated watershed management.

The NSERC Canadian Lake Pulse Network: A national assessment of lake health providing science for water management in a changing climate.

The distribution and quality of water resources vary dramatically across Canada, and human impacts such as land-use and climate changes are exacerbating uncertainties in water supply and security. At the national level, Canada has no enforceable standards for safe drinking water and no comprehensive water-monitoring program to provide detailed, timely reporting on the state of water resources. To provide Canada's first national assessment of lake health, the NSERC Canadian Lake Pulse Network was launched in 2016 as an academic-government research partnership. LakePulse uses traditional approaches for limnological monitoring as well as state-of-the-art methods in the fields of genomics, emerging contaminants, greenhouse gases, invasive pathogens, paleolimnology, spatial modelling, statistical analysis, and remote sensing. A coordinated sampling program of about 680 lakes together with historical archives and a geomatics analysis of over 80,000 lake watersheds are used to examine the extent to which lakes are being altered now and in the future, and how this impacts aquatic ecosystem services of societal importance. Herein we review the network context, objectives and methods.

An improved null model for assessing the net effects of multiple stressors on communities.

Ecological stressors (i.e., environmental factors outside their normal range of variation) can mediate each other through their interactions, leading to unexpected combined effects on communities. Determining whether the net effect of stressors is ecologically surprising requires comparing their cumulative impact to a null model that represents the linear combination of their individual effects (i.e., an additive expectation). However, we show that standard additive and multiplicative null models that base their predictions on the effects of single stressors on community properties (e.g., species richness or biomass) do not provide this linear expectation, leading to incorrect interpretations of antagonistic and synergistic responses by communities. We present an alternative, the compositional null model, which instead bases its predictions on the effects of stressors on individual species, and then aggregates them to the community level. Simulations demonstrate the improved ability of the compositional null model to accurately provide a linear expectation of the net effect of stressors. We simulate the response of communities to paired stressors that affect species in a purely additive fashion and compare the relative abilities of the compositional null model and two standard community property null models (additive and multiplicative) to predict these linear changes in species richness and community biomass across different combinations (both positive, negative, or opposite) and intensities of stressors. The compositional model predicts the linear effects of multiple stressors under almost all scenarios, allowing for proper classification of net effects, whereas the standard null models do not. Our findings suggest that current estimates of the prevalence of ecological surprises on communities based on community property null models are unreliable, and should be improved by integrating the responses of individual species to the community level as does our compositional null model.

Regional diversity reverses the negative impacts of an alien predator on local species-poor communities.

Species diversity is often an implicit source of biological insurance for communities against the impacts of novel perturbations, such as the introduction of an invasive species. High environmental heterogeneity (e.g., a mountainous gradient) is expected to beget greater regional species diversity and variation in functional traits related to environmental tolerances. Thus, heterogeneous metacommunities are expected to provide more tolerant colonists that buffer stressed local communities in the absence of dispersal limitation. We tested the hypothesis that importation of a regional zooplankton pool assembled from a diverse array of lakes and ponds lessens the impacts of a novel predator on local species-poor alpine communities by increasing response diversity (i.e., diversity of tolerances to environmental change) as mediated by variation in functional traits related to predator evasion. We also tested whether impacts varied with temperature, as warming may modify (e.g., dampen or amplify) invasion effects. An eight-week factorial experiment ([fishless vs. introduced Oncorhynchus mykiss (rainbow trout)] × [ambient temperature vs. heated] × [local vs. local + regional species pool]) was conducted using 32 1,000-L mesocosms. Associations between experimental treatments and species functional traits were tested by R-mode linked to Q-mode (RLQ) and fourth-corner analyses. Although the introduced predator suppressed local species richness and community biomass, colonization by several montane zooplankters reversed these negative effects, resulting in increased species diversity and production. Invasion resistance was unaffected by higher temperatures, which failed to elicit any significance impacts on the community. We discovered that the smaller body sizes of imported species drove functional overcompensation (i.e., increased production) in invaded communities. The observed ecological surprise showed how regionally sourced biodiversity from a highly heterogeneous landscape can offset, and even reverse, the local negative impacts of an invasive species. Further, prey body size was found to be a key species trait mediating the ecological impacts of the aquatic invasive predator. Our study highlights the novel application of a functional approach to understanding the impacts of biological invasions, using species traits that pertain directly to potential responses to exotic species.

Experimental iron amendment suppresses toxic cyanobacteria in a hypereutrophic lake.

The effects of reducing nutrient inputs to lakes and reservoirs are often delayed by hysteresis resulting from internal phosphorus (P) loading from sediments. Consequently, controlling harmful algal blooms (HABs) in many eutrophic ecosystems requires additional management to improve water quality. We manipulated iron (Fe) concentrations in a hypereutrophic lake to determine if Fe amendment would suppress HABs by inhibiting P release from sediments. Our experiment consisted of 15 in situ mesocosms, 12 of which each received a different dose of Fe (ranging from 2 to 225 g/m2 ); the remaining three were unmanipulated to serve as controls. Iron amendment decreased P accumulation in porewaters and the flux of P from sediments, which significantly lowered P concentrations in the water column. Iron exerted significant dose-dependent negative effects on the biomass of phytoplankton and periphyton, and reduced the dominance of cyanobacteria. Even at the lowest doses, Fe appeared to reduce the toxicity of cyanobacterial blooms, as measured by concentrations of hepatotoxic microcystins. Overall, our findings highlight the potential for Fe treatment as an effective strategy for minimizing HABs in eutrophic lakes and reservoirs. More broadly, our study reinforces the importance of Fe in regulating the trophic state of freshwaters, and the sensitivity of certain ecosystems to changes in Fe supply. Finally, we hypothesize that decreases in natural Fe supplies to lakes associated with anthropogenic activities may worsen outbreaks of toxic cyanobacteria.

Net effects of multiple stressors in freshwater ecosystems: a meta-analysis.

The accelerating rate of global change has focused attention on the cumulative impacts of novel and extreme environmental changes (i.e. stressors), especially in marine ecosystems. As integrators of local catchment and regional processes, freshwater ecosystems are also ranked highly sensitive to the net effects of multiple stressors, yet there has not been a large-scale quantitative synthesis. We analysed data from 88 papers including 286 responses of freshwater ecosystems to paired stressors and discovered that overall, their cumulative mean effect size was less than the sum of their single effects (i.e. an antagonistic interaction). Net effects of dual stressors on diversity and functional performance response metrics were additive and antagonistic, respectively. Across individual studies, a simple vote-counting method revealed that the net effects of stressor pairs were frequently more antagonistic (41%) than synergistic (28%), additive (16%) or reversed (15%). Here, we define a reversal as occurring when the net impact of two stressors is in the opposite direction (negative or positive) from that of the sum of their single effects. While warming paired with nutrification resulted in additive net effects, the overall mean net effect of warming combined with a second stressor was antagonistic. Most importantly, the mean net effects across all stressor pairs and response metrics were consistently antagonistic or additive, contrasting the greater prevalence of reported synergies in marine systems. Here, a possible explanation for more antagonistic responses by freshwater biota to stressors is that the inherent greater environmental variability of smaller aquatic ecosystems fosters greater potential for acclimation and co-adaptation to multiple stressors.

Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene.

Increases in atmospheric temperature and nutrients from land are thought to be promoting the expansion of harmful cyanobacteria in lakes worldwide, yet to date there has been no quantitative synthesis of long-term trends. To test whether cyanobacteria have increased in abundance over the past ~ 200 years and evaluate the relative influence of potential causal mechanisms, we synthesised 108 highly resolved sedimentary time series and 18 decadal-scale monitoring records from north temperate-subarctic lakes. We demonstrate that: (1) cyanobacteria have increased significantly since c. 1800 ce, (2) they have increased disproportionately relative to other phytoplankton, and (3) cyanobacteria increased more rapidly post c. 1945 ce. Variation among lakes in the rates of increase was explained best by nutrient concentration (phosphorus and nitrogen), and temperature was of secondary importance. Although cyanobacterial biomass has declined in some managed lakes with reduced nutrient influx, the larger spatio-temporal scale of sedimentary records show continued increases in cyanobacteria throughout the north temperate-subarctic regions.

Missing effects of anthropogenic nutrient deposition on sentinel alpine ecosystems.

Anthropogenic nitrogen (N) deposition affects unproductive remote alpine and circumpolar ecosystems, which are often considered sentinels of global change. Human activities and forest fires can also elevate phosphorus (P) deposition, possibly compounding the ecological effects of increased N deposition given the ubiquity of nutrient co-limitation of primary producers. Low N : P ratios coupled with evidence of NP-limitation from bioassays led us to hypothesize that P indirectly stimulates phytoplankton by amplifying the direct positive effect of N (i.e. serial N-limitation) in alpine ponds. We tested the hypothesis using the first replicated N × P enrichment experiment conducted at the whole-ecosystem level, which involved 12 alpine ponds located in the low N deposition backcountry of the eastern Front Range of the Canadian Rockies. Although applications of N and P elevated ambient N and P concentrations by 2-5×, seston and plankton remained relatively unaffected in the amended ponds. However, additions of ammonium nitrate elevated the δ(15) N signals of both primary producers and herbivores (fairy shrimp; Anostraca), attesting to trophic transfer of N deposition to consumers. Further, in situ bioassays revealed that grazing by high ambient densities of fairy shrimp together with potential competition from algae lining the pond bottoms suppressed the otherwise serially N-limited response by phytoplankton. Our findings highlight how indirect effects of biotic interactions rather the often implicit direct effects of chemical changes can regulate the sensitivities of extreme ecosystems to nutrient deposition.

Increased mercury loadings to western Canadian alpine lakes over the past 150 years.

We reconstructed historical trends in mercury (Hg) accumulation over the past ∼ 150 years in nine western Canadian alpine lakes. Recent Hg accumulation rates (fluxes) ranged between ∼ 7 and 75 µg m(-2) yr(-1), which were an average of 1.8 times higher than preindustrial (i.e., pre-1850) fluxes. Increased Hg fluxes in these lakes were less than at lower elevation sites, showing that despite the potential for increased deposition, alpine lakes are no more susceptible to Hg accumulation. Unlike other studies, we found that geographic setting, changes in chlorophyll-inferred algal production, and climate were not significant predictors of [Hg] or Hg flux in lakes. Instead, our findings highlight how a combination of atmospheric deposition and site-specific processes, including organic matter supply and catchment weathering, better explain sequestration of Hg in alpine lakes.

Recent climate extremes alter alpine lake ecosystems.

Here, we show that alpine lake ecosystems are responsive to interannual variation in climate, based on long-term limnological and meteorological data from the Canadian Rockies. In the 2000s, in years with colder winter temperatures, higher winter snowfall, later snowmelt, shorter ice-free seasons, and dryer summers, relative to the 1990s, alpine lakes became clearer, warmer, and mixed to deeper depths. Further, lakes became more dilute and nutrient-poor, the latter leading to significant declines in total phytoplankton biomass. However, increased concentrations of dissolved organic carbon in lake water stimulated the appearance of small mixotrophic algal species, partially offsetting the decline in autotrophic phytoplankton biomass and increasing algal species richness. The climate regime in the 2000s altered the physical, chemical, and biological character and the function of high-elevation aquatic ecosystems. Forecasts of increased climatic variability in the future pose serious ramifications for both the biodiversity and ecosystem function of high-elevation lakes.

Resilience of epilithic algal assemblages in atmospherically and experimentally acidified boreal lakes.

Algal assemblages can be highly responsive to environmental changes in recovering acidified lakes. We compared epilithic algal assemblages in boreal lakes during chemical recovery from atmospheric (Killarney Park, Ontario) and experimental (Lake 302S, Experimental Lakes Area, Ontario) acidification to assess the impact of spatial and temporal scale of severe acidification on taxonomic resilience (i.e. recovery rate). Resilience was measured as the distance traveled by lakes in ordination space during pH recovery based on canonical correspondence analysis. Resilience was relatively negligible in the Killarney lakes, suggesting that eight years of experimental acidification in Lake 302S had less impact on biological recovery than did decades of regional acidification. Increases in dissolved organic carbon, dissolved inorganic carbon, and calcium best explained temporal variance of epilithic species abundances in the recovering acidified lakes. In Lake 302S, contrasting trajectories of taxonomic resilience and resistance, i.e. displacement from reference conditions following a perturbation, indicated that ecological factors affecting epilithon differed at corresponding pH levels during recovery and acidification. Our findings reveal that modeling of ecosystem recovery from severe acidification must account for the spatial and temporal scale of the perturbation, and biological delay responses that result in differences between recovery and acidification trajectories.