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.

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.

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.