Jeremy J. Piggott

Reconceptualizing synergism and antagonism among multiple stressors

The potential for complex synergistic or antagonistic interactions between multiple stressors presents one of the largest uncertainties when predicting ecological change but, despite common use of the terms in the scientific literature, a consensus on their operational definition is still lacking. The identification of synergism or antagonism is generally straightforward when stressors operate in the same direction, but if individual stressor effects oppose each other, the definition of synergism is paradoxical because what is synergistic to one stressors effect direction is antagonistic to the others. In their highly cited meta-analysis, Crain et al. (Ecology Letters, 11, 2008: 1304) assumed in situations with opposing individual effects that synergy only occurs when the cumulative effect is more negative than the additive sum of the opposing individual effects. We argue against this and propose a new systematic classification based on an additive effects model that combines the magnitude and response direction of the cumulative effect and the interaction effect. A new class of “mitigating synergism” is identified, where cumulative effects are reversed and enhanced. We applied our directional classification to the dataset compiled by Crain et al. (Ecology Letters, 11, 2008: 1304) to determine the prevalence of synergistic, antagonistic, and additive interactions. Compared to their original analysis, we report differences in the representation of interaction classes by interaction type and we document examples of mitigating synergism, highlighting the importance of incorporating individual stressor effect directions in the determination of synergisms and antagonisms. This is particularly pertinent given a general bias in ecology toward investigating and reporting adverse multiple stressor effects (double negative). We emphasize the need for reconsideration by the ecological community of the interpretation of synergism and antagonism in situations where individual stressor effects oppose each other or where cumulative effects are reversed and enhanced.

Multiple Stressors in Agricultural Streams: A Mesocosm Study of Interactions among Raised Water Temperature, Sediment Addition and Nutrient Enrichment

Changes to land use affect streams through nutrient enrichment, increased inputs of sediment and, where riparian vegetation has been removed, raised water temperature. We manipulated all three stressors in experimental streamside channels for 30 days and determined the individual and pair-wise combined effects on benthic invertebrate and algal communities and on leaf decay, a measure of ecosystem functioning. We added nutrients (phosphorus+nitrogen; high, intermediate, natural) and/or sediment (grain size 0.2 mm; high, intermediate, natural) to 18 channels supplied with water from a nearby stream. Temperature was increased by 1.4°C in half the channels, simulating the loss of upstream and adjacent riparian shade. Sediment affected 93% of all biological response variables (either as an individual effect or via an interaction with another stressor) generally in a negative manner, while nutrient enrichment affected 59% (mostly positive) and raised temperature 59% (mostly positive). More of the algal components of the community responded to stressors acting individually than did invertebrate components, whereas pair-wise stressor interactions were more common in the invertebrate community. Stressors interacted often and in a complex manner, with interactions between sediment and temperature most common. Thus, the negative impact of high sediment on taxon richness of both algae and invertebrates was stronger at raised temperature, further reducing biodiversity. In addition, the decay rate of leaf material (strength loss) accelerated with nutrient enrichment at ambient but not at raised temperature. A key implication of our findings for resource managers is that the removal of riparian shading from streams already subjected to high sediment inputs, or land-use changes that increase erosion or nutrient runoff in a landscape without riparian buffers, may have unexpected effects on stream health. We highlight the likely importance of intact or restored buffer strips, both in reducing sediment input and in maintaining cooler water temperatures.

Climate warming and agricultural stressors interact to determine stream macroinvertebrate community dynamics.

Global climate change is likely to modify the ecological consequences of currently acting stressors, but potentially important interactions between climate warming and land-use related stressors remain largely unknown. Agriculture affects streams and rivers worldwide, including via nutrient enrichment and increased fine sediment input. We manipulated nutrients (simulating agricultural run-off) and deposited fine sediment (simulating agricultural erosion) (two levels each) and water temperature (eight levels, 0-6°C above ambient) simultaneously in 128 streamside mesocosms to determine the individual and combined effects of the three stressors on macroinvertebrate community dynamics (community composition and body size structure of benthic, drift and insect emergence assemblages). All three stressors had pervasive individual effects, but in combination often produced additive or antagonistic outcomes. Changes in benthic community composition showed a complex interplay among habitat quality (with or without sediment), resource availability (with or without nutrient enrichment) and the behavioural/physiological tendency to drift or emerge as temperature rose. The presence of sediment and raised temperature both resulted in a community of smaller organisms. Deposited fine sediment strongly increased the propensity to drift. Stressor effects were most prominent in the benthic assemblage, frequently reflected by opposite patterns in individuals quitting the benthos (in terms of their propensity to drift or emerge). Of particular importance is that community measures of stream health routinely used around the world (taxon richness, EPT richness and diversity) all showed complex three-way interactions, with either a consistently stronger temperature response or a reversal of its direction when one or both agricultural stressors were also in operation. The negative effects of added fine sediment, which were often stronger at raised temperatures, suggest that streams already impacted by high sediment loads may be further degraded under a warming climate. However, the degree to which this will occur may also depend on in-stream nutrient conditions.

Altitudinal patterns of vegetation, flora, life forms, and environments in the alpine zone of the Fiord Ecological Region, New Zealand

Abstract The altitudinal zonation patterns of vegetation structure, vascular flora, and life/growth forms were comprehensively assessed in relation to temperature and soil factors from treeline (1040 m) to the high‐alpine summit of Mt Burns (1645 m) in southeastern Fiord Ecological Region. We tested Körners hypothesis which stipulates that the physiognomic zonation pattern: treeline, shrub line, tussockline, and beyond, is driven mainly by increased decoupling between the ambient temperature and that experienced directly by plants in relation to proximity of their canopy to the ground. This hypothesis is generally supported, particularly with replacement of the tussock life form by dwarfed, mostly cushion species, at the low‐ to high‐alpine zone transition. The soil pattern appears to be more of a response to, rather than a driver of, the alpine vegetation pattern, including a localised area of frost‐active solifluc‐tion terraces. The Nothofagus menziesii treeline conformed to the “warmest month” model and also with a worldwide growing season mean (7.15°C) of 5.5–7.5°C. We stress the closer analogy in the overall alpine zonation pattern in this region of oceanic New Zealand to that of the tropical high mountains and other oceanic regions, than with the temperate Northern Hemisphere continental mountains.

Climate change and multiple stressors in small tropical streams

Despite the importance of small tropical streams for maintaining freshwater biodiversity and providing essential ecosystem services to humans, relatively few studies have investigated multiple-stressor effects of climate and land-use change on these ecosystems, and how these effects may interact. To illustrate these knowledge gaps, we reviewed the current state of knowledge regarding the ecological impacts of climate change and catchment land use on small tropical streams. We consider the effects of predicted changes in streamflow dynamics and water temperatures on water chemistry, habitat structure, aquatic biota, and ecosystem processes. We highlight the pervasive individual effects of climate and land-use change on algal, macroinvertebrate, and fish communities, and in stream metabolism and decomposition processes. We also discuss potential responses of tropical streams in a multiple-stressor scenario, considering higher temperatures and shifts in hydrological dynamics. Finally, we identify six key knowledge gaps in the ecology of low-order tropical streams and indicate future research directions that may improve catchment management in the tropics to help alleviate climate-change impacts and biodiversity losses.

Describing and understanding behavioral responses to multiple stressors and multiple stimuli

Summary Understanding the effects of environmental change on natural ecosystems is a major challenge, particularly when multiple stressors interact to produce unexpected “ecological surprises” in the form of complex, nonadditive effects that can amplify or reduce their individual effects. Animals often respond behaviorally to environmental change, and multiple stressors can have both population‐level and community‐level effects. However, the individual, not combined, effects of stressors on animal behavior are commonly studied. There is a need to understand how animals respond to the more complex combinations of stressors that occur in nature, which requires a systematic and rigorous approach to quantify the various potential behavioral responses to the independent and interactive effects of stressors. We illustrate a robust, systematic approach for understanding behavioral responses to multiple stressors based on integrating schemes used to quantitatively classify interactions in multiple‐stressor research and to qualitatively view interactions between multiple stimuli in behavioral experiments. We introduce and unify the two frameworks, highlighting their conceptual and methodological similarities, and use four case studies to demonstrate how this unification could improve our interpretation of interactions in behavioral experiments and guide efforts to manage the effects of multiple stressors. Our unified approach: (1) provides behavioral ecologists with a more rigorous and systematic way to quantify how animals respond to interactions between multiple stimuli, an important theoretical advance, (2) helps us better understand how animals behave when they encounter multiple, potentially interacting stressors, and (3) contributes more generally to the understanding of “ecological surprises” in multiple stressors research.

Multiple-stressor effects on stream macroinvertebrate communities: A mesocosm experiment manipulating salinity, fine sediment and flow velocity

Stream ecosystems are impacted by multiple stressors worldwide. Recent studies have shown that the effects of multiple stressors are often complex and difficult to predict based on the effects of single stressors. More research is needed to understand stressor impacts on stream communities and to design appropriate counteractions. We carried out an outdoor mesocosm experiment to assess single and interactive multiple-stressor effects on stream macroinvertebrates in a setup with controlled application of three globally important stressors, namely, reduced stream flow velocity, deposition of fine sediment and increased chloride concentration in a full-factorial design. Each mesocosm comprised three compartments (channel substratum, leaf litter bag and drift net) that were individually analyzed and also compared. We identified 102,501 specimens in total (mainly to family level), 36.5% of which were found in the substratum, 60.6% in litter bags and 2.9% in the drift. Added fine sediment and reduced flow velocity had strong negative single-stressor effects on the abundances of EPT taxa, i.e. Ephemeroptera (mayflies), Plecoptera (stoneflies) and Trichoptera (caddisflies), and a positive effect on chironomid abundances in the substratum. Increased salt concentration reduced abundances of Ephemeroptera. Chironomids migrated from litter bag to channel substratum when water velocity was reduced and Leptophlebiidae in the opposite direction when sediment was added. All three stressors caused higher drift propensities, especially added fine sediment. Both additive and complex multiple-stressor effects were common. A complex three-way interaction affected EPT richness in the substratum, demonstrating the need to evaluate higher-order interactions for more than two stressors. Our results add further evidence that multiple-stressor interactions, notably increased salinity with other stressors, affect a variety of invertebrate taxa across different habitats of stream communities. The results have direct implications for water management as they highlight the need to re-evaluate defined salinity thresholds in the context of multiple-stressor interactions.

Individual and combined effects of fine sediment and glyphosate herbicide on invertebrate drift and insect emergence: a stream mesocosm experiment

Pesticides and deposited fine sediment have been associated independently with changes in relative abundance and number of sensitive species in aquatic ecosystems, but the interplay between these stressors in agricultural streams is poorly understood. We used a 28-d experiment in outdoor streamside mesocosms to examine the effects of varying levels of fine sediment and a glyphosate-based herbicide on 2 important aspects of macroinvertebrate community dynamics, invertebrate drift and adult insect emergence. We applied 4 levels of each stressor in a full factorial, repeated-measures design (4 glyphosate × 4 sediment levels × 2 replicates of each treatment combination). We focused on the propensities of the invertebrates to drift or emerge (number drifting per mesocosm/benthic individuals per m2). Sediment addition affected drift propensities of 4 of the 10 most common invertebrate taxa, community-level measures of drift (total taxon and Ephemeroptera, Plecoptera, Trichoptera [EPT] richness) and adult emergence (total propensity and taxon richness), whereas glyphosate addition affected drift propensity of only 1 taxon. These results suggest that glyphosate entering streams during terrestrial herbicide operations may be less problematic for aquatic invertebrate community dynamics than fine sediment from catchment erosion. No significant sediment × glyphosate interaction was detected for any individual taxon drift propensity or community-level drift or emergence measure, indicating that the 2 stressors acted additively, rather than synergistically or antagonistically. The dynamic measures (invertebrate drift and adult insect emergence propensities) often showed the opposite pattern compared to benthic invertebrate densities in the same experiment, a result highlighting the value of using dynamic aspects of stream invertebrate communities to identify mechanisms underlying stressor effects on benthic standing stocks.

High-throughput amplicon sequencing and stream benthic bacteria: identifying the best taxonomic level for multiple-stressor research

Disentangling the individual and interactive effects of multiple stressors on microbial communities is a key challenge to our understanding and management of ecosystems. Advances in molecular techniques allow studying microbial communities in situ and with high taxonomic resolution. However, the taxonomic level which provides the best trade-off between our ability to detect multiple-stressor effects versus the goal of studying entire communities remains unknown. We used outdoor mesocosms simulating small streams to investigate the effects of four agricultural stressors (nutrient enrichment, the nitrification inhibitor dicyandiamide (DCD), fine sediment and flow velocity reduction) on stream bacteria (phyla, orders, genera, and species represented by Operational Taxonomic Units with 97% sequence similarity). Community composition was assessed using amplicon sequencing (16S rRNA gene, V3-V4 region). DCD was the most pervasive stressor, affecting evenness and most abundant taxa, followed by sediment and flow velocity. Stressor pervasiveness was similar across taxonomic levels and lower levels did not perform better in detecting stressor effects. Community coverage decreased from 96% of all sequences for abundant phyla to 28% for species. Order-level responses were generally representative of responses of corresponding genera and species, suggesting that this level may represent the best compromise between stressor sensitivity and coverage of bacterial communities.

Advancing understanding and prediction in multiple stressor research through a mechanistic basis for null models

Global environmental change is driven by multiple anthropogenic stressors. Conservation and restoration require understanding the individual and joint action of these stressors to evaluate and prioritize management measures. To date, most studies on multiple stressor effects have sought to identify potential stressor interactions, defined as deviations from null models, and related meta-analyses have focused on quantifying the relative proportion of stressor interactions across studies. These studies have provided valuable insights about the complexity of multiple stressor effects, but remain largely devoid of a theoretical framework for null model selection and prediction of effects. We suggest that multiple stressor research would benefit by (1) integrating and developing additional null models and (2) selecting null models based on their mechanistic assumptions of the stressor mode of action and organism sensitivities as well as stressor-effect relationships for individuals and populations. We present a range of null models and outline their underlying assumptions and application in multiple stressor research. Moving beyond mere description requires multiple stressor research to shift its focus from identifying statistically significant interactions to the use and development of mechanistic (null) models. Justified selection of the appropriate null model is a first step to achieve this.