Detecting and interpreting higher-order interactions in ecological communities.

When species simultaneously compete with two or more species of competitor, higher-order interactions (HOIs) can lead to emergent properties not present when species interact in isolated pairs. To extend ecological theory to multi-competitor communities, ecologists must confront the challenges of measuring and interpreting HOIs in models of competition fit to data from nature. Such efforts are hindered by the fact that different studies use different definitions, and these definitions have unclear relationships to one another. Here, we propose a distinction between 'soft' HOIs, which identify possible interaction modification by competitors, and 'hard' HOIs, which identify interactions uniquely emerging in systems with three or more competitors. We show how these two classes of HOI differ in their motivation and interpretation, as well as the tests one uses to identify them in models fit to data. We then show how to operationalise this structure of definitions by analysing the results of a simulated competition experiment underlain by a consumer resource model. In the course of doing so, we clarify the challenges of interpreting HOIs in nature, and suggest a more precise framing of this research endeavour to catalyse further investigations.

Author Correction: Leaf nutrients, not specific leaf area, are consistent indicators of elevated nutrient inputs.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Climate change, snow mold and the Bromus tectorum invasion: mixed evidence for release from cold weather pathogens.

Climate change is reducing the depth and duration of winter snowpack, leading to dramatic changes in the soil environment with potentially important ecological consequences. Previous experiments in the Intermountain West of North America indicated that loss of snowpack increases survival and population growth rates of the invasive annual grass Bromus tectorum; however, the underlying mechanism is unknown. We hypothesized that reduced snowpack might promote B. tectorum population growth by decreasing damage from snow molds, a group of subnivean fungal pathogens. To test this hypothesis, we conducted greenhouse and field experiments to investigate the interaction between early snowmelt and either fungicide addition or snow mold infection of B. tectorum. The greenhouse experiment confirmed that the snow mold Microdochium nivale can cause mortality of B. tectorum seedlings. In the field experiment, early snowmelt and fungicide application both increased B. tectorum survival, but their effects did not interact, and snow mold inoculation had no effect on survival. We did find interactive effects of snowmelt and fungal treatments on B. tectorum seed production: with ambient snowpack, M. nivale inoculation reduced seed production and fungicide increased it, whereas in the early snowmelt treatment seed production was high regardless of fungal treatment. However, treatment effects on seed production did not translate directly to overall population growth, which did not respond to the snow melt by fungal treatment interaction. Based on our mixed results, the hypothesis that reduced snowpack may increase B. tectorum fitness by limiting the effects of plant pathogens deserves further investigation.

Leaf nutrients, not specific leaf area, are consistent indicators of elevated nutrient inputs.

Leaf traits are frequently measured in ecology to provide a 'common currency' for predicting how anthropogenic pressures impact ecosystem function. Here, we test whether leaf traits consistently respond to experimental treatments across 27 globally distributed grassland sites across 4 continents. We find that specific leaf area (leaf area per unit mass)-a commonly measured morphological trait inferring shifts between plant growth strategies-did not respond to up to four years of soil nutrient additions. Leaf nitrogen, phosphorus and potassium concentrations increased in response to the addition of each respective soil nutrient. We found few significant changes in leaf traits when vertebrate herbivores were excluded in the short-term. Leaf nitrogen and potassium concentrations were positively correlated with species turnover, suggesting that interspecific trait variation was a significant predictor of leaf nitrogen and potassium, but not of leaf phosphorus concentration. Climatic conditions and pretreatment soil nutrient levels also accounted for significant amounts of variation in the leaf traits measured. Overall, we find that leaf morphological traits, such as specific leaf area, are not appropriate indicators of plant response to anthropogenic perturbations in grasslands.

The response of big sagebrush (Artemisia tridentata) to interannual climate variation changes across its range.

Understanding how annual climate variation affects population growth rates across a species' range may help us anticipate the effects of climate change on species distribution and abundance. We predict that populations in warmer or wetter parts of a species' range should respond negatively to periods of above average temperature or precipitation, respectively, whereas populations in colder or drier areas should respond positively to periods of above average temperature or precipitation. To test this, we estimated the population sensitivity of a common shrub species, big sagebrush (Artemisia tridentata), to annual climate variation across its range. Our analysis includes 8,175 observations of year-to-year change in sagebrush cover or production from 131 monitoring sites in western North America. We coupled these observations with seasonal weather data for each site and analyzed the effects of spring through fall temperatures and fall through spring accumulated precipitation on annual changes in sagebrush abundance. Sensitivity to annual temperature variation supported our hypothesis: years with above average temperatures were beneficial to sagebrush in colder locations and detrimental to sagebrush in hotter locations. In contrast, sensitivity to precipitation did not change significantly across the distribution of sagebrush. This pattern of responses suggests that regional abundance of this species may be more limited by temperature than by precipitation. We also found important differences in how the ecologically distinct subspecies of sagebrush responded to the effects of precipitation and temperature. Our model predicts that a short-term temperature increase could produce an increase in sagebrush cover at the cold edge of its range and a decrease in cover at the warm edge of its range. This prediction is qualitatively consistent with predictions from species distribution models for sagebrush based on spatial occurrence data, but it provides new mechanistic insight and helps estimate how much and how fast sagebrush cover may change within its range.

Ecosystem functional response across precipitation extremes in a sagebrush steppe.

BACKGROUND: Precipitation is predicted to become more variable in the western United States, meaning years of above and below average precipitation will become more common. Periods of extreme precipitation are major drivers of interannual variability in ecosystem functioning in water limited communities, but how ecosystems respond to these extremes over the long-term may shift with precipitation means and variances. Long-term changes in ecosystem functional response could reflect compensatory changes in species composition or species reaching physiological thresholds at extreme precipitation levels. METHODS: We conducted a five year precipitation manipulation experiment in a sagebrush steppe ecosystem in Idaho, United States. We used drought and irrigation treatments (approximately 50% decrease/increase) to investigate whether ecosystem functional response remains consistent under sustained high or low precipitation. We recorded data on aboveground net primary productivity (ANPP), species abundance, and soil moisture. We fit a generalized linear mixed effects model to determine if the relationship between ANPP and soil moisture differed among treatments. We used nonmetric multidimensional scaling to quantify community composition over the five years. RESULTS: Ecosystem functional response, defined as the relationship between soil moisture and ANPP, was similar among irrigation and control treatments, but the drought treatment had a greater slope than the control treatment. However, all estimates for the effect of soil moisture on ANPP overlapped zero, indicating the relationship is weak and uncertain regardless of treatment. There was also large spatial variation in ANPP within-years, which contributes to the uncertainty of the soil moisture effect. Plant community composition was remarkably stable over the course of the experiment and did not differ among treatments. DISCUSSION: Despite some evidence that ecosystem functional response became more sensitive under sustained drought conditions, the response of ANPP to soil moisture was consistently weak and community composition was stable. The similarity of ecosystem functional responses across treatments was not related to compensatory shifts at the plant community level, but instead may reflect the insensitivity of the dominant species to soil moisture. These species may be successful precisely because they have evolved life history strategies that buffer them against precipitation variability.

Multi-model comparison highlights consistency in predicted effect of warming on a semi-arid shrub.

A number of modeling approaches have been developed to predict the impacts of climate change on species distributions, performance, and abundance. The stronger the agreement from models that represent different processes and are based on distinct and independent sources of information, the greater the confidence we can have in their predictions. Evaluating the level of confidence is particularly important when predictions are used to guide conservation or restoration decisions. We used a multi-model approach to predict climate change impacts on big sagebrush (Artemisia tridentata), the dominant plant species on roughly 43 million hectares in the western United States and a key resource for many endemic wildlife species. To evaluate the climate sensitivity of A. tridentata, we developed four predictive models, two based on empirically derived spatial and temporal relationships, and two that applied mechanistic approaches to simulate sagebrush recruitment and growth. This approach enabled us to produce an aggregate index of climate change vulnerability and uncertainty based on the level of agreement between models. Despite large differences in model structure, predictions of sagebrush response to climate change were largely consistent. Performance, as measured by change in cover, growth, or recruitment, was predicted to decrease at the warmest sites, but increase throughout the cooler portions of sagebrush's range. A sensitivity analysis indicated that sagebrush performance responds more strongly to changes in temperature than precipitation. Most of the uncertainty in model predictions reflected variation among the ecological models, raising questions about the reliability of forecasts based on a single modeling approach. Our results highlight the value of a multi-model approach in forecasting climate change impacts and uncertainties and should help land managers to maximize the value of conservation investments.

Direct effects dominate responses to climate perturbations in grassland plant communities.

Theory predicts that strong indirect effects of environmental change will impact communities when niche differences between competitors are small and variation in the direct effects experienced by competitors is large, but empirical tests are lacking. Here we estimate negative frequency dependence, a proxy for niche differences, and quantify the direct and indirect effects of climate change on each species. Consistent with theory, in four of five communities indirect effects are strongest for species showing weak negative frequency dependence. Indirect effects are also stronger in communities where there is greater variation in direct effects. Overall responses to climate perturbations are driven primarily by direct effects, suggesting that single species models may be adequate for forecasting the impacts of climate change in these communities.

Indirect Effects of Environmental Change in Resource Competition Models.

Anthropogenic environmental change can affect species directly by altering physiological rates or indirectly by changing competitive outcomes. The unknown strength of competition-mediated indirect effects makes it difficult to predict species abundances in the face of ongoing environmental change. Theory developed with phenomenological competition models shows that indirect effects are weak when coexistence is strongly stabilized, but these models lack a mechanistic link between environmental change and species performance. To extend existing theory, we examined the relationship between coexistence and indirect effects in mechanistic resource competition models. We defined environmental change as a change in resource supply points and quantified the resulting competition-mediated indirect effects on species abundances. We found that the magnitude of indirect effects increases in proportion to niche overlap. However, indirect effects also depend on differences in how competitors respond to the change in resource supply, an insight hidden in nonmechanistic models. Our analysis demonstrates the value of using niche overlap to predict the strength of indirect effects and clarifies the types of indirect effects that global change can have on competing species.

Shrubs as ecosystem engineers across an environmental gradient: effects on species richness and exotic plant invasion.

Ecosystem-engineering plants modify the physical environment and can increase species diversity and exotic species invasion. At the individual level, the effects of ecosystem engineers on other plants often become more positive in stressful environments. In this study, we investigated whether the community-level effects of ecosystem engineers also become stronger in more stressful environments. Using comparative and experimental approaches, we assessed the ability of a native shrub (Ericameria ericoides) to act as an ecosystem engineer across a stress gradient in a coastal dune in northern California, USA. We found increased coarse organic matter and lower wind speeds within shrub patches. Growth of a dominant invasive grass (Bromus diandrus) was facilitated both by aboveground shrub biomass and by growing in soil taken from shrub patches. Experimental removal of shrubs negatively affected species most associated with shrubs and positively affected species most often found outside of shrubs. Counter to the stress-gradient hypothesis, the effects of shrubs on the physical environment and individual plant growth did not increase across the established stress gradient at this site. At the community level, shrub patches increased beta diversity, and contained greater rarified richness and exotic plant cover than shrub-free patches. Shrub effects on rarified richness increased with environmental stress, but effects on exotic cover and beta diversity did not. Our study provides evidence for the community-level effects of shrubs as ecosystem engineers in this system, but shows that these effects do not necessarily become stronger in more stressful environments.

Trait-based tests of coexistence mechanisms.

Recent functional trait studies have shown that trait differences may favour certain species (environmental filtering) while simultaneously preventing competitive exclusion (niche partitioning). However, phenomenological trait-dispersion analyses do not identify the mechanisms that generate niche partitioning, preventing trait-based prediction of future changes in biodiversity. We argue that such predictions require linking functional traits with recognised coexistence mechanisms involving spatial or temporal environmental heterogeneity, resource partitioning and natural enemies. We first demonstrate the limitations of phenomenological approaches using simulations, and then (1) propose trait-based tests of coexistence, (2) generate hypotheses about which plant functional traits are likely to interact with particular mechanisms and (3) review the literature for evidence for these hypotheses. Theory and data suggest that all four classes of coexistence mechanisms could act on functional trait variation, but some mechanisms will be stronger and more widespread than others. The highest priority for future research is studies of interactions between environmental heterogeneity and trait variation that measure environmental variables at within-community scales and quantify species' responses to the environment in the absence of competition. Evidence that similar trait-based coexistence mechanisms operate in many ecosystems would simplify biodiversity forecasting and represent a rare victory for generality over contingency in community ecology.

Responses to invasion and invader removal differ between native and exotic plant groups in a coastal dune.

The spread of exotic, invasive species is a global phenomenon that is recognized as a major source of environmental change. Although many studies have addressed the effects of exotic plants on the communities they invade, few have quantified the effects of invader removal on plant communities, or considered the degree to which different plant groups vary in response to invasion and invader removal. We evaluated the effects of an exotic succulent, iceplant (Carpobrotus edulis), on a coastal dune plant community in northern California, as well as the community responses to its removal. To assess possible mechanisms by which iceplant affects other plants, we also evaluated its above- and belowground influences on the germination and growth of a dominant exotic annual grass, Bromus diandrus. We found that iceplant invasion was associated with reduced native plant cover as well as increased cover and density of some exotic plants-especially exotic annual grasses. However, iceplant removal did not necessarily lead to a reversal of these effects: removal increased the cover and density of both native and exotic species. We also found that B. diandrus grown in iceplant patches, or in soil where iceplant had been removed, had poorer germination and growth than B. diandrus grown in soil not influenced by iceplant. This suggests that the influence of iceplant on this dune plant community occurs, at least in part, due to belowground effects, and that these effects remain after iceplant has been removed. Our study demonstrates the importance of considering how exotic invasive plants affect not only native species, but also co-occurring exotic taxa. It also shows that combining observational studies with removal experiments can lead to important insights into the influence of invaders and the mechanisms of their effects.