Plant interaction networks reveal the limits of our understanding of diversity maintenance.

Species interactions are key drivers of biodiversity and ecosystem stability. Current theoretical frameworks for understanding the role of interactions make many assumptions which unfortunately, do not always hold in natural, diverse communities. This mismatch extends to annual plants, a common model system for studying coexistence, where interactions are typically averaged across environmental conditions and transitive competitive hierarchies are assumed to dominate. We quantify interaction networks for a community of annual wildflowers in Western Australia across a natural shade gradient at local scales. Whilst competition dominated, intraspecific and interspecific facilitation were widespread in all shade categories. Interaction strengths and directions varied substantially despite close spatial proximity and similar levels of local species richness, with most species interacting in different ways under different environmental conditions. Contrary to expectations, all networks were predominantly intransitive. These findings encourage us to rethink how we conceive of and categorize the mechanisms driving biodiversity in plant systems.

What Can Evolutionary History Tell Us about the Functioning of Ecological Communities? The ASN Presidential Debate.

AbstractIn January 2018, Sharon Strauss, then president of the American Society of Naturalists, organized a debate on the following topic: does evolutionary history inform the current functioning of ecological communities? The debaters-Ives, Lau, Mayfield, and Tobias-presented pro and con arguments, caricatured in standard debating format. Numerous examples show that both recent microevolutionary and longer-term macroevolutionary history are important to the ecological functioning of communities. On the other hand, many other examples illustrate that the evolutionary history of communities or community members does not influence ecological function, or at least not very much. This article aims to provide a provocative discussion of the consistent and conflicting patterns that emerge in the study of contemporary and historical evolutionary influences on community function, as well as to identify questions for further study. It is intended as a thought-provoking exercise to explore this complex field, specifically addressing (1) key assumptions and how they can lead us astray and (2) issues that need additional study. The debaters all agree that evolutionary history can inform us about at least some aspects of community function. The underlying question at the root of the debate, however, is how the fields of ecology and evolution can most profitably collaborate to provide a deeper and broader understanding of ecological communities.

Weak evidence of trade-offs modulated by seed mass among a guild of closely related winter annuals.

Plant-plant interactions are integral to the establishment and persistence of diversity in plant communities. For annual plant species that depend on seeds to regenerate, seed characteristics that confer fitness advantages may mediate processes such as plant-plant interactions. Seed mass is known to vary widely and has been shown to associate with species' differences in stress tolerance and competitive effects. However, understanding of how seed mass influences species' responses to competition is less well understood. Using natural assemblages of six closely related annual plant species in Western Australia, we implemented a thinning study to assess how seed mass influences the outcomes of plant-plant interactions. We found relatively weak evidence for competition or facilitation among species. Our strongest results indicated that heavy-seeded species had lower survivorship than light-seeded species when interacting with heterospecifics. Seed mass was also negatively related to overall survival, counter to expectations. These findings indicate some evidence for trade-offs mediated by seed mass in this system. However, we acknowledge that other factors may have influenced our results, such as the use of natural assemblages (rather than using sowing experiments) and the presence of important small-scale environmental variation not captured with our choice of abiotic variables. Further research is required to clarify the role of seed mass in this diverse annual system, ideally including many focal species, and using sowing experiments.

Restoration ecology through the lens of coexistence theory.

Advances in restoration ecology are needed to guide ecological restoration in a variable and changing world. Coexistence theory provides a framework for how variability in environmental conditions and species interactions affects species success. Here, we conceptually link coexistence theory and restoration ecology. First, including low-density growth rates (LDGRs), a classic metric of coexistence, can improve abundance-based restoration goals, because abundances are sensitive to initial treatments and ongoing variability. Second, growth-rate partitioning, developed to identify coexistence mechanisms, can improve restoration practice by informing site selection and indicating necessary interventions (e.g., site amelioration or competitor removal). Finally, coexistence methods can improve restoration assessment, because initial growth rates indicate trajectories, average growth rates measure success, and growth partitioning highlights interventions needed in future.

Optimal restoration for pollination services increases forest cover while doubling agricultural profits.

Pollinators are currently facing dramatic declines in abundance and richness across the globe. This can have profound impacts on agriculture, as 75% of globally common food crops benefit from pollination services. As many native bee species require natural areas for nesting, restoration efforts within croplands may be beneficial to support pollinators and enhance agricultural yields. Yet, restoration can be challenging to implement due to large upfront costs and the removal of land from production. Designing sustainable landscapes will require planning approaches that include the complex spatiotemporal dynamics of pollination services flowing from (restored) vegetation into crops. We present a novel planning framework to determine the best spatial arrangement for restoration in agricultural landscapes while accounting for yield improvements over 40 years following restoration. We explored a range of production and conservation goals using a coffee production landscape in Costa Rica as a case study. Our results show that strategic restoration can increase forest cover by approximately 20% while doubling collective landholder profits over 40 years, even when accounting for land taken out of production. We show that restoration can provide immense economic benefits in the long run, which may be pivotal to motivating local landholders to undertake conservation endeavours in pollinator-dependent croplands.

Patterns of frequency and density dependence are highly variable in diverse annual flowering plant communities.

Applications of ecological theory to natural communities often assume that competitive, negative density-dependent processes are the only type of interaction important for diversity maintenance. Recent advances suggest that positive interactions within trophic levels (e.g., plant-plant) may also affect plant coexistence. Though positive plant-plant interactions theoretically might result in positive or nonmonotonic frequency or density dependence (FD/DD), less is known about how commonly these patterns occur or which ecological processes might result in such patterns in natural plant communities. In this study we tested for signals of variable frequency and density dependence in annual flowering plant communities in Western Australia and searched for evidence that interactions among plants during flowering might induce positive or nonmonotonic FD/DD in flowering plants. Using four common annual wildflower species, we ask if plant fecundity exhibited positive or nonmonotonic FD/DD and if pollinator-mediated plant-plant interactions during flowering change patterns of FD/DD relative to pollinator-independent plant interactions. Three species exhibited nonmonotonic (hump-shaped) density dependence, and only one species experienced strictly negative density dependence. Each species exhibited a different pattern of frequency dependence (positive, negative, weakly nonmonotonic, and no detectable frequency dependence). Pollinator-mediated plant-plant interactions during flowering induced both nonmonotonic density dependence and negative frequency dependence in one species. Importantly, the extent of variation in FD/DD observed in our study brings into question the dominance of negative density and frequency dependence in theory, suggesting instead that demographic responses of plants to their communities fall along a continuum of possible density- and frequency-dependent patterns.

Ecology: Lifting the curtain on higher-order interactions.

Higher-order interactions - the modification of interactions between a species pair by a third - remain poorly understood in nature. A new study manipulates pairwise and higher-order interactions in the field, offering exciting new insights into how higher-order interactions contribute to coexistence.

Positive effects of exotic species dampened by neighborhood heterogeneity.

It is well known that species interactions between exotic and native species are important for determining the success of biological invasions and how influential exotic species become in invaded communities. The strength and type of interactions between species can substantially vary, however, from negative and detrimental to minimal or even positive. Increasing evidence from the literature shows that exotic species have positive interactions with native species more often than originally thought. Gaps in our theory for how population growth is limited when interactions are positive, however, restrict our understanding of the mechanisms by which exotic "facilitators" contribute to diversity maintenance in invaded systems. Here, we quantified interactions between seven native and four exotic (established nonnative) common annual plant species in the highly diverse, York Gum woodlands of Western Australia. We used a Bayesian demographic modeling approach that allowed for interaction coefficients to be positive or negative, and explored key sources of variation in species responses to native and exotic neighbors at per capita (individual) and neighborhood levels. We observed positive per capita effects from exotic neighbors on exotic focal species as well as on several native focal species. However, all focal species were, on average, inhibited by their interaction neighborhood, when the variance in identity and abundance of observed neighbors was considered. At the neighborhood scale, exotic species were found to suppress all focal species, particularly those with high intrinsic fecundity. Our study demonstrates that within-neighborhood heterogeneity can regulate per capita positive effects of invaders, limiting runaway population growth of both natives and exotic invaders.

Accounting for demographic uncertainty increases predictions for species coexistence: A case study with annual plants.

Natural systems contain more complexity than is accounted for in models of modern coexistence theory. Coexistence modelling often disregards variation arising from stochasticity in biological processes, heterogeneity among individuals and plasticity in trait values. However, these unaccounted-for sources of uncertainty are likely to be ecologically important and have the potential to impact estimates of coexistence. We applied a Bayesian modelling framework to data from an annual plant community in Western Australia to propagate uncertainty in coexistence outcomes using the invasion criterion and ratio of niche to fitness differences. We found accounting for this uncertainty altered predictions of coexistence versus competitive exclusion for 3 out of 14 species pairs and yielded a probability of priority effects for an additional species pair. The propagation of uncertainty arising from sources of biological complexity improves our ability to predict coexistence more accurately in natural systems.

Drivers of Acacia and Eucalyptus growth rate differ in strength and direction in restoration plantings across Australia.

Functional traits are proxies for a species' ecology and physiology and are often correlated with plant vital rates. As such they have the potential to guide species selection for restoration projects. However, predictive trait-based models often only explain a small proportion of plant performance, suggesting that commonly measured traits do not capture all important ecological differences between species. Some residual variation in vital rates may be evolutionarily conserved and captured using taxonomic groupings alongside common functional traits. We tested this hypothesis using growth rate data for 17,299 trees and shrubs from 80 species of Eucalyptus and 43 species of Acacia, two hyper-diverse and co-occurring genera, collected from 497 neighborhood plots in 137 Australian mixed-species revegetation plantings. We modeled relative growth rates of individual plants as a function of environmental conditions, species-mean functional traits, and neighbor density and diversity, across a moisture availability gradient. We then assessed whether the strength and direction of these relationships differed between the two genera. We found that the inclusion of genus-specific relationships offered a significant but modest improvement to model fit (1.6%-1.7% greater R2 than simpler models). More importantly, almost all correlates of growth rate differed between Eucalyptus and Acacia in strength, direction, or how they changed along the moisture gradient. These differences mapped onto physiological differences between the genera that were not captured solely by measured functional traits. Our findings suggest taxonomic groupings can capture or mediate variation in plant performance missed by common functional traits. The inclusion of taxonomy can provide a more nuanced understanding of how functional traits interact with abiotic and biotic conditions to drive plant performance, which may be important for constructing trait-based frameworks to improve restoration outcomes.

Disentangling key species interactions in diverse and heterogeneous communities: A Bayesian sparse modelling approach.

Modelling species interactions in diverse communities traditionally requires a prohibitively large number of species-interaction coefficients, especially when considering environmental dependence of parameters. We implemented Bayesian variable selection via sparsity-inducing priors on non-linear species abundance models to determine which species interactions should be retained and which can be represented as an average heterospecific interaction term, reducing the number of model parameters. We evaluated model performance using simulated communities, computing out-of-sample predictive accuracy and parameter recovery across different input sample sizes. We applied our method to a diverse empirical community, allowing us to disentangle the direct role of environmental gradients on species' intrinsic growth rates from indirect effects via competitive interactions. We also identified a few neighbouring species from the diverse community that had non-generic interactions with our focal species. This sparse modelling approach facilitates exploration of species interactions in diverse communities while maintaining a manageable number of parameters.

Variable seed bed microsite conditions and light influence germination in Australian winter annuals.

Environmentally cued germination may play an important role in promoting coexistence in Mediterranean annual plant systems if it causes niche differentiation across heterogeneous microsite conditions. In this study, we tested how microsite conditions experienced by seeds in the field and light conditions in the laboratory influenced germination in 12 common annual plant species occurring in the understorey of the York gum-jam woodlands in southwest Western Australia. Specifically, we hypothesized that if germination promotes spatial niche differentiation, then we should observe species-specific germination responses to light. In addition, we hypothesized that species' laboratory germination response may depend on the microsite conditions experienced by seeds while buried. We tested the laboratory germination response of seeds under diurnally fluctuating light and complete darkness, which were collected from microsites spanning local-scale environmental gradients known to influence community structure in this system. We found that seeds of 6 out of the 12 focal species exhibited significant positive germination responses to light, but that the magnitude of these responses varied greatly with the relative light requirement for germination ranging from 0.51 to 0.86 for these species. In addition, germination increased significantly across a gradient of canopy cover for two species, but we found little evidence to suggest that species' relative light requirement for germination varied depending on seed bank microsite conditions. Our results suggest that variability in light availability may promote coexistence in this system and that the microsite conditions seeds experience in the intra-growing season period can further nuance species germination behaviour.

Non-additive biotic interactions improve predictions of tropical tree growth and impact community size structure.

Growth in individual size or biomass is a key demographic component in population models, with wide-ranging applications from quantifying species performance across abiotic or biotic conditions to assessing landscape-level dynamics under global change. In forest ecology, the responses of tree growth to biotic interactions are widely held to be crucial for understanding forest diversity, function, and structure. To date, most studies on plant-plant interactions only examine the additive competitive or facilitative interactions between species pairs; however, there is increasing evidence of non-additive, higher-order interactions (HOIs) impacting species demographic rates. When HOIs are present, the dynamics of a multispecies community cannot be fully understood or accurately predicted solely from pairwise outcomes because of how additional species "interfere" with the direct, pairwise interactions. Such HOIs should be particularly prevalent when species show non-linear functional responses to resource availability and resource-acquisition traits themselves are density dependent. With this in mind, we used data from a tropical secondary forest-a system that fulfills both of these conditions-to build an ontogenetic diameter growth model for individuals across 10 woody-plant species. We allowed both direct and indirect interactions within communities to influence the species-specific growth parameters in a generalized Lotka-Volterra model. Specifically, indirect interactions entered the model as higher-order quadratic terms, i.e., non-additive effects of conspecific and heterospecific neighbor size on the focal individual's growth. For the whole community and for four out of 10 focal species, the model that included HOIs had more statistical support than the model that included only direct interactions, despite the former containing a far greater number of parameters. HOIs had comparable effect sizes to direct interactions, and tended to further reduce the diameter growth rates of most species beyond what direct interactions had already reduced. In a simulation of successional stand dynamics, the inclusion of HOIs led to rank swaps in species' diameter hierarchies, even when community-level size distributions remained qualitatively similar. Our study highlights the implications, and discusses possible mechanisms, of non-additive density dependence in highly diverse and light-competitive tropical forests.

Beyond direct neighbourhood effects: higher-order interactions improve modelling and predicting tree survival and growth.

It is known that biotic interactions are the key to species coexistence and maintenance of species diversity. Traditional studies focus overwhelmingly on pairwise interactions between organisms, ignoring complex higher-order interactions (HOIs). In this study, we present a novel method of calculating individual-level HOIs for trees, and use this method to test the importance of size- and distance-dependent individual-level HOIs to tree performance in a 25-ha temperate forest dynamic plot. We found that full HOI-inclusive models improved our ability to model and predict the survival and growth of trees, providing empirical evidence that HOIs strongly influence tree performance in this temperate forest. Specifically, assessed HOIs mitigate the competitive direct effects of neighbours on survival and growth of focal trees. Our study lays a foundation for future investigations of the prevalence and relative importance of HOIs in global forests and their impact on species diversity.

Identifying "Useful" Fitness Models: Balancing the Benefits of Added Complexity with Realistic Data Requirements in Models of Individual Plant Fitness.

AbstractDirect species interactions are commonly included in individual fitness models used for coexistence and local diversity modeling. Though widely considered important for such models, direct interactions alone are often insufficient for accurately predicting fitness, coexistence, or diversity outcomes. Incorporating higher-order interactions (HOIs) can lead to more accurate individual fitness models but also adds many model terms, which can quickly result in model overfitting. We explore approaches for balancing the trade-off between tractability and model accuracy that occurs when HOIs are added to individual fitness models. To do this, we compare models parameterized with data from annual plant communities in Australia and Spain, varying in the extent of information included about the focal and neighbor species. The best-performing models for both data sets were those that grouped neighbors based on origin status and life form, a grouping approach that reduced the number of model parameters substantially while retaining important ecological information about direct interactions and HOIs. Results suggest that the specific identity of focal or neighbor species is not necessary for building well-performing fitness models that include HOIs. In fact, grouping neighbors by even basic functional information seems sufficient to maximize model accuracy, an important outcome for the practical use of HOI-inclusive fitness models.

The evolution of niche overlap and competitive differences.

Competition can result in evolutionary changes to coexistence between competitors but there are no theoretical models that predict how the components of coexistence change during this eco-evolutionary process. Here we study the evolution of the coexistence components, niche overlap and competitive differences, in a two-species eco-evolutionary model based on consumer-resource interactions and quantitative genetic inheritance. Species evolve along a one-dimensional trait axis that allows for changes in both niche position and species intrinsic growth rates. There are three main results. First, the breadth of the environment has a strong effect on the dynamics, with broader environments leading to reduced niche overlap and enhanced coexistence. Second, coexistence often involves a reduction in niche overlap while competitive differences stay relatively constant or vice versa; in general changes in competitive differences maintain coexistence only when niche overlap remains constant. Large simultaneous changes in niche overlap and competitive difference often result in one of the species being excluded. Third, provided that the species evolve to a state where they coexist, the final niche overlap and competitive difference values are independent of the system's initial state, although they do depend on the model's parameters. The model suggests that evolution is often a destructive force for coexistence due to evolutionary changes in competitive differences, a finding that expands the paradox of diversity maintenance.

Aridity drives coordinated trait shifts but not decreased trait variance across the geographic range of eight Australian trees.

Large intraspecific functional trait variation strongly impacts many aspects of communities and ecosystems, and is the medium upon which evolution works. Yet intraspecific trait variation is inconsistent and hard to predict across traits, species and locations. We measured within-species variation in leaf mass per area (LMA), leaf dry matter content (LDMC), branch wood density (WD), and allocation to stem area vs leaf area in branches (branch Huber value (HV)) across the aridity range of seven Australian eucalypts and a co-occurring Acacia species to explore how traits and their variances change with aridity. Within species, we found consistent increases in LMA, LDMC and WD and HV with increasing aridity, resulting in consistent trait coordination across leaves and branches. However, this coordination only emerged across sites with large climate differences. Unlike trait means, patterns of trait variance with aridity were mixed across populations and species. Only LDMC showed constrained trait variation in more xeric species and drier populations that could indicate limits to plasticity or heritable trait variation. Our results highlight that climate can drive consistent within-species trait patterns, but that patterns might often be obscured by the complex nature of morphological traits, sampling incomplete species ranges or sampling confounded stress gradients.

Requirements for the spatial storage effect are weakly evident for common species in natural annual plant assemblages.

Coexistence in spatially varying environments is theorized to be promoted by a variety of mechanisms including the spatial storage effect. The spatial storage effect promotes coexistence when (1) species have unique vital rate responses to their spatial environment and, when abundant, (2) experience stronger competition in the environmental patches where they perform better. In a naturally occurring southwest Western Australian annual plant system, we conducted a neighbor removal experiment involving eleven focal species growing in high-abundance populations. Specifically, we measured species' fecundity across a variety of environmental gradients in both the presence and absence of neighbors. For the environmental variables that we measured, there was only limited evidence for species-specific responses to the environment, with a composite variable describing overstory cover and leaf litter cover being the best predictor of fecundity for a subset of focal species. In addition, although we found strong evidence for intraspecific competition, positive environment-competition covariance was only detected for one species. Thus, positive environment-competition covariance may not be as common as expected in populations of species growing at high abundance, at least when tested in natural assemblages. Our findings highlight the inherent limitations of using natural assemblages to study spatial coexistence mechanisms, and we urge empirical ecologists to take these limitations into account when designing future experiments.

Integrating the underlying structure of stochasticity into community ecology.

Stochasticity is a core component of ecology, as it underlies key processes that structure and create variability in nature. Despite its fundamental importance in ecological systems, the concept is often treated as synonymous with unpredictability in community ecology, and studies tend to focus on single forms of stochasticity rather than taking a more holistic view. This has led to multiple narratives for how stochasticity mediates community dynamics. Here, we present a framework that describes how different forms of stochasticity (notably demographic and environmental stochasticity) combine to provide underlying and predictable structure in diverse communities. This framework builds on the deep ecological understanding of stochastic processes acting at individual and population levels and in modules of a few interacting species. We support our framework with a mathematical model that we use to synthesize key literature, demonstrating that stochasticity is more than simple uncertainty. Rather, stochasticity has profound and predictable effects on community dynamics that are critical for understanding how diversity is maintained. We propose next steps that ecologists might use to explore the role of stochasticity for structuring communities in theoretical and empirical systems, and thereby enhance our understanding of community dynamics.

Looks can be deceiving: ecologically similar exotics have different impacts on a native competitor.

Exotic species are often predicted to successfully invade when their functional traits differ from species in recipient communities. Many studies have related trait differences among natives and invaders to competitive outcomes. Few studies, however, have tested whether functionally similar invaders have similar competitive impacts on natives. We investigated interactions in communities of a native annual forb Waitzia acuminata (Asteraceae) and two invasive annual grasses that are ecologically similar and co-occur in southwestern Australia. Using a combination of field and laboratory experiments and several performance measures, we assessed impacts of these grasses on W. acuminata. We also examined differences among species in their responses to intraspecific versus interspecific competition, including their frequency dependence. The two similar exotic grasses differed in interaction impacts, with one facilitating and the other suppressing the native. In general, intraspecific competition was stronger than interspecific competition for the native, while evidence of competition was weak for the exotics. These patterns may reflect that W. acuminata does well in these communities due to the combined impacts of stabilization and facilitation, whereas the exotics benefit from limited stabilization (mediated by their weak intraspecific competition) or weak interspecific competition with W. acuminata. We found divergent impacts of the exotic species despite their similar functional traits. We demonstrate that a native species may benefit from interactions with an exotic "benefactor" species, highlighting the potential importance of positive interactions in invaded communities. Our findings underscore the necessity of considering neutral and positive interactions in addition to competition in understanding invasion dynamics in real plant communities.