Assembly and response rules: two goals for predictive community ecology

Abstract. Assembly rules provide one possible unifying framework for community ecology. Given a species pool, and measured traits for each species, the objective is to specify which traits (and therefore which subset of species) will occur in a particular environment. Because the problem primarily involves traits and environments, answers should be generalizable to systems with very different taxonomic composition. In this context, the environment functions like a filter (or sieve) removing all species lacking specified combinations of traits. In this way, assembly rules are a community level analogue of natural selection. Response rules follow a similar process except that they transform a vector of species abundances to a new vector using the same information. Examples already exist from a range of habitats, scales, and kinds of organisms.     

The merging of community ecology and phylogenetic biology

The increasing availability of phylogenetic data, computing power and informatics tools has facilitated a rapid expansion of studies that apply phylogenetic data and methods to community ecology. Several key areas are reviewed in which phylogenetic information helps to resolve long-standing controversies in community ecology, challenges previous assumptions, and opens new areas of investigation. In particular, studies in phylogenetic community ecology have helped to reveal the multitude of processes driving community assembly and have demonstrated the importance of evolution in the assembly process. Phylogenetic approaches have also increased understanding of the consequences of community interactions for speciation, adaptation and extinction. Finally, phylogenetic community structure and composition holds promise for predicting ecosystem processes and impacts of global change. Major challenges to advancing these areas remain. In particular, determining the extent to which ecologically relevant traits are phylogenetically conserved or convergent, and over what temporal scale, is critical to understanding the causes of community phylogenetic structure and its evolutionary and ecosystem consequences. Harnessing phylogenetic information to understand and forecast changes in diversity and dynamics of communities is a critical step in managing and restoring the Earth's biota in a time of rapid global change.     

Sequentially assembled food webs and extremum principles in ecosystem ecology

1. Successional changes during sequential assembly of food webs were examined. This was carried out by numerical methods, drawing one species at a time from a species pool and obtaining the permanent (persistent) community emerging at each step. Interactions among species were based on some simple rules about body sizes of consumers and their prey, and community dynamics were described in terms of flows of biomass density. 2. Sequential assembly acted as a sieve on the communities, assembled communities having many properties different on average from those of feasible, stable communities taken at random from the species pools. 3. Time-series of community development were consistent with certain functions thought to go to an extremum (maximum or minimum) in ecosystem ecology, including a rapid early increase in net primary productivity and ascendency, although a clear trend in total biomass density was not evident and resilience decreased rather than increased. 4. In addition, more gradual changes in food web structure took place during succession to which the ecosystem goal functions were relatively insensitive. These changes included gradual increases in the number of species, invasion resistance, number of loops of length > 2 and number of prey species per consumer species. 5. We therefore argue that ecosystem and community dynamics can offer complementary insights into the process of ecological succession. The extremum principles of ecosystem ecology highlight some of the major properties of succession, whereas the community ecology sheds light on some more subtle changes taking place within the networks.     

Linking traits to species diversity and community structure in phytoplankton

In addition to answering Hutchinson’s question “Why are there so many species?”, we need to understand why certain species are found only under certain environmental conditions and not others. Trait-based approaches are being increasingly used in ecology to do just that: explain and predict species distributions along environmental gradients. These approaches can be successful in understanding the diversity and community structure of phytoplankton. Among major traits shaping phytoplankton distributions are resource utilization traits, morphological traits (with size being probably the most influential), grazer resistance traits, and temperature responses. We review these trait-based approaches and give examples of how trait data can explain species distributions in both freshwater and marine systems. We also outline new directions in trait-based approaches applied to phytoplankton such as looking simultaneously at trait and phylogenetic structure of phytoplankton communities and using adaptive dynamics models to predict trait evolution.     

How to make more out of community data? A conceptual framework and its implementation as models and software

Community ecology aims to understand what factors determine the assembly and dynamics of species assemblages at different spatiotemporal scales. To facilitate the integration between conceptual and statistical approaches in community ecology, we propose Hierarchical Modelling of Species Communities (HMSC) as a general, flexible framework for modern analysis of community data. While non‐manipulative data allow for only correlative and not causal inference, this framework facilitates the formulation of data‐driven hypotheses regarding the processes that structure communities. We model environmental filtering by variation and covariation in the responses of individual species to the characteristics of their environment, with potential contingencies on species traits and phylogenetic relationships. We capture biotic assembly rules by species‐to‐species association matrices, which may be estimated at multiple spatial or temporal scales. We operationalise the HMSC framework as a hierarchical Bayesian joint species distribution model, and implement it as R‐ and Matlab‐packages which enable computationally efficient analyses of large data sets. Armed with this tool, community ecologists can make sense of many types of data, including spatially explicit data and time‐series data. We illustrate the use of this framework through a series of diverse ecological examples.     

Functional traits explain phytoplankton community structure and seasonal dynamics in a marine ecosystem

A fundamental yet elusive goal of ecology is to predict the structure of communities from the environmental conditions they experience. Trait‐based approaches to terrestrial plant communities have shown that functional traits can help reveal the mechanisms underlying community assembly, but such approaches have not been tested on the microbes that dominate ecosystem processes in the ocean. Here, we test whether functional traits can explain community responses to seasonal environmental fluctuation, using a time series of the phytoplankton of the English Channel. We show that interspecific variation in response to major limiting resources, light and nitrate, can be well‐predicted by lab‐measured traits characterising light utilisation, nitrate utilisation and maximum growth rate. As these relationships were predicted a priori, using independently measured traits, our results show that functional traits provide a strong mechanistic foundation for understanding the structure and dynamics of ecological communities.     

Seed germination traits can contribute better to plant community ecology

Analyses of functional traits have become fundamental tools for understanding patterns and processes in plant community ecology. In this context, regenerative seed traits play an important, yet overlooked, role because they largely determine the ability of plants to disperse and re‐establish. A survey of recent publications in community ecology suggests that seed germination traits in particular are neglected at the expense of other relevant but overused traits based only on seed morphology. As a response to this bias, we discuss the functional significance of seed germination traits in comparison with morphological and biophysical seed traits, and advocate their use in vegetation science. We also demonstrate how research in community assembly, climate change and restoration ecology can benefit from the inclusion of germination traits, encompassing functions that cannot be explained solely by adult plant traits. Seed germination experiments conducted in the laboratory or field to quantify these traits provide ecologically meaningful and relatively easy‐to‐obtain information about the functional properties of plant communities. We argue that bridging the gap between seed physiologists and community ecologists will improve the prediction of plant assemblages, and propose further perspectives for including seed traits into the research agenda of functional community ecologists.     

Lack of pattern among phytoplankton assemblages. Or,what does the exception to the rule mean?

In Science we cannot say that `the exception proves the rule'. We have been looking to define patterns in phytoplankton occurrence across trophic spectra where conspicuous covariations between algae and trophic states have been reported. We consider quite different phytoplankton communities observed under similar trophic conditions: we illustrate this point by considering five different phytoplankton communities living in five water bodies in the same wetland, along a TP gradient and over a period of 2 years. This system showed a remarkable dissimilarity of species representation, implying communities of uncorrelated species vary considerably over time. Despite the presence of some characteristic species, communities were not related to a given trophic state. However, coarser community attributes, such as clusters of taxonomic classes, appeared to be more useful in identifying patterns and assembly rules related to trophic spectra. Some ecological concepts can be related to this lack of pattern, e.g., nonconvergence, trajectories far from equilibrium and assembly rules of communities.     

The role of experimental microcosms in ecological research

A number of recent and important developments in community ecology have been derived from experiments conducted in microcosms. Studies with microcosms have addressed a broad range of phenomena, including climate change, biodiversity, assembly rules, habitat restoration, trophic dynamics and mycorrhizal associations. The common factor linking these studies is that they manipulate an individual environmental axis and explore the role that axis plays in structuring communities. We discuss six recent studies to illustrate the use and design of microcosms for community ecology research.     

Trait‐based ecology of terrestrial arthropods

In focusing on how organisms' generalizable functional properties (traits) interact mechanistically with environments across spatial scales and levels of biological organization, trait‐based approaches provide a powerful framework for attaining synthesis, generality and prediction. Trait‐based research has considerably improved understanding of the assembly, structure and functioning of plant communities. Further advances in ecology may be achieved by exploring the trait–environment relationships of non‐sessile, heterotrophic organisms such as terrestrial arthropods, which are geographically ubiquitous, ecologically diverse, and often important functional components of ecosystems. Trait‐based studies and trait databases have recently been compiled for groups such as ants, bees, beetles, butterflies, spiders and many others; however, the explicit justification, conceptual framework, and primary‐evidence base for the burgeoning field of ‘terrestrial arthropod trait‐based ecology’ have not been well established. Consequently, there is some confusion over the scope and relevance of this field, as well as a tendency for studies to overlook important assumptions of the trait‐based approach. Here we aim to provide a broad and accessible overview of the trait‐based ecology of terrestrial arthropods. We first define and illustrate foundational concepts in trait‐based ecology with respect to terrestrial arthropods, and justify the application of trait‐based approaches to the study of their ecology. Next, we review studies in community ecology where trait‐based approaches have been used to elucidate how assembly processes for terrestrial arthropod communities are influenced by niche filtering along environmental gradients (e.g. climatic, structural, and land‐use gradients) and by abiotic and biotic disturbances (e.g. fire, floods, and biological invasions). We also review studies in ecosystem ecology where trait‐based approaches have been used to investigate biodiversity–ecosystem function relationships: how the functional diversity of arthropod communities relates to a host of ecosystem functions and services that they mediate, such as decomposition, pollination and predation. We then suggest how future work can address fundamental assumptions and limitations by investigating trait functionality and the effects of intraspecific variation, assessing the potential for sampling methods to bias the traits and trait values observed, and enhancing the quality and consolidation of trait information in databases. A roadmap to guide observational trait‐based studies is also presented. Lastly, we highlight new areas where trait‐based studies on terrestrial arthropods are well positioned to advance ecological understanding and application. These include examining the roles of competitive, non‐competitive and (multi‐)trophic interactions in shaping coexistence, and macro‐scaling trait–environment relationships to explain and predict patterns in biodiversity and ecosystem functions across space and time. We hope this review will spur and guide future applications of the trait‐based framework to advance ecological insights from the most diverse eukaryotic organisms on Earth.     

Can metabolic traits explain animal community assembly and functioning?

All animals on Earth compete for free energy, which is acquired, assimilated, and ultimately allocated to growth and reproduction. Competition is strongest within communities of sympatric, ecologically similar animals of roughly equal size (i.e. horizontal communities), which are often the focus of traditional community ecology. The replacement of taxonomic identities with functional traits has improved our ability to decipher the ecological dynamics that govern the assembly and functioning of animal communities. Yet, the use of low-resolution and taxonomically idiosyncratic traits in animals may have hampered progress to date. An animal's metabolic rate (MR) determines the costs of basic organismal processes and activities, thus linking major aspects of the multifaceted constructs of ecological niches (where, when, and how energy is obtained) and ecological fitness (how much energy is accumulated and passed on to future generations). We review evidence from organismal physiology to large-scale analyses across the tree of life to propose that MR gives rise to a group of meaningful functional traits – resting metabolic rate (RMR), maximum metabolic rate (MMR), and aerobic scope (AS) – that may permit an improved quantification of the energetic basis of species coexistence and, ultimately, the assembly and functioning of animal communities. Specifically, metabolic traits integrate across a variety of typical trait proxies for energy acquisition and allocation in animals (e.g. body size, diet, mobility, life history, habitat use), to yield a smaller suite of continuous quantities that: (1) can be precisely measured for individuals in a standardized fashion; and (2) apply to all animals regardless of their body plan, habitat, or taxonomic affiliation. While integrating metabolic traits into animal community ecology is neither a panacea to disentangling the nuanced effects of biological differences on animal community structure and functioning, nor without challenges, a small number of studies across different taxa suggest that MR may serve as a useful proxy for the energetic basis of competition in animals. Thus, the application of MR traits for animal communities can lead to a more general understanding of community assembly and functioning, enhance our ability to trace eco-evolutionary dynamics from genotypes to phenotypes (and vice versa), and help predict the responses of animal communities to environmental change. While trait-based ecology has improved our knowledge of animal communities to date, a more explicit energetic lens via the integration of metabolic traits may further strengthen the existing framework.     

Branching out: Towards a trait-based understanding of fungal ecology

Fungal ecology lags behind in the use of traits (i.e. phenotypic characteristics) to understand ecological phenomena. We argue that this is a missed opportunity and that the selection and systematic collection of trait data throughout the fungal kingdom will reap major benefits in ecological and evolutionary understanding of fungi. To develop our argument, we first employ plant trait examples to show the power of trait-based approaches in understanding ecological phenomena such as identifying species allocation resources patterns, inferring community assembly and understanding diversity–ecosystem functioning relationships. Second, we discuss ecologically relevant traits in fungi that could be used to answer such ecological phenomena and can be measured on a large proportion of the fungal kingdom. Third, we identify major challenges and opportunities for widespread, coordinated collection and sharing of fungal trait data. The view that we propose has the potential to allow mycologists to contribute considerably more influential studies in the area of fungal ecology and evolution, as has been demonstrated by comparable earlier efforts by plant ecologists. This represents a change of paradigm, from community profiling efforts through massive sequencing tools, to a more mechanistic understanding of fungal ecology.     

Rebuilding community ecology from functional traits

There is considerable debate about whether community ecology will ever produce general principles. We suggest here that this can be achieved but that community ecology has lost its way by focusing on pairwise species interactions independent of the environment. We assert that community ecology should return to an emphasis on four themes that are tied together by a two-step process: how the fundamental niche is governed by functional traits within the context of abiotic environmental gradients; and how the interaction between traits and fundamental niches maps onto the realized niche in the context of a biotic interaction milieu. We suggest this approach can create a more quantitative and predictive science that can more readily address issues of global change.     

Changing assembly rules during secondary succession: evidence for non-random patterns

Describing the rules of community assembly is a central topic of ecology. Studying successional processes through a trait-based null model approach can help to better understand the rules of community assembly.According to theoretical considerations, at the beginning of succession - after getting over the dispersal limitation stage - community composition is primarily shaped by environmental filters (generating functional convergence), while in later stages limiting similarity (generating functional divergence) will be dominant. However, empirical evidence does not clearly support theoretical expectations.Our aim was to detect the presence and changes of trait-based assembly processes during old-field succession based on twelve traits. Changes in vegetation composition were evaluated by a combination of time series and space-for-time substitution: conducting three resurveys of permanent plots on four old-field age-groups. The individual dispersion of traits was transformed into effect size (i.e. departure from null model expectation). The impact of time since abandonment on effect sizes was tested by generalized additive mixed effect models.We detected a non-random pattern for each trait in at least some part of the succession. Departure from randomness did not change significantly over time for six traits: seed mass, lateral spread and pollination type were divergent, while leaf size, generative height and length of flowering were convergent. Six traits had changing patterns along the succession. Four of them showed increasing divergence (e.g. dispersal type, LDMC), which supports our hypothesis. While two (SLA, life form) displayed increasing convergence, contrary to expectations.We confirmed the general hypothesis that convergence is predominant initially and that divergence can be detected later in succession for four traits. However, the large variation found in trait dispersion indicates that complex processes operate during succession.     

Macrosystem community change in lake phytoplankton and its implications for diversity and function

Aim

We use lake phytoplankton community data to quantify the spatio-temporal and scale-dependent impacts of eutrophication, land-use and climate change on species niches and community assembly processes while accounting for species traits and phylogenetic constraints.

Location

Finland.

Time period

1977–2017.

Major taxa

Phytoplankton.

Methods

We use hierarchical modelling of species communities (HMSC) to model metacommunity trajectories at 853 lakes over four decades of environmental change, including a hierarchical spatial structure to account for scale-dependent processes. Using a “region of common profile” approach, we evaluate compositional changes of species communities and trait profiles and investigate their temporal development.

Results

We demonstrate the emergence of novel and widespread community composition clusters in previously more compositionally homogeneous communities, with cluster-specific community trait profiles, indicating functional differences. A strong phylogenetic signal of species responses to the environment implies similar responses among closely related taxa. Community cluster-specific species prevalence indicates lower taxonomic dispersion within the current dominant clusters compared with the historically dominant cluster and an overall higher prevalence of smaller species sizes within communities. Our findings denote profound spatio-temporal structuring of species co-occurrence patterns and highlight functional differences of lake phytoplankton communities.

Main conclusions

Diverging community trajectories have led to a nationwide reshuffling of lake phytoplankton communities. At regional and national scales, lakes are not single entities but metacommunity hubs in an interconnected waterscape. The assembly mechanisms of phytoplankton communities are strongly structured by spatio-temporal dynamics, which have led to novel community types, but only a minor part of this reshuffling could be linked to temporal environmental change.     

Seasonal and spatial functional shifts in phytoplankton communities of five tropical reservoirs

Trait-based approaches have become increasingly important and valuable in understanding phytoplankton community assembly and composition. These approaches allow for comparisons between water bodies with different species composition. We hypothesize that similar changes in environmental conditions lead to similar responses with regard to functional traits of phytoplankton communities, regardless of trophic state or species composition. We studied the phytoplankton (species composition, community trait mean and diversity) of five reservoirs in Brazil along a trophic gradient from ultra-oligotrophic to meso-eutrophic. Samples at two seasons (summer/rainy and winter/dry) with a horizontal and vertical resolution were taken. Using multivariate analysis, the five reservoirs separated, despite some overlap, according to their environmental variables (mainly total phosphorus, conductivity, pH, chlorophyll a). However, between the seasonal periods, the reservoirs shifted in a similar direction in the multi-dimensional space. The seasonal response of the overall phytoplankton community trait mean differed between the ultra-oligotrophic and the other reservoirs, with three reservoirs exhibiting a very similar community trait mean despite considerable differences in species composition. Within-season differences between different water layers were low. The functional diversity was also unrelated to the trophic state of the reservoirs. Thus, seasonal environmental changes had strong influence on the functional characteristics of the phytoplankton community in reservoirs with distinct trophic condition and species composition. These results demonstrate that an ataxonomic trait-based approach is a relevant tool for comparative studies in phytoplankton ecology.     

Impairing the largest and most productive forest on our planet: how do human activities impact phytoplankton?

This article summarizes the outcomes of the 16th Workshop of the International Association for Phytoplankton Taxonomy and Ecology. Four major issues dealing with the impact exerted by human activities on phytoplankton were addressed in the articles of this special volume: climate change and its impacts on phytoplankton, the role of land use in shaping composition and diversity of phytoplankton, the importance of autecological studies to fully understand how phytoplankton is impacted by stressors and the role of ecological classification to evaluate community changes due to the different impacts. Case studies from different types of aquatic environments (rivers, deep and shallow lakes, reservoirs, mountain lakes, and temporary ponds) and from diverse geographical locations (not only from the Mediterranean and temperate regions, but also from subtropical and tropical ones) have shown that a complex spectrum of human impacts, not exclusively linked to eutrophication, severely conditions structure and dynamics of phytoplankton assemblage both in the short and long terms. Moreover, the trade-offs between climate change and other human-induced stresses as eutrophication, agricultural and urban land use or water overexploitation contribute to make more severe the impact exerted by humans on phytoplankton and, in turn, on the functioning of aquatic ecosystems.     

Tropical dung beetle morphological traits predict functional traits and show intraspecific differences across land uses

Functional traits and functional diversity measures are increasingly being used to examine land use effects on biodiversity and community assembly rules. Morphological traits are often used directly as functional traits. However, behavioral characteristics are more difficult to measure. Establishing methods to derive behavioral traits from morphological measurements is necessary to facilitate their inclusion in functional diversity analyses. We collected morphometric data from over 1,700 individuals of 12 species of dung beetle to establish whether morphological measurements can be used as predictors of behavioral traits. We also compared morphology among individuals collected from different land uses (primary forest, logged forest, and oil palm plantation) to identify whether intraspecific differences in morphology vary among land use types. We show that leg and eye measurements can be used to predict dung beetle nesting behavior and period of activity and we used this information to confirm the previously unresolved nesting behavior for Synapsis ritsemae. We found intraspecific differences in morphological traits across different land use types. Phenotypic plasticity was found for traits associated with dispersal (wing aspect ratio and wing loading) and reproductive capacity (abdomen size). The ability to predict behavioral functional traits from morphology is useful where the behavior of individuals cannot be directly observed, especially in tropical environments where the ecology of many species is poorly understood. In addition, we provide evidence that land use change can cause phenotypic plasticity in tropical dung beetle species. Our results reinforce recent calls for intraspecific variation in traits to receive more attention within community ecology.     

Species coexistence in temperate, mixed deciduous forests

The response of tree life-history traits to community profiles (horizontal and vertical heterogeneity, disturbances and biotic interactions) determines community assembly rules, which are currently a hot issue in community ecology. Important mechanisms of coexistence differ throughout the developing stages of tree life history. Many processes of niche partitioning and tradeoffs that potentially enable tree coexistence have been reported to be present in temperate forests, although some of these life-history traits are either correlated with each other or are not independent. Not all of the proposed mechanisms explain coexistence equally well; some could predominate in determining the community organization of forest communities. Population studies need to concentrate more on the component species of a target community to detect the ecological assembly rule. These approaches can also address how chance factors contribute to the composition of temperate tree communities, which might be less dependent on chance than are tropical ones.     

Individual Cell Based Traits Obtained by Scanning Flow-Cytometry Show Selection by Biotic and Abiotic Environmental Factors during a Phytoplankton Spring Bloom

In ecology and evolution, the primary challenge in understanding the processes that shape biodiversity is to assess the relationship between the phenotypic traits of organisms and the environment. Here we tested for selection on physio-morphological traits measured by scanning flow-cytometry at the individual level in phytoplankton communities under a temporally changing biotic and abiotic environment. Our aim was to study how high-frequency temporal changes in the environment influence biodiversity dynamics in a natural community. We focused on a spring bloom in Lake Zurich (Switzerland), characterized by rapid changes in phytoplankton, water conditions, nutrients and grazing (mainly mediated by herbivore ciliates). We described bloom dynamics in terms of taxonomic and trait-based diversity and found that diversity dynamics of trait-based groups were more pronounced than those of identified phytoplankton taxa. We characterized the linkage between measured phytoplankton traits, abiotic environmental factors and abundance of the main grazers and observed weak but significant correlations between changing abiotic and biotic conditions and measured size-related and fluorescence-related traits. We tested for deviations in observed community-wide distributions of focal traits from random patterns and found evidence for both clustering and even spacing of traits, occurring sporadically over the time series. Patterns were consistent with environmental filtering and phenotypic divergence under herbivore pressure, respectively. Size-related traits showed significant even spacing during the peak of herbivore abundance, suggesting that morphology-related traits were under selection from grazing. Pigment distribution within cells and colonies appeared instead to be associated with acclimation to temperature and water chemistry. We found support for trade-offs among grazing resistance and environmental tolerance traits, as well as for substantial periods of dynamics in which our measured traits were not under selection.