Functional traits shape plant-plant interactions and recruitment in a hotspot of woody plant diversity.

Understanding and predicting recruitment in species-rich plant communities requires identifying functional determinants of both density-independent performance and interactions. In a common-garden field experiment with 25 species of the woody plant genus Protea, we varied the initial spatial and taxonomic arrangement of seedlings and followed their survival and growth during recruitment. Neighbourhood models quantified how six key functional traits affect density-independent performance, interaction effects and responses. Trait-based neighbourhood models accurately predicted individual survival and growth from the initial spatial and functional composition of species-rich experimental communities. Functional variation among species caused substantial variation in density-independent survival and growth that was not correlated with interaction effects and responses. Interactions were spatially restricted but had important, predominantly competitive, effects on recruitment. Traits increasing the acquisition of limiting resources (water for survival and soil P for growth) mediated trade-offs between interaction effects and responses. Moreover, resprouting species had higher survival but reduced growth, likely reinforcing the survival-growth trade-off in adult plants. Resource acquisition of juvenile plants shapes Protea community dynamics with acquisitive species with strong competitive effects suffering more from competition. Together with functional determinants of density-independent performance, this makes recruitment remarkably predictable, which is critical for efficient restoration and near-term ecological forecasts of species-rich communities.

Alien plant fitness is limited by functional trade-offs rather than a long-term increase in competitive effects of native communities.

Alien plants experience novel abiotic conditions and interactions with native communities in the introduced area. Intra- and interspecific selection on functional traits in the new environment may lead to increased population growth with time since introduction (residence time). However, selection regimes might differ depending on the invaded habitat. Additionally, in high-competition habitats, a build-up of biotic resistance of native species due to accumulation of eco-evolutionary experience to aliens over time may limit invasion success. We tested if the effect of functional traits and the population dynamics of aliens depends on interspecific competition with native plant communities. We conducted a multi-species experiment with 40 annual Asteraceae that differ in residence time in Germany. We followed their population growth in monocultures and in interspecific competition with an experienced native community (varying co-existence times between focals and community). To more robustly test our findings, we used a naïve community that never co-existed with the focals. We found that high seed mass decreased population growth in monocultures but tended to increase population growth under high interspecific competition. We found no evidence for a build-up of competition-mediated biotic resistance by the experienced community over time. Instead, population growth of the focal species was similarly inhibited by the experienced and naïve community. By comparing the effect of experienced and naïve communities on population dynamics over 2 years across a large set of species with a high variation in functional traits and residence time, this study advances the understanding of the long-term dynamics of plant invasions. In our study system, population growth of alien species was not limited by an increase of competitive effects by native communities (one aspect of biotic resistance) over time. Instead, invasion success of alien plants may be limited because initial spread in low-competition habitats requires different traits than establishment in high-competition habitats.

Improving measurements of the falling trajectory and terminal velocity of wind-dispersed seeds.

Seed dispersal by wind is one of the most important dispersal mechanisms in plants. The key seed trait affecting seed dispersal by wind is the effective terminal velocity (hereafter "terminal velocity", V t ), the maximum falling speed of a seed in still air. Accurate estimates of V t are crucial for predicting intra- and interspecific variation in seed dispersal ability. However, existing methods produce biased estimates of V t for slow- or fast-falling seeds, fragile seeds, and seeds with complex falling trajectories. We present a new video-based method that estimates the falling trajectory and V t of wind-dispersed seeds. The design involves a mirror that enables a camera to simultaneously record a falling seed from two perspectives. Automated image analysis then determines three-dimensional seed trajectories at high temporal resolution. To these trajectories, we fit a physical model of free fall with air resistance to estimate V t . We validated this method by comparing the estimated V t of spheres of different diameters and materials to theoretical expectations and by comparing the estimated V t of seeds to measurements in a vertical wind tunnel. V t estimates closely match theoretical expectations for spheres and vertical wind tunnel measurements for seeds. However, our V t estimates for fast-falling seeds are markedly higher than those in an existing trait database. This discrepancy seems to arise because previous estimates inadequately accounted for seed acceleration. The presented method yields accurate, efficient, and affordable estimates of the three-dimensional falling trajectory and terminal velocity for a wide range of seed types. The method should thus advance the understanding and prediction of wind-driven seed dispersal.

Global relationships in tree functional traits.

Due to massive energetic investments in woody support structures, trees are subject to unique physiological, mechanical, and ecological pressures not experienced by herbaceous plants. Despite a wealth of studies exploring trait relationships across the entire plant kingdom, the dominant traits underpinning these unique aspects of tree form and function remain unclear. Here, by considering 18 functional traits, encompassing leaf, seed, bark, wood, crown, and root characteristics, we quantify the multidimensional relationships in tree trait expression. We find that nearly half of trait variation is captured by two axes: one reflecting leaf economics, the other reflecting tree size and competition for light. Yet these orthogonal axes reveal strong environmental convergence, exhibiting correlated responses to temperature, moisture, and elevation. By subsequently exploring multidimensional trait relationships, we show that the full dimensionality of trait space is captured by eight distinct clusters, each reflecting a unique aspect of tree form and function. Collectively, this work identifies a core set of traits needed to quantify global patterns in functional biodiversity, and it contributes to our fundamental understanding of the functioning of forests worldwide.

Seed dispersal by wind decreases when plants are water-stressed, potentially counteracting species coexistence and niche evolution.

Hydrology is a major environmental factor determining plant fitness, and hydrological niche segregation (HNS) has been widely used to explain species coexistence. Nevertheless, the distribution of plant species along hydrological gradients does not only depend on their hydrological niches but also depend on their seed dispersal, with dispersal either weakening or reinforcing the effects of HNS on coexistence. However, it is poorly understood how seed dispersal responds to hydrological conditions. To close this gap, we conducted a common-garden experiment exposing five wind-dispersed plant species (Bellis perennis, Chenopodium album, Crepis sancta, Hypochaeris glabra, and Hypochaeris radicata) to different hydrological conditions. We quantified the effects of hydrological conditions on seed production and dispersal traits, and simulated seed dispersal distances with a mechanistic dispersal model. We found species-specific responses of seed production, seed dispersal traits, and predicted dispersal distances to hydrological conditions. Despite these species-specific responses, there was a general positive relationship between seed production and dispersal distance: Plants growing in favorable hydrological conditions not only produce more seeds but also disperse them over longer distances. This arises mostly because plants growing in favorable environments grow taller and thus disperse their seeds over longer distances. We postulate that the positive relationship between seed production and dispersal may reduce the concentration of each species to the environments favorable for it, thus counteracting species coexistence. Moreover, the resulting asymmetrical gene flow from favorable to stressful habitats may slow down the microevolution of hydrological niches, causing evolutionary niche conservatism. Accounting for context-dependent seed dispersal should thus improve ecological and evolutionary models for the spatial dynamics of plant populations and communities.

The importance of individual movement and feeding behaviour for long-distance seed dispersal by red deer: a data-driven model.

BACKGROUND: Long-distance seed dispersal (LDD) has strong impacts on the spatiotemporal dynamics of plants. Large animals are important LDD vectors because they regularly transport seeds of many plant species over long distances. While there is now ample evidence that behaviour varies considerably between individual animals, it is not clear to what extent inter-individual variation in behaviour alters seed dispersal by animals. METHODS: We study how inter-individual variation in the movement and feeding behaviour of one of Europe's largest herbivores (the red deer, Cervus elaphus) affects internal seed dispersal (endozoochory) of multiple plant species. We combine movement data of 21 individual deer with measurements of seed loads in the dung of the same individuals and with data on gut passage time. These data serve to parameterize a model of passive dispersal that predicts LDD in three orientations (horizontal as well as upward and downward in elevation).With this model we investigate to what extent per-seed probabilities of LDD and seed load vary between individuals and throughout the vegetation period (May-December). Subsequently, we test whether per-seed LDD probability and seed load are positively (or negatively) correlated so that more mobile animals disperse more (or less) seeds. Finally, we examine whether non-random associations between per-seed LDD probability and seed load affect the LDD of individual plant species. RESULTS: The studied deer dispersed viable seeds of at least 62 plant species. Deer individuals varied significantly in per-seed LDD probability and seed loads. However, more mobile animals did not disperse more or less seeds than less mobile ones. Plant species also did not differ significantly in the relationship between per-seed LDD probability and seed load. Yet plant species differed in how their seed load was distributed across deer individuals and in time, and this caused their LDD potential to differ more than twofold. For several plant species, we detected non-random associations between per-seed LDD probability and seed load that generally increased LDD potential. CONCLUSIONS: Inter-individual variation in movement and feeding behaviour means that certain deer are substantially more effective LDD vectors than others. This inter-individual variation reduces the reliability of LDD and increases the sensitivity of LDD to the decline of deer populations. Variation in the dispersal services of individual animals should thus be taken into account in models in order to improve LDD projections.

Shifts in plant functional community composition under hydrological stress strongly decelerate litter decomposition.

Litter decomposition is a key process of nutrient and carbon cycling in terrestrial ecosystems. The decomposition process will likely be altered under ongoing climate change, both through direct effects on decomposer activity and through indirect effects caused by changes in litter quality. We studied how hydrological change indirectly affects decomposition via plant functional community restructuring caused by changes in plant species' relative abundances (community-weighted mean (CWM) traits and functional diversity). We further assessed how those indirect litter quality effects compare to direct effects. We set up a mesocosm experiment, in which sown grassland communities and natural turf pieces were subjected to different hydrological conditions (dryness and waterlogging) for two growing seasons. Species-level mean traits were obtained from trait databases and combined with species' relative abundances to assess functional community restructuring. We studied decomposition of mixed litter from these communities in a common "litterbed." These indirect effects were compared to effects of different hydrological conditions on soil respiration and on decomposition of standard litter (direct effects). Dryness reduced biomass production in sown communities and natural turf pieces, while waterlogging only reduced biomass in sown communities. Hydrological stress caused profound shifts in species' abundances and consequently in plant functional community composition. Hydrologically stressed communities had higher CMW leaf dry matter content, lower CMW leaf nitrogen content, and lower functional diversity. Lower CWM leaf N content and functional diversity were strongly related to slower decomposition. These indirect effects paralleled direct effects, but were larger and longer-lasting. Species mean traits from trait databases had therefore considerable predictive power for decomposition. Our results show that stressful soil moisture conditions, that are likely to occur more frequently in the future, quickly shift species' abundances. The resulting functional community restructuring will decelerate decomposition under hydrological stress.

Mismatches between demographic niches and geographic distributions are strongest in poorly dispersed and highly persistent plant species.

The ecological niche of a species describes the variation in population growth rates along environmental gradients that drives geographic range dynamics. Niches are thus central for understanding and forecasting species' geographic distributions. However, theory predicts that migration limitation, source-sink dynamics, and time-lagged local extinction can cause mismatches between niches and geographic distributions. It is still unclear how relevant these niche-distribution mismatches are for biodiversity dynamics and how they depend on species life-history traits. This is mainly due to a lack of the comprehensive, range-wide demographic data needed to directly infer ecological niches for multiple species. Here we quantify niches from extensive demographic measurements along environmental gradients across the geographic ranges of 26 plant species (Proteaceae; South Africa). We then test whether life history explains variation in species' niches and niche-distribution mismatches. Niches are generally wider for species with high seed dispersal or persistence abilities. Life-history traits also explain the considerable interspecific variation in niche-distribution mismatches: poorer dispersers are absent from larger parts of their potential geographic ranges, whereas species with higher persistence ability more frequently occupy environments outside their ecological niche. Our study thus identifies major demographic and functional determinants of species' niches and geographic distributions. It highlights that the inference of ecological niches from geographical distributions is most problematic for poorly dispersed and highly persistent species. We conclude that the direct quantification of ecological niches from demographic responses to environmental variation is a crucial step toward a better predictive understanding of biodiversity dynamics under environmental change.

The geometry of habitat fragmentation: Effects of species distribution patterns on extinction risk due to habitat conversion.

Land-use changes, which cause loss, degradation, and fragmentation of natural habitats, are important anthropogenic drivers of biodiversity change. However, there is an ongoing debate about how fragmentation per se affects biodiversity in a given amount of habitat. Here, we illustrate why it is important to distinguish two different aspects of fragmentation to resolve this debate: (a) geometric fragmentation effects, which exclusively arise from the spatial distributions of species and habitat fragments, and (b) demographic fragmentation effects due to reduced fragment sizes, and/or changes in fragment isolation, edge effects, or species interactions. While most empirical studies are primarily interested in quantifying demographic fragmentation effects, geometric effects are typically invoked as post hoc explanations of biodiversity responses to fragmentation per se. Here, we present an approach to quantify geometric fragmentation effects on species survival and extinction probabilities. We illustrate this approach using spatial simulations where we systematically varied the initial abundances and distribution patterns (i.e., random, aggregated, or regular) of species as well as habitat amount and fragmentation per se. As expected, we found no geometric fragmentation effects when species were randomly distributed. However, when species were aggregated, we found positive effects of fragmentation per se on survival probability for a large range of scenarios. For regular species distributions, we found weakly negative geometric effects. These findings are independent of the ecological mechanisms which generate nonrandom species distributions. Our study helps to reconcile seemingly contradictory results of previous fragmentation studies. Since intraspecific aggregation is a ubiquitous pattern in nature, our findings imply widespread positive geometric fragmentation effects. This expectation is supported by many studies that find positive effects of fragmentation per se on species occurrences and diversity after controlling for habitat amount. We outline how to disentangle geometric and demographic fragmentation effects, which is critical for predicting the response of biodiversity to landscape change.

The dimensionality of stability depends on disturbance type.

Ecosystems respond in various ways to disturbances. Quantifying ecological stability therefore requires inspecting multiple stability properties, such as resistance, recovery, persistence and invariability. Correlations among these properties can reduce the dimensionality of stability, simplifying the study of environmental effects on ecosystems. A key question is how the kind of disturbance affects these correlations. We here investigated the effect of three disturbance types (random, species-specific, local) applied at four intensity levels, on the dimensionality of stability at the population and community level. We used previously parameterized models that represent five natural communities, varying in species richness and the number of trophic levels. We found that disturbance type but not intensity affected the dimensionality of stability and only at the population level. The dimensionality of stability also varied greatly among species and communities. Therefore, studying stability cannot be simplified to using a single metric and multi-dimensional assessments are still to be recommended.

Life-History Traits Evolved Jointly with Climatic Niche and Disturbance Regime in the Genus Leucadendron (Proteaceae).

Organisms have evolved a diversity of life-history strategies to cope with variation in their environment. Persistence as adults and/or seeds across recruitment events allows species to dampen the effects of environmental fluctuations. The evolution of life cycles with overlapping generations should thus permit the colonization of environments with uncertain recruitment. We tested this hypothesis in Leucadendron (Proteaceae), a genus with high functional diversity native to fire-prone habitats in the South African fynbos. We analyzed the joint evolution of life-history traits (adult survival and seed-bank strategies) and ecological niches (climate and fire regime), using comparative methods and accounting for various sources of uncertainty. In the fynbos, species with canopy seed banks that are unable to survive fire as adults display nonoverlapping generations. In contrast, resprouters with an underground seed bank may be less threatened by extreme climatic events and fire intervals, given their iteroparity and long-lasting seed bank. Life cycles with nonoverlapping generations indeed jointly evolved with niches with less exposure to frost but not with those with less exposure to drought. Canopy seed banks jointly evolved with niches with more predictable fire return, compared to underground seed banks. The evolution of extraordinary functional diversity among fynbos plants thus reflects, at least in part, the diversity of both climates and fire regimes in this region.

Statistical ecology comes of age.

The desire to predict the consequences of global environmental change has been the driver towards more realistic models embracing the variability and uncertainties inherent in ecology. Statistical ecology has gelled over the past decade as a discipline that moves away from describing patterns towards modelling the ecological processes that generate these patterns. Following the fourth International Statistical Ecology Conference (1-4 July 2014) in Montpellier, France, we analyse current trends in statistical ecology. Important advances in the analysis of individual movement, and in the modelling of population dynamics and species distributions, are made possible by the increasing use of hierarchical and hidden process models. Exciting research perspectives include the development of methods to interpret citizen science data and of efficient, flexible computational algorithms for model fitting. Statistical ecology has come of age: it now provides a general and mathematically rigorous framework linking ecological theory and empirical data.

Convergent and correlated evolution of major life-history traits in the angiosperm genus Leucadendron (Proteaceae).

Natural selection is expected to cause convergence of life histories among taxa as well as correlated evolution of different life-history traits. Here, we quantify the extent of convergence of five key life-history traits (adult fire survival, seed storage, degree of sexual dimorphism, pollination mode, and seed-dispersal mode) and test hypotheses about their correlated evolution in the genus Leucadendron (Proteaceae) from the fire-prone South African fynbos. We reconstructed a new molecular phylogeny of this highly diverse genus that involves more taxa and molecular markers than previously. This reconstruction identifies new clades that were not detected by previous molecular study and morphological classifications. Using this new phylogeny and robust methods that account for phylogenetic uncertainty, we show that the five life-history traits studied were labile during the evolutionary history of the genus. This diversity allowed us to tackle major questions about the correlated evolution of life-history strategies. We found that species with longer seed-dispersal distances tended to evolve lower pollen-dispersal distance, that insect-pollinated species evolved decreased sexual dimorphism, and that species with a persistent soil seed-bank evolved toward reduced fire-survival ability of adults.

Does probability of occurrence relate to population dynamics?

Hutchinson defined species' realized niche as the set of environmental conditions in which populations can persist in the presence of competitors. In terms of demography, the realized niche corresponds to the environments where the intrinsic growth rate (r) of populations is positive. Observed species occurrences should reflect the realized niche when additional processes like dispersal and local extinction lags do not have overwhelming effects. Despite the foundational nature of these ideas, quantitative assessments of the relationship between range-wide demographic performance and occurrence probability have not been made. This assessment is needed both to improve our conceptual understanding of species' niches and ranges and to develop reliable mechanistic models of species geographic distributions that incorporate demography and species interactions. The objective of this study is to analyse how demographic parameters (intrinsic growth rate r and carrying capacity K) and population density (N) relate to occurrence probability (Pocc ). We hypothesized that these relationships vary with species' competitive ability. Demographic parameters, density, and occurrence probability were estimated for 108 tree species from four temperate forest inventory surveys (Québec, Western US, France and Switzerland). We used published information of shade tolerance as indicators of light competition strategy, assuming that high tolerance denotes high competitive capacity in stable forest environments. Interestingly, relationships between demographic parameters and occurrence probability did not vary substantially across degrees of shade tolerance and regions. Although they were influenced by the uncertainty in the estimation of the demographic parameters, we found that r was generally negatively correlated with Pocc , while N, and for most regions K, was generally positively correlated with Pocc . Thus, in temperate forest trees the regions of highest occurrence probability are those with high densities but slow intrinsic population growth rates. The uncertain relationships between demography and occurrence probability suggests caution when linking species distribution and demographic models.

The influence of interspecific interactions on species range expansion rates.

Ongoing and predicted global change makes understanding and predicting species' range shifts an urgent scientific priority. Here, we provide a synthetic perspective on the so far poorly understood effects of interspecific interactions on range expansion rates. We present theoretical foundations for how interspecific interactions may modulate range expansion rates, consider examples from empirical studies of biological invasions and natural range expansions as well as process-based simulations, and discuss how interspecific interactions can be more broadly represented in process-based, spatiotemporally explicit range forecasts. Theory tells us that interspecific interactions affect expansion rates via alteration of local population growth rates and spatial displacement rates, but also via effects on other demographic parameters. The best empirical evidence for interspecific effects on expansion rates comes from studies of biological invasions. Notably, invasion studies indicate that competitive dominance and release from specialized enemies can enhance expansion rates. Studies of natural range expansions especially point to the potential for competition from resident species to reduce expansion rates. Overall, it is clear that interspecific interactions may have important consequences for range dynamics, but also that their effects have received too little attention to robustly generalize on their importance. We then discuss how interspecific interactions effects can be more widely incorporated in dynamic modeling of range expansions. Importantly, models must describe spatiotemporal variation in both local population dynamics and dispersal. Finally, we derive the following guidelines for when it is particularly important to explicitly represent interspecific interactions in dynamic range expansion forecasts: if most interacting species show correlated spatial or temporal trends in their effects on the target species, if the number of interacting species is low, and if the abundance of one or more strongly interacting species is not closely linked to the abundance of the target species.

Differentiation of reproductive and competitive ability in the invaded range of Senecio inaequidens: the role of genetic Allee effects, adaptive and nonadaptive evolution.

Genetic differentiation in the competitive and reproductive ability of invading populations can result from genetic Allee effects or r/K selection at the local or range-wide scale. However, the neutral relatedness of populations may either mask or falsely suggest adaptation and genetic Allee effects. In a common-garden experiment, we investigated the competitive and reproductive ability of invasive Senecio inaequidens populations that vary in neutral genetic diversity, population age and field vegetation cover. To account for population relatedness, we analysed the experimental results with 'animal models' adopted from quantitative genetics. Consistent with adaptive r/K differentiation at local scales, we found that genotypes from low-competition environments invest more in reproduction and are more sensitive to competition. By contrast, apparent effects of large-scale r/K differentiation and apparent genetic Allee effects can largely be explained by neutral population relatedness. Invading populations should not be treated as homogeneous groups, as they may adapt quickly to small-scale environmental variation in the invaded range. Furthermore, neutral population differentiation may strongly influence invasion dynamics and should be accounted for in analyses of common-garden experiments.

Effects of harvesting flowers from shrubs on the persistence and abundance of wild shrub populations at multiple spatial extents.

Wildflower harvesting is an economically important activity of which the ecological effects are poorly understood. We assessed how harvesting of flowers affects shrub persistence and abundance at multiple spatial extents. To this end, we built a process-based model to examine the mean persistence and abundance of wild shrubs whose flowers are subject to harvest (serotinous Proteaceae in the South African Cape Floristic Region). First, we conducted a general sensitivity analysis of how harvesting affects persistence and abundance at nested spatial extents. For most spatial extents and combinations of demographic parameters, persistence and abundance of flowering shrubs decreased abruptly once harvesting rate exceeded a certain threshold. At larger extents, metapopulations supported higher harvesting rates before their persistence and abundance decreased, but persistence and abundance also decreased more abruptly due to harvesting than at smaller extents. This threshold rate of harvest varied with species' dispersal ability, maximum reproductive rate, adult mortality, probability of extirpation or local extinction, strength of Allee effects, and carrying capacity. Moreover, spatial extent interacted with Allee effects and probability of extirpation because both these demographic properties affected the response of local populations to harvesting more strongly than they affected the response of metapopulations. Subsequently, we simulated the effects of harvesting on three Cape Floristic Region Proteaceae species and found that these species reacted differently to harvesting, but their persistence and abundance decreased at low rates of harvest. Our estimates of harvesting rates at maximum sustainable yield differed from those of previous investigations, perhaps because researchers used different estimates of demographic parameters, models of population dynamics, and spatial extent than we did. Good demographic knowledge and careful identification of the spatial extent of interest increases confidence in assessments and monitoring of the effects of harvesting. Our general sensitivity analysis improved understanding of harvesting effects on metapopulation dynamics and allowed qualitative assessment of the probability of extirpation of poorly studied species.

Spread of North American wind-dispersed trees in future environments.

Despite ample research, understanding plant spread and predicting their ability to track projected climate changes remain a formidable challenge to be confronted. We modelled the spread of North American wind-dispersed trees in current and future (c. 2060) conditions, accounting for variation in 10 key dispersal, demographic and environmental factors affecting population spread. Predicted spread rates vary substantially among 12 study species, primarily due to inter-specific variation in maturation age, fecundity and seed terminal velocity. Future spread is predicted to be faster if atmospheric CO(2) enrichment would increase fecundity and advance maturation, irrespective of the projected changes in mean surface windspeed. Yet, for only a few species, predicted wind-driven spread will match future climate changes, conditioned on seed abscission occurring only in strong winds and environmental conditions favouring high survival of the farthest-dispersed seeds. Because such conditions are unlikely, North American wind-dispersed trees are expected to lag behind the projected climate range shift.