Effects of two traits of the ecological state equation on our understanding of species coexistence and ecosystem services

Species coexistence has been a fundamental issue to understand ecosystem functioning since the beginnings of ecology as a science. The search of a reliable and all-encompassing explanation for this issue has become a complex goal with several apparently opposing trends. On the other side, seemingly unconnected with species coexistence, an ecological state equation based on the inverse correlation between an indicator of dispersal that fits gamma distribution and species diversity has been recently developed. This article explores two factors, whose effects are inconspicuous in such an equation at the first sight, that are used to develop an alternative general theoretical background in order to provide a better understanding of species coexistence. Our main outcomes are: (i) the fit of dispersal and diversity values to gamma distribution is an important factor that promotes species coexistence mainly due to the right-skewed character of gamma distribution; (ii) the opposite correlation between species diversity and dispersal implies that any increase of diversity is equivalent to a route of ���ecological cooling��� whose maximum limit should be constrained by the influence of the third law of thermodynamics; this is in agreement with the well-known asymptotic trend of diversity values in space and time; (iii) there are plausible empirical and theoretical ways to apply physical principles to explain important ecological processes; (iv) the gap between theoretical and empirical ecology in those cases where species diversity is paradoxically high could be narrowed by a wave model of species coexistence based on the concurrency of local equilibrium states. In such a model, competitive exclusion has a limited but indispensable role in harmonious coexistence with functional redundancy. We analyze several literature references as well as ecological and evolutionary examples that support our approach, reinforcing the meaning equivalence between important physical and ecological principles.

A missing link between facilitation and plant species coexistence: nurses benefit generally rare species more than common ones

1. Positive interactions among plants can increase species richness by relaxing environmental filters and providing more heterogeneous environments. However, it is not known if facilitation could affect coexistence through other mechanisms. Most studies on plant coexistence focus on negative frequency-dependent mechanisms (decreasing the abundance of common species); here, we test if facilitation can enhance coexistence by giving species an advantage when rare. 2. To test our hypothesis, we used a global data set from drylands and alpine environments and measured the intensity of facilitation (based on co-occurrences with nurse plants) for 48 species present in at least 4 different sites and with a range of abundances in the field. We compared these results with the degree of facilitation experienced by species which are globally rare or common (according to the IUCN Red List), and with a larger data base including over 1200 co-occurrences of target species with their nurses. 3. Facilitation was stronger for rare species (i.e. those having lower local abundances or considered endangered by the IUCN) than for common species, and strongly decreased with the abundance of the facilitated species. These results hold after accounting for the distance of each species from its ecological optimum (i.e. the degree of functional stress it experiences). 4. Synthesis. Our results highlight that nurse plants not only increase the number of species able to colonize a given site, but may also promote species coexistence by preventing the local extinction of rare species. Our findings illustrate the role that nurse plants play in conserving endangered species and link the relationship between facilitation and diversity with coexistence theory. As such, they provide further mechanistic understanding on how facilitation maintains plant diversity.

Recruitment limitation constrains local species richness and productivity in dry grassland

Species coexistence and local-scale species richness are limited by the availability of seeds and microsites for germination and establishment. We conducted a seed addition experiment in seminatural grassland at three sites in southern Switzerland and repeated the experiment in two successive years to evaluate various circumstances under which seed limitation and establishment success affect community functioning. A collection of 144000 seeds of 22 meadow species including grasses and forbs of local provenance was gathered, and seeds were individually sown in a density that resembled natural seed rain. The three communities were seed limited. Three years after sowing, single species varied in emergence (0���50%), survival (0���69%), and establishment rates (0���27%). One annual and 13 perennial species reached reproductive stage. Low establishment at one site and reduced growth at another site indicated stronger microsite limitation compared to the third site. Recruitment was influenced by differences in abiotic environmental conditions between sites (water availability, soil minerals) and by within-site differences in biotic interaction (competition). At the least water-limited site, sowing resulted in an increase in phytomass due to establishment of short-lived perennials in the second and third years after sowing. This increase persisted over the following two years due to establishment of longer-lived perennials. After sowing in a wetter year with higher phytomass, however, productivity did not increase, because higher intensity of competition in an early phase of establishment resulted in less vigorous plants later on. Due to the generally favorable weather conditions during this study, sowing year had a small effect on numbers of established individuals over all species. Recruitment limitation can thus constrain local-scale species richness and productivity, either by a lack of seeds or by reduced seedling growth, likely due to competition from the established vegetation.

Herbivores equalize the seedling height growth of three dominant tree species in an African tropical rain forest

Determining the impact of insect herbivores on forest tree seedlings and saplings is difficult without experimentation in the field. Moreover, this impact may be heterogeneous in time and space because of seasonal rainfall and canopy disturbances, or ���gaps���, which can influence both insect abundance and plant performance. In this study we used fine netting to individually protect seedlings of Microberlinia bisulcata, Tetraberlinia bifoliolata and Tetraberlinia korupensis trees (Fabaceae = Leguminosae) from insects in 41 paired gap-understorey locations across 80 ha of primary rain forest (Korup, Cameroon). For all species, growth in height and leaf numbers was negligible in the understorey, where M. bisulcata had the lowest survival after c. 2 years. In gaps, however, all species responded positively with pronounced above-ground growth across seasons. When exposed to herbivores their seedling height growth was similar, but in the absence of herbivores, M. bisulcata significantly outgrew both Tetraberlinia species and matched their leaf numbers. This result suggests that insect herbivores might play an important role in maintaining species coexistence by mitigating sapling abundance of the more palatable M. bisulcata, which in gaps was eaten the most severely. The higher ratio in static leaf damage of control-to-caged M. bisulcata seedlings in gaps than understorey locations was consistent with the Plant Vigour Hypothesis. This result, however, did not apply to either Tetraberlinia species. For M. bisulcata and T. korupensis, but not T. bifoliolata (the most shade-tolerant species), caging improved relative seedling survival in the understory locations compared to gaps, providing restricted support for the Limiting Resource Model. Approximately 2.25 years after treatments were removed, the caged seedlings were taller and had more leaves than controls in all three species, and the effect remained strongest for M. bisulcata. We conclude that in this community the impact of leaf herbivory on seedling growth in gaps is strong for the dominant M. bisulcata, which coupled to a very low shade-tolerance contributes to limiting its regeneration. However, because gaps are common to most forests, insect herbivores may be having impacts upon functionally similar tree species that are also characterized by low sapling recruitment much more widely than currently appreciated. An implication for the restoration and management of M. bisulcata populations in forests outside of Korup is that physical protection from herbivores of new seedlings where the canopy is opened by gaps, or by harvesting, should substantially increase its subcanopy regeneration, and thus, too, its opportunities for adult recruitment.

Matrix models for quantifying competitive intransitivity from species abundance data

In a network of competing species, a competitive intransitivity occurs when the ranking of competitive abilities does not follow a linear hierarchy (A > B > C but C > A). A variety of mathematical models suggests that intransitive networks can prevent or slow down competitive exclusion and maintain biodiversity by enhancing species coexistence. However, it has been difficult to assess empirically the relative importance of intransitive competition because a large number of pairwise species competition experiments are needed to construct a competition matrix that is used to parameterize existing models. Here we introduce a statistical framework for evaluating the contribution of intransitivity to community structure using species abundance matrices that are commonly generated from replicated sampling of species assemblages. We provide metrics and analytical methods for using abundance matrices to estimate species competition and patch transition matrices by using reverse-engineering and a colonization-competition model. These matrices provide complementary metrics to estimate the degree of intransitivity in the competition network of the sampled communities. Benchmark tests reveal that the proposed methods could successfully detect intransitive competition networks, even in the absence of direct measures of pairwise competitive strength. To illustrate the approach, we analyzed patterns of abundance and biomass of five species of necrophagous Diptera and eight species of their hymenopteran parasitoids that co-occur in beech forests in Germany. We found evidence for a strong competitive hierarchy within communities of flies and parasitoids. However, for parasitoids, there was a tendency towards increasing intransitivity in higher weight classes, which represented larger resource patches. These tests provide novel methods for empirically estimating the degree of intransitivity in competitive networks from observational datasets. They can be applied to experimental measures of pairwise species interactions, as well as to spatio-temporal samples of assemblages in homogenous environments or environmental gradients.

Relationships between functional traits and inorganic nitrogen acquisition among eight contrasting European grass species

Backgrounds and Aims Leaf functional traits have been used as a basis to categoize plants across a range of resource-use specialization, from those that conserve available resources to those that exploit them. However, the extent to which the leaf functional traits used to define the resource-use strategies are related to root traits and are good indicators of the ability of the roots to take up nitrogen (N) are poorly known. This is an important question because interspecific differences in N uptake have been proposed as one mechanism by which species coexistence may be determined. This study therefore investigated the relationships between functional traits and N uptake ability for grass species across a range of conservative to exploitative resource-use strategies.Methods Root uptake of NH4+ and NO3-, and leaf and root functional traits were measured for eight grass species sampled at three grassland sites across Europe, in France, Austria and the UK. Species were grown in hydroponics to determine functional traits and kinetic uptake parameters (Imax and Km) under standardized conditions.Key Results Species with high specific leaf area (SLA) and shoot N content, and low leaf and root dry matter content (LDMC and RDMC, respectively), which are traits associated with the exploitative syndrome, had higher uptake and affinity for both N forms. No trade-off was observed in uptake between the two forms of N, and all species expressed a higher preference for NH4+.Conclusions The results support the use of leaf traits, and especially SLA and LDMC, as indicators of the N uptake ability across a broad range of grass species. The difficulties associated with assessing root properties are also highlighted, as root traits were only weakly correlated with leaf traits, and only RDMC and, to a lesser extent, root N content were related to leaf traits.

Intransitive competition is widespread in plant communities and maintains their species richness

Intransitive competition networks, those in which there is no single best competitor, may ensure species coexistence. However, their frequency and importance in maintaining diversity in real-world ecosystems remain unclear. We used two large data sets from drylands and agricultural grasslands to assess: (1) the generality of intransitive competition, (2) intransitivity���richness relationships and (3) effects of two major drivers of biodiversity loss (aridity and land-use intensification) on intransitivity and species richness. Intransitive competition occurred in > 65% of sites and was associated with higher species richness. Intransitivity increased with aridity, partly buffering its negative effects on diversity, but was decreased by intensive land use, enhancing its negative effects on diversity. These contrasting responses likely arise because intransitivity is promoted by temporal heterogeneity, which is enhanced by aridity but may decline with land-use intensity. We show that intransitivity is widespread in nature and increases diversity, but it can be lost with environmental homogenisation.

Seed fate and seedling dynamics after masting in two African rain forest trees

How the effects of biotic factors are moderated by abiotic factors, and their consequences for species interactions, is generally understudied in ecology. A key abiotic feature of forests is regular canopy disturbances that create temporary patches, or ���gaps,��� of above-average light availability. Co-occurring in lowland primary forest of Korup National Park (Cameroon), Microberlinia bisulcata and Tetraberlinia bifoliolata are locally dominant, ectomycorrhizal trees whose seeds share predator guilds in masting years. Here, we experimentally tested the impact of small mammal predators upon seedling abundance, growth, and survivorship. In 2007, we added a fixed density of seeds of each species to exclosures at 48 gap���understory locations across 82.5 ha within a large Microberlinia grove, and at 15 locations outside it. For both species, small mammals removed more seeds in gaps than in understory, whereas this was reversed for seeds killed by invertebrates. Nonetheless, Microberlinia lost twice as many seeds to small mammals, and more to invertebrates in exclosures, than Tetraberlinia, which was more prone to a pathogenic white fungus. After six weeks, both species had greater seedling establishment in gaps than understory, and in exclosures outside compared to exclosures inside the grove. In the subsequent two-year period, seedling growth and survivorship peaked in exclosures in gaps, but Microberlinia had more seedlings' stems clipped by animals than Tetraberlinia, and more than twice the percentage of leaf area damaged. Whereas Microberlinia seedling performance in gaps was inferior to Tetraberlinia inside the grove, outside it Microberlinia had reduced leaf damage, grew taller, and had many more leaves than Tetraberlinia. No evidence was found for ���apparent mutualism��� in the understory as seedling establishment of both species increased away from (>25 m) large stems of either species, pointing to ���apparent competition��� instead. In gaps, Microberlinia seedling establishment was lower near Tetraberlinia than conspecific adults because of context-dependent small mammal satiation. Stage-matrix analysis suggested that protecting Microberlinia from small mammals could increase its population growth rate by 0.06. In the light of prior research we conclude that small mammals and canopy gaps play an important role in promoting species coexistence in this forest, and that their strong interaction contributes to Microberlinia's currently very poor regeneration.

Changes in biodiversity and vegetation composition in the central Swiss Alps during the transition from pristine forest to first farming

Aim: We investigate the response of vegetation composition and plant diversity to increasing land clearance, burning and agriculture at the Mesolithic���Neolithic transition (c. 6400���5000 bc) when first farming was introduced. Location: The Valais, a dry alpine valley in Switzerland. Methods: We combine high-resolution pollen, microscopic charcoal and sedimentological data to reconstruct past vegetation, fire and land use. Pollen evenness, rarefaction-based and accumulation-based palynological richness analyses were used to reconstruct past trends in plant diversity. Results: Our results show that from c. 5500 cal. yr bc, slash-and-burn activities created a more open landscape for agriculture, at the expense of Pinus and Betula forests. Land clearance by slash-and-burn promoted diverse grassland ecosystems, while on the long term it reduced woodland and forest diversity, affecting important tree species such as Ulmus and Tilia. Main conclusions: Understanding the resilience of Alpine ecosystems to past disturbance variability is relevant for future nature conservation plans. Our study suggests that forecasted land abandonment in the Alps will lead to pre-Neolithic conditions, with significant biodiversity losses in abandoned grassland ecosystems. Thus, management measures for biodiversity, such as ecological compensation areas, are needed in agricultural landscapes with a millennial history of human impact, such as the non-boreal European lowlands. Our study supports the hypothesis that species coexistence is maximized at an intermediate level of disturbances. For instance, species richness decreased when fire exceeded the quasi-natural variability observed during the Mesolithic times. Under a more natural disturbance regime, rather closed Pinus sylvestris and mixed oak forests would prevail.

Chapter Six ��� Individual Trait Variation and Diversity in Food Webs

In recent years, there has been a renewed interest in the ecological consequences of individual trait variation within populations. Given that individual variability arises from evolutionary dynamics, to fully understand eco-evolutionary feedback loops, we need to pay special attention to how standing trait variability affects ecological dynamics. There is mounting empirical evidence that intra-specific phenotypic variation can exceed species-level means, but theoretical models of multi-trophic species coexistence typically neglect individual-level trait variability. What is needed are multispecies datasets that are resolved at the individual level that can be used to discriminate among alternative models of resource selection and species coexistence in food webs. Here, using one the largest individual-based datasets of a food web compiled to date, along with an individual trait-based stochastic model that incorporates Approximate Bayesian computation methods, we document intra-population variation in the strength of prey selection by different classes or predator phenotypes which could potentially alter the diversity and coexistence patterns of food webs. In particular, we found that strongly connected individual predators preferentially consumed common prey, whereas weakly connected predators preferentially selected rare prey. Such patterns suggest that food web diversity may be governed by the distribution of predator connectivity and individual trait variation in prey selection. We discuss the consequences of intra-specific variation in prey selection to assess fitness differences among predator classes (or phenotypes) and track longer term food web patterns of coexistence accounting for several phenotypes within each prey and predator species.

Herbivores differentially limit the seedling growth and sapling recruitment of two dominant rain forest trees

Resource heterogeneity may influence how plants are attacked and respond to consumers in multiple ways. Perhaps a better understanding of how this interaction might limit sapling recruitment in tree populations may be achieved by examining species��� functional responses to herbivores on a continuum of resource availability. Here, we experimentally reduced herbivore pressure on newly established seedlings of two dominant masting trees in 40 canopy gaps, across c. 80 ha of tropical rain forest in central Africa (Korup, Cameroon). Mesh cages were built to protect individual seedlings, and their leaf production and changes in height were followed for 22 months. With more light, herbivores increasingly prevented the less shade-tolerant Microberlinia bisulcata from growing as tall as it could and producing more leaves, indicating an undercompensation. The more shade-tolerant Tetraberlinia bifoliolata was much less affected by herbivores, showing instead near to full compensation for leaf numbers, and a negligible to weak impact of herbivores on its height growth. A stage-matrix model that compared control and caged populations lent evidence for a stronger impact of herbivores on the long-term population dynamics of M. bisulcata than T. bifoliolata. Our results suggest that insect herbivores can contribute to the local coexistence of two abundant tree species at Korup by disproportionately suppressing sapling recruitment of the faster-growing dominant via undercompensation across the light gradient created by canopy disturbances. The functional patterns we have documented here are consistent with current theory, and, because gap formations are integral to forest regeneration, they may be more widely applicable in other tropical forest communities. If so, the interaction between life-history and herbivore impact across light gradients may play a substantial role in tree species coexistence.

Intraspecific Aggregation Alters Competitive Interactions in Experimental Plant Communities

We tested the prediction from spatial competition models that intraspecific aggregation may promote coexistence and thus maintain biodiversity with experimental communities of four annual species. Monocultures, three-species mixtures, and the four-species mixture were sown at two densities and with either random or intraspecifically aggregated distributions. There was a hierarchy of competitive abilities among the four species. The weaker competitors showed higher aboveground biomass in the aggregated distribution compared to the random distribution, especially at high density. In one species, intraspecific aggregation resulted in an 86% increase in the number of flowering individuals and a 171% increase in the reproductive biomass at high density. The competitively superior species had a lower biomass in the aggregated distribution than in the random distribution at high density. The data support the hypothesis that the spatial distribution of plants profoundly affects competition in such a way that weaker competitors increase their fitness while stronger competitors are suppressed when grown in the neighborhood of conspecifics. This implies that the spatial arrangement of plants in a community can be an important determinant of species coexistence and biodiversity.

Density-dependent dynamics of a dominant rain forest tree change with juvenile stage and time of masting

Although negative density dependence (NDD) can facilitate tree species coexistence in forests, the underlying mechanisms can differ, and rarely are the dynamics of seedlings and saplings studied together. Herein we present and discuss a novel mechanism based on our investigation of NDD predictions for the large, grove-forming ectomycorrhizal mast fruiting tree, Microberlinia bisulcata (Caesalpiniaceae), in an 82.5-ha plot at Korup, Cameroon. We tested whether juvenile density, size, growth and survival decreases with increasing conspecific adult basal area for 3245 ���new��� seedlings and 540 ���old��� seedlings (< 75-cm tall) during an approximately 4-year study period (2008���2012) and for 234 ���saplings��� (��� 75-cm tall) during an approximately 6-year study period (2008���2014). We found that the respective densities of new seedlings, old seedlings and saplings were positively, not and negatively related to increasing BA. Maximum leaf numbers and heights of old seedlings were negatively correlated with increasing basal areas, as were sapling heights and stem diameters. Whereas survivorship of new seedlings decreased by more than one-half with increasing basal area over its range in 2010���2012, that of old seedlings decreased by almost two-thirds, but only in 2008���2010, and was generally unrelated to conspecific seedling density. In 2010���2012 relative growth rates in new seedlings��� heights decreased with increasing basal area, as well as with increasing seedling density, together with increasing leaf numbers, whereas old seedlings��� growth was unrelated to either conspecific density or basal area. Saplings of below-average height had reduced survivorship with increasing basal area (probability decreasing from approx. 0.4 to 0.05 over the basal area range tested), but only sapling growth in terms of leaf numbers decreased with increasing basal area. These static and dynamic results indicate that NDD is operating within this system, possibly stabilizing the M. bisulcata population. However, these NDD patterns are unlikely to be caused by symmetric competition or by consumers. Instead, an alternative mechanism for conspecific adult���juvenile negative feedback is proposed, one which involves the interaction between tree phenology and ectomycorrhizal linkages.

Changes in species composition in alpine snowbeds with climate change inferred from small-scale spatial patterns

Alpine snowbeds are characterised by a very short growing season. However, the length of the snow-free period is increasingly prolonged due to climate change, so that snowbeds become susceptible to invasions from neighbouring alpine meadow communities. We hypothesised that spatial distribution of species generated by plant interactions may indicate whether snowbed species will coexist with or will be out-competed by invading alpine species ��� spatial aggregation or segregation will point to coexistence or competitive exclusion, respectively. We tested this hypothesis in snowbeds of the Swiss Alps using the variance ratio statistics. We focused on the relationships between dominant snowbed species, subordinate snowbed species, and potentially invading alpine grassland species. Subordinate snowbed species were generally spatially aggregated with each other, but were segregated from alpine grassland species. Competition between alpine grassland and subordinate snowbed species may have caused this segregation. Segregation between these species groups increased with earlier snowmelt, suggesting an increasing importance of competition with climate change. Further, a dominant snowbed species (Alchemilla pentaphyllea) was spatially aggregated with subordinate snowbed species, while two other dominants (Gnaphalium supinum and Salix herbacea) showed aggregated patterns with alpine grassland species. These dominant species are known to show distinct microhabitat preferences suggesting the existence of hidden microhabitats with different susceptibility to invaders. These results allow us to suggest that alpine snowbed areas are likely to be reduced as a consequence of climate change and that invading species from nearby alpine grasslands could outcompete subordinate snowbed species. On the other hand, microhabitats dominated by Gnaphalium or Salix seem to be particularly prone to invasions by non-snowbed species.