Species pool, local assembly processes: Disentangling the mechanisms determining bacterial α- and ß-diversity during forest secondary succession.

Across ecology, and particularly within microbial ecology, there is limited understanding how the generation and maintenance of diversity. Although recent work has shown that both local assembly processes and species pools are important in structuring microbial communities, the relative contributions of these mechanisms remain an important question. Moreover, the roles of local assembly processes and species pools are drastically different when explicitly considering the potential for saturation or unsaturation, yet this issue is rarely addressed. Thus, we established a conceptual model that incorporated saturation theory into the microbiological domain to advance the understanding of mechanisms controlling soil bacterial diversity during forest secondary succession. Conceptual model hypotheses were tested by coupling soil bacterial diversity, local assembly processes and species pools using six different forest successional chronosequences distributed across multiple climate zones. Consistent with the unsaturated case proposed in our conceptual framework, we found that species pool consistently affected α-diversity, even while local assembly processes on local richness operate. In contrast, the effects of species pool on ß-diversity disappeared once local assembly processes were taken into account, and changes in environmental conditions during secondary succession led to shifts in ß-diversity through mediation of the strength of heterogeneous selection. Overall, this study represents one of the first to demonstrate that most local bacterial communities might be unsaturated, where the effect of species pool on α-diversity is robust to the consideration of multiple environmental influences, but ß-diversity is constrained by environmental selection.

The neglected roles of adjacent natural ecosystems in maintaining bacterial diversity in agroecosystems.

A central aim of community ecology is to understand how local species diversity is shaped. Agricultural activities are reshaping and filtering soil biodiversity and communities; however, ecological processes that structure agricultural communities have often overlooked the role of the regional species pool, mainly owing to the lack of large datasets across several regions. Here, we conducted a soil survey of 941 plots of agricultural and adjacent natural ecosystems (e.g., forest, wetland, grassland, and desert) in 38 regions across diverse climatic and soil gradients to evaluate whether the regional species pool of soil microbes from adjacent natural ecosystems is important in shaping agricultural soil microbial diversity and completeness. Using a framework of multiscales community assembly, we revealed that the regional species pool was an important predictor of agricultural bacterial diversity and explained a unique variation that cannot be predicted by historical legacy, large-scale environmental factors, and local community assembly processes. Moreover, the species pool effects were associated with microbial dormancy potential, where taxa with higher dormancy potential exhibited stronger species pool effects. Bacterial diversity in regions with higher agricultural intensity was more influenced by species pool effects than that in regions with low intensity, indicating that the maintenance of agricultural biodiversity in high-intensity regions strongly depends on species present in the surrounding landscape. Models for community completeness indicated the positive effect of regional species pool, further implying the community unsaturation and increased potential in bacterial diversity of agricultural ecosystems. Overall, our study reveals the indubitable role of regional species pool from adjacent natural ecosystems in predicting bacterial diversity, which has useful implication for biodiversity management and conservation in agricultural systems.

Local Community Assembly Mechanisms and the Size of Species Pool Jointly Explain the Beta Diversity of Soil Fungi.

Fungi play vital regulatory roles in terrestrial ecosystems. Local community assembly mechanisms, including deterministic and stochastic processes, as well as the size of regional species pools (gamma diversity), typically influence overall soil microbial community beta diversity patterns. However, there is limited evidence supporting their direct and indirect effects on beta diversity of different soil fungal functional groups in forest ecosystems. To address this gap, we collected 1606 soil samples from a 25-ha subtropical forest plot in southern China. Our goal was to determine the direct effects and indirect effects of regional species pools on the beta diversity of soil fungi, specifically arbuscular mycorrhizal (AM), ectomycorrhizal (EcM), plant-pathogenic, and saprotrophic fungi. We quantified the effects of soil properties, mycorrhizal tree abundances, and topographical factors on soil fungal diversity. The beta diversity of plant-pathogenic fungi was predominantly influenced by the size of the species pool. In contrast, the beta diversity of EcM fungi was primarily driven indirectly through community assembly processes. Neither of them had significant effects on the beta diversity of AM and saprotrophic fungi. Our results highlight that the direct and indirect effects of species pools on the beta diversity of soil functional groups of fungi can significantly differ even within a relatively small area. They also demonstrate the independent and combined effects of various factors in regulating the diversities of soil functional groups of fungi. Consequently, it is crucial to study the fungal community not only as a whole but also by considering different functional groups within the community.

Phylogenetic and functional clustering illustrate the roles of adaptive radiation and dispersal filtering in jointly shaping late-Quaternary mammal assemblages on oceanic islands.

Islands frequently harbour unique assemblages of species, yet their ecological roles and differences are largely ignored in island biogeography studies. Here, we examine eco-evolutionary processes structuring mammal assemblages on oceanic islands worldwide, including all extant and extinct late-Quaternary mammal species. We find island mammal assemblages tend to be phylogenetically clustered (share more recent evolutionary histories), with clustering increasing with island area and isolation. We also observe that mammal assemblages often tend to be functionally clustered (share similar traits), but the strength of clustering is weak and generally independent from island area or isolation. These findings indicate the important roles of in situ speciation and dispersal filtering in shaping island mammal assemblages under pre-anthropogenic conditions, notably through adaptive radiation of a few clades (e.g. bats, with generally high dispersal abilities). Our study demonstrates that considering the functional and phylogenetic axes of diversity can better reveal the eco-evolutionary processes of island community assembly.

We should not necessarily expect positive relationships between biodiversity and ecosystem functioning in observational field data.

Our current, empirical understanding of the relationship between biodiversity and ecosystem function is based on two information sources. First, controlled experiments which show generally positive relationships. Second, observational field data which show variable relationships. This latter source coupled with a lack of observed declines in local biodiversity has led to the argument that biodiversity-ecosystem functioning relationships may be uninformative for conservation and management. We review ecological theory and re-analyse several biodiversity datasets to argue that ecosystem function correlations with local diversity in observational field data are often difficult to interpret in the context of biodiversity-ecosystem function research. This occurs because biotic interactions filter species during community assembly which means that there can be a high biodiversity effect on functioning even with low observed local diversity. Our review indicates that we should not necessarily expect any specific relationship between local biodiversity and ecosystem function in observational field data. Rather, linking predictions from biodiversity-ecosystem function theory and experiments to observational field data requires considering the pool of species available during colonisation: the local species pool. We suggest that, even without local biodiversity declines, biodiversity loss at regional scales-which determines local species pools-may still negatively affect ecosystem functioning.

Greater local diversity under older species pools may arise from enhanced competitive equivalence.

Ecological communities typically contain more species when located within geologically older regions. This pattern is traditionally attributed to the long-term accumulation of species in the regional species pool, with local species interactions playing a minor role. We provide evidence suggesting a more important role of local species interactions than generally assumed. We assembled 320 communities of root-associated fungi under 80 species pools, varying species pool richness and the mean age of the sites from which the fungi were collected across a 4-myr soil chronosequence. We found that local diversity increased more with increasing species pool richness when species were from older sites. We also found that older species pools had lower functional and phylogenetic diversity, indicating greater competitive equivalence among species. Our results suggest that older regions have higher local richness not simply because older pools are more speciose but also because species have evolved traits that allow them to locally co-occur.

Observed Ecological Communities Are Formed by Species Combinations That Are among the Most Likely to Persist under Changing Environments.

AbstractDespite the rich biodiversity found in nature, it is unclear to what extent some combinations of interacting species, while conceivable in a given place and time, may never be realized. Yet solving this problem is important for understanding the role of randomness and predictability in the assembly of ecological communities. Here we show that the specific combinations of interacting species that emerge from the ecological dynamics within regional species pools are not all equally likely to be seen; rather, they are among the most likely to persist under changing environments. First, we use niche-based competition matrices and Lotka-Volterra models to demonstrate that realized combinations of interacting species are more likely to persist under random parameter perturbations than the majority of potential combinations with the same number of species that could have been formed from the regional pool. We then corroborate our theoretical results using a 10-year observational study, recording 88 plant-herbivore communities across three different forest successional stages. By inferring and validating plant-mediated communities of competing herbivore species, we find that observed combinations of herbivores have an expected probability of species persistence higher than half of all potential combinations. Our findings open up the opportunity to establish a formal probabilistic and predictive understanding of the composition of ecological communities.

Disturbed habitats locally reduce the signal of deep evolutionary history in functional traits of plants.

The functioning of present ecosystems reflects deep evolutionary history of locally cooccurring species if their functional traits show high phylogenetic signal (PS). However, we do not understand what drives local PS. We hypothesize that local PS is high in undisturbed and stressful habitats, either due to ongoing local assembly of species that maintained ancestral traits, or to past evolutionary maintenance of ancestral traits within habitat species-pools, or to both. We quantified PS and diversity of 10 traits within 6704 local plant communities across 38 Dutch habitat types differing in disturbance or stress. Mean local PS varied 50-fold among habitat types, often independently of phylogenetic or trait diversity. Mean local PS decreased with disturbance but showed no consistent relationship to stress. Mean local PS exceeded species-pool PS, reflecting nonrandom subsampling from the pool. Disturbance or stress related more strongly to mean local than to species-pool PS. Disturbed habitats harbour species with evolutionary divergent trait values, probably driven by ongoing, local assembly of species: environmental fluctuations might maintain different trait values within lineages through an evolutionary storage effect. If functional traits do not reflect phylogeny, ecosystem functioning might not be contingent on the presence of particular lineages, and lineages might establish evolutionarily novel interactions.

Plant community responses to grassland restoration efforts across a large-scale precipitation gradient.

Identifying how plant species diversity varies across environmental gradients remains a controversial topic in plant community ecology because of complex interactions among putative factors. This is especially true for grasslands where habitat loss has limited opportunities for systematic study across broad spatial scales. Here we overcome these limitations by examining restored plant community responses to a large-scale precipitation gradient under two common Conservation Reserve Program (CRP) restoration approaches. The two restoration strategies examined were CP2, which seeds a relatively low number of species, and CP25, which seeds a higher number of species. We sampled plant communities on 55 CRP fields distributed along a broad precipitation gradient (410-1,170 mm mean annual precipitation) spanning 650 km within the grassland biome of North America. Mean annual precipitation (MAP) was the most important predicator of plant species richness and had a positive, linear response across the gradient. To a lesser degree, restoration practices also played a role in determining community diversity. The linear increase in species richness across the precipitation gradient reflects the species pool increase from short to tallgrass prairie communities and explained most of the richness variation. These findings provide insight into the diversity constraints and fundamental drivers of change across a large-scale gradient representing a wide variety of grassland habitats. Across a broad environmental gradient, initial planting differences between restoration practices had lower effects on plant diversity than expected. This suggests that new strategies are needed to effectively establish diverse plant communities on large-scale restorations such as these.

Reducing dispersal limitation via seed addition increases species richness but not above-ground biomass.

Seed dispersal limitation, which can be exacerbated by a number of anthropogenic causes, can result in local communities having fewer species than they might potentially support, representing a potential diversity deficit. The link between processes that shape natural variation in diversity, such as dispersal limitation, and the consequent effects on productivity is less well known. Here, we synthesised data from 12 seed addition experiments in grassland communities to examine the influence of reducing seed dispersal limitation (from 1 to 60 species added across experiments) on species richness and productivity. For every 10 species of seed added, we found that species richness increased by about two species. However, the increase in species richness by overcoming seed limitation did not lead to a concomitant increase in above-ground biomass production. This highlights the need to consider the relationship between biodiversity and ecosystem functioning in a pluralistic way that considers both the processes that shape diversity and productivity simultaneously in naturally assembled communities.

Biogeographic historical legacies in the net primary productivity of Northern Hemisphere forests.

It has been suggested that biogeographic historical legacies in plant diversity may influence ecosystem functioning. This is expected because of known diversity effects on ecosystem functions, and impacts of historical events such as past climatic changes on plant diversity. However, empirical evidence for a link between biogeographic history and present-day ecosystem functioning is still limited. Here, we explored the relationships between Late-Quaternary climate instability, species-pool size, local species and functional diversity, and the net primary productivity (NPP) of Northern Hemisphere forests using structural equation modelling. Our study confirms that past climate instability has negative effects on plant functional diversity and through that on NPP, after controlling for present-day climate, soil conditions, stand biomass and age. We conclude that global models of terrestrial plant productivity need to consider the biogeographical context to improve predictions of plant productivity and feedbacks with the climate system.

Temporal lags in observed and dark diversity in the Anthropocene.

Understanding biodiversity changes in the Anthropocene (e.g. due to climate and land-use change) is an urgent ecological issue. This important task is challenging because global change effects and species responses are dependent on the spatial scales considered. Furthermore, responses are often not immediate. However, both scale and time delay issues can be tackled when, at each study site, we consider dynamics in both observed and dark diversity. Dark diversity includes those species in the region that can potentially establish and thrive in the local sites' conditions but are currently locally absent. Effectively, dark diversity connects biodiversity at the study site to the regional scales and defines the site-specific species pool (observed and dark diversity together). With dark diversity, it is possible to decompose species gains and losses into two space-related components: one associated with local dynamics (species moving from observed to dark diversity and vice versa) and another related to gains and losses of site-specific species pool (species moving to and from the pool after regional immigration, regional extinction or change in local ecological conditions). Extinction debt and immigration credit are useful to understand dynamics in observed diversity, but delays might happen in species pool changes as well. In this opinion piece we suggest that considering both observed and dark diversity and their temporal dynamics provides a deeper understanding of biodiversity changes. Considering both observed and dark diversity creates opportunities to improve conservation by allowing to identify species that are likely to go regionally extinct as well as foreseeing which of the species that newly arrive to the region are more likely to colonize local sites. Finally, by considering temporal lags and species gains and losses in observed and dark diversity, we combine phenomena at both spatial and temporal scales, providing a novel tool to examine biodiversity change in the Anthropocene.

Beta Diversity Patterns Derived from Island Biogeography Theory.

Metacommunity theory and its constituent theory of island biogeography (TIB) have the potential to unify ecology across different scales. The TIB has been successful in predicting alpha diversity patterns, such as species-area relationships and species-abundance distributions, but lags behind in predicting spatial beta diversity patterns. In this study we use island biogeography theory as the starting point to integrate spatial beta diversity patterns into metacommunity theory. We first derive theoretical predictions for the expected beta diversity patterns under the classic MacArthur and Wilson framework, where all species have equal colonization and extinction rates. We then test these predictions for the avian community composition of 42 islands (and 93 species) in Thousand Island Lake, China. Our theoretical results corroborate that longer distance and smaller area lead to higher beta diversity and further reveal that pairwise beta diversity is independent of the size of the mainland species pool. We also find that for the partitioned pairwise beta diversity components, the turnover component increases with the ratio of extinction rates and colonization rates, while the nestedness component is a unimodal function of the ratio of extinction rates and colonization rates. For the empirical island system, we find that beta diversity patterns better distinguish a species-equivalent model from a species-nonequivalent model than alpha diversity patterns. Our findings suggest that beta diversity patterns provide a powerful tool in detecting nonneutral processes, and our model has the potential to incorporate more biological realism in future analyses.

Effects of landscape complexity on pollinators are moderated by pollinators' association with mass-flowering crops.

Conserving and restoring semi-natural habitat, i.e. enhancing landscape complexity, is one of the main strategies to mitigate pollinator decline in agricultural landscapes. However, we still have limited understanding of how landscape complexity shapes pollinator communities in both crop and non-crop habitat, and whether pollinator responses to landscape complexity vary with their association with mass-flowering crops. Here, we surveyed pollinator communities on mass-flowering leek crops and in nearby semi-natural habitat in landscapes of varying complexity. Surveys were done before and during crop bloom and distinguished between pollinators that visit the crop frequently (dominant), occasionally (opportunistic), or not at all (non-crop). Forty-seven per cent of the species in the wider landscape were also observed on leek flowers. Crop pollinator richness increased with local pollinator community size and increasing landscape complexity, but relationships were stronger for opportunistic than for dominant crop pollinators. Relationships between pollinator richness in semi-natural habitats and landscape complexity differed between groups with the most pronounced positive effects on non-crop pollinators. Our results indicate that while dominant crop pollinators are core components of crop pollinator communities in all agricultural landscapes, opportunistic crop pollinators largely determine species-richness responses and complex landscapes are local hotspots for both biodiversity conservation and potential ecosystem service provision.

Lifetime productivity of tree cavities used by cavity-nesting animals in temperate and subtropical forests.

Tree cavities are a critical multi-annual resource that can limit populations and structure communities of cavity-nesting vertebrates. We examined the regional and local factors influencing lifetime productivity (number and richness of occupants) of individual tree cavities across two divergent forest ecosystems: temperate mixed forest in Canada and subtropical Atlantic Forest, Argentina. We predicted that (1) species would accumulate more rapidly within cavities in the species-rich system (Argentina: 76 species) than the poorer system (Canada: 31 species), (2) cavity characteristics associated with nest-site selection in short-term studies would predict lifetime cavity productivity, and (3) species would accumulate more rapidly across highly used cavities than across cavities used only once, and in Argentina than in Canada. We monitored and measured nesting cavities used by birds and mammals over 22 breeding seasons (1995-2016) in Canada and 12 breeding seasons (2006-2017) in Argentina. Cavities were used an average of 3.1 times by 1.7 species in Canada and 2.2 times by 1.4 species in Argentina. Species richness within cavities increased with number of nesting events at similar rates in Canada and Argentina, in both cases much slower than expected if within-cavity species assemblages were random, suggesting that lifetime richness of individual cavities is more strongly influenced by local ecological factors (nest site fidelity, nest niche) than by the regional species pool. The major determinant of lifetime cavity productivity was the cavity's life span. We found only weak or inconsistent relationships with cavity characteristics selected by individuals in short-term nest-site selection studies. Turnover among (vs. within) cavities was the primary driver of diversity at the landscape scale. In Canada, as predicted, species accumulation was fastest when sampling across high-use cavities. In Argentina, the rates of species accumulation were similar across high- and low-use cavities, and fastest when both high- and low-use cavities were pooled. These findings imply that biodiversity of cavity nesters is maintained by a mix of long-lived (highly productive, legacy trees) and many high-turnover (single-use, fast decaying) tree cavities. Conservation of both long-lasting and single-use cavities should be incorporated into decisions about stand-level forest management, regional land use policies, and reserve networks.

Eco-Evolutionary Buffering: Rapid Evolution Facilitates Regional Species Coexistence despite Local Priority Effects.

Inhibitory priority effects, in which early-arriving species exclude competing species from local communities, are thought to enhance regional species diversity via community divergence. Theory suggests, however, that these same priority effects make it difficult for species to coexist in the region unless individuals are continuously supplied from an external species pool, often an unrealistic assumption. Here we develop an eco-evolutionary hypothesis to solve this conundrum. We build a metacommunity model in which local priority effects occur between two species via interspecific interference. Within each species there are two genotypes: one is more resistant to interspecific interference than the other but pays a fitness cost for its resistance. Because of this trade-off, species evolve to become less resistant as they become regionally more common. Rare species can then invade some local patches and consequently recover in regional frequency. This "eco-evolutionary buffering" enables the regional coexistence of species despite local priority effects, even in the absence of immigration from an external species pool. Our model predicts that eco-evolutionary buffering is particularly effective when local communities are small and connected by infrequent dispersal.

Integrating species traits into species pools.

Despite decades of research on the species-pool concept and the recent explosion of interest in trait-based frameworks in ecology and biogeography, surprisingly little is known about how spatial and temporal changes in species-pool functional diversity (SPFD) influence biodiversity and the processes underlying community assembly. Current trait-based frameworks focus primarily on community assembly from a static regional species pool, without considering how spatial or temporal variation in SPFD alters the relative importance of deterministic and stochastic assembly processes. Likewise, species-pool concepts primarily focus on how the number of species in the species pool influences local biodiversity. However, species pools with similar richness can vary substantially in functional-trait diversity, which can strongly influence community assembly and biodiversity responses to environmental change. Here, we integrate recent advances in community ecology, trait-based ecology, and biogeography to provide a more comprehensive framework that explicitly considers how variation in SPFD, among regions and within regions through time, influences the relative importance of community assembly processes and patterns of biodiversity. First, we provide a brief overview of the primary ecological and evolutionary processes that create differences in SPFD among regions and within regions through time. We then illustrate how SPFD may influence fundamental processes of local community assembly (dispersal, ecological drift, niche selection). Higher SPFD may increase the relative importance of deterministic community assembly when greater functional diversity in the species pool increases niche selection across environmental gradients. In contrast, lower SPFD may increase the relative importance of stochastic community assembly when high functional redundancy in the species pool increases the influence of dispersal history or ecological drift. Next, we outline experimental and observational approaches for testing the influence of SPFD on assembly processes and biodiversity. Finally, we highlight applications of this framework for restoration and conservation. This species-pool functional diversity framework has the potential to advance our understanding of how local- and regional-scale processes jointly influence patterns of biodiversity across biogeographic regions, changes in biodiversity within regions over time, and restoration outcomes and conservation efforts in ecosystems altered by environmental change.

Shifts in the importance of the species pool and environmental controls of epiphytic bryophyte richness across multiple scales.

Species richness is influenced by a nested set of environmental factors, but how do these factors interact across several scales? Our main aim is to disentangle the relative importance of environmental filters and the species pool on the richness of epiphytic bryophytes across spatial scales. To do so, we sampled epiphytic bryophytes in 43 oak forests across the northwest of the Iberian Peninsula. As predictors we used climate, descriptors of forest structure and micro-environment. We applied structural equation modeling to relate these variables with richness and cover at three scales: locality (forest), stand (three stands per forest), and sample (a quadrate in a tree). We assumed top-down relationships, so that large-scale variables influenced lower scale variables, and in which cover directly influenced richness. Richness at the next larger scale (locality to stand and stand to sample) is considered a surrogate of the species pool and included as a predictor of richness at the next smaller scale. Environmental variables explain locality richness, but as we decrease the spatial scale, its importance decreases and the dependence on species pool increases. In addition, we found unexpected bottom-up relationships (between micro-scale environment to locality richness). Our results point to the scale dependence of niche vs. neutral processes: niche processes are important at the locality (forest) scale, while neutral processes are significant at the small (sample) scale. We propose a modified conceptualization of the factors influencing biodiversity at different spatial scales by adding links across different scales (between micro-environment and locality-scale richness in our study).

Historical biome distribution and recent human disturbance shape the diversity of arbuscular mycorrhizal fungi.

The availability of global microbial diversity data, collected using standardized metabarcoding techniques, makes microorganisms promising models for investigating the role of regional and local factors in driving biodiversity. Here we modelled the global diversity of symbiotic arbuscular mycorrhizal (AM) fungi using currently available data on AM fungal molecular diversity (small subunit (SSU) ribosomal RNA (rRNA) gene sequences) in field samples. To differentiate between regional and local effects, we estimated species pools (sets of potentially suitable taxa) for each site, which are expected to reflect regional processes. We then calculated community completeness, an index showing the fraction of the species pool present, which is expected to reflect local processes. We found significant spatial variation, globally in species pool size, as well as in local and dark diversity (absent members of the species pool). Species pool size was larger close to areas containing tropical grasslands during the last glacial maximum, which are possible centres of diversification. Community completeness was greater in regions of high wilderness (remoteness from human disturbance). Local diversity was correlated with wilderness and current connectivity to mountain grasslands. Applying the species pool concept to symbiotic fungi facilitated a better understanding of how biodiversity can be jointly shaped by large-scale historical processes and recent human disturbance.

Characterizing fish responses to a river restoration over 21 years based on species' traits.

Understanding restoration effectiveness is often impaired by a lack of high-quality, long-term monitoring data and, to date, few researchers have used species' trait information to gain insight into the processes that drive the reaction of fish communities to restoration. We examined fish-community responses with a highly resolved data set from 21 consecutive years of electrofishing (4 years prerestoration and 17 years postrestoration) at multiple restored and unrestored reaches from a river restoration project on the Lippe River, Germany. Fish abundance peaked in the third year after the restoration; abundance was 6 times higher than before the restoration. After 5-7 years, species richness and abundance stabilized at 2 and 3.5 times higher levels relative to the prerestoration level, respectively. However, interannual variability of species richness and abundance remained considerable, illustrating the challenge of reliably assessing restoration outcomes based on data from individual samplings, especially in the first years following restoration. Life-history and reproduction-related traits best explained differences in species' responses to restoration. Opportunistic short-lived species with early female maturity and multiple spawning runs per year exhibited the strongest increase in abundance, which reflected their ability to rapidly colonize new habitats. These often small-bodied and fusiform fishes typically live in dynamic and ephemeral instream and floodplain areas that river-habitat restorations often aim to create, and in this case their increases in abundance indicated successful restoration. Our results suggest that a greater consideration of species' traits may enhance the causal understanding of community processes and the coupling of restoration to functional ecology. Trait-based assessments of restoration outcomes would furthermore allow for easier transfer of knowledge across biogeographic borders than studies based on taxonomy.