Reciprocal inhibition and competitive hierarchy cause negative biodiversity-ecosystem function relationships.

The relationship between biodiversity and ecosystem function (BEF) captivates ecologists, but the factors responsible for the direction of this relationship remain unclear. While higher ecosystem functioning at higher biodiversity levels ('positive BEF') is not universal in nature, negative BEF relationships seem puzzlingly rare. Here, we develop a dynamical consumer-resource model inspired by microbial decomposer communities in pitcher plant leaves to investigate BEF. We manipulate microbial diversity via controlled colonization and measure their function as total ammonia production. We test how niche partitioning among bacteria and other ecological processes influence BEF in the leaves. We find that a negative BEF can emerge from reciprocal interspecific inhibition in ammonia production causing a negative complementarity effect, or from competitive hierarchies causing a negative selection effect. Absent these factors, a positive BEF was the typical outcome. Our findings provide a potential explanation for the rarity of negative BEF in empirical data.

Predator dispersal influences predator distribution but not prey diversity in pitcher plant microbial metacommunities.

The spatial distribution of predators can affect both the distribution and diversity of their prey. Therefore, differences in predator dispersal ability that affect their spatial distribution, could also affect prey communities. Here, we use the microbial communities within pitcher plant leaves as a model system to test the relationship between predator (protozoa) dispersal ability and distribution, and its consequences for prey (bacteria) diversity and composition. We hypothesized that limited predator dispersal results in clustered distributions and heterogeneous patches for prey species, whereas wide predator dispersal and distribution could homogenize prey metacommunities. We analyzed the distribution of two prominent bacterivore protozoans from a 2-year survey of an intact field of Sarracenia purpurea pitcher plants, and found a clustered distribution of Tetrahymena and homogeneous distribution of Poterioochromonas. We manipulated the sources of protozoan colonists and recorded protozoan recruitment and bacterial diversity in target leaves in a field experiment. We found the large ciliate, Tetrahymena, was dispersal limited and occupied few leaves, whereas the small flagellate Poterioochromonas was widely dispersed. However, the bacterial communities these protozoans feed on was unaffected by clustering of Tetrahymena, but likely influenced by Poterioochromonas and other bacterivores dispersing in the field. We propose that bacterial communities in this system are structured by a combination of well dispersed bacterivores, bacterial dispersal, and bottom-up mechanisms. Clustered predators could become strong drivers of prey communities if they were specialists or keystone predators, or if they exerted a dominant influence on other predators in top-down controlled systems. Linking dispersal ability within trophic levels and its consequences for trophic dynamics can lead to a more robust perspective on trophic metacommunities.

Effects of Community Richness and Competitive Asymmetry on Protozoa Evolution in Sarracenia purpurea Leaves.

AbstractPredicting evolution in natural systems will require understanding how selection operates in multispecies communities. We predicted that the amount that traits evolve in multispecies mixtures would be less than the amount that would be predicted from the additive contributions of the pairwise interactions and that subordinate species will be more likely to evolve in competitive systems than dominant species. We conducted an experimental test of these predictions using a guild of protozoans found in the water-filled leaves of the pitcher plant Sarracenia purpurea. The response to selection did not significantly change as we increased richness from monocultures to two- and four-species mixtures. In accordance with our second prediction, subordinate species demonstrated greater growth in competition after selection than before, while dominant species generally showed no response to selection. Monod-type experiments to determine minimum resource levels found that the dominant species had much higher resource requirements than the subordinate species and that the minimum resource requirements evolved to be higher in the subordinate species. Importantly, these results suggest that subordinate species evolve to become more similar to dominant species, which may involve resource use convergence. Our findings and other recent works suggest that community diversity can affect evolution in surprising ways that warrant further investigation.

Habitat filters mediate successional trajectories in bacterial communities associated with the striped shore crab.

The relative importance of stochastic- and niche-based processes shifts during successional time and across different types of habitats. Microbial biofilms are known to undergo such successional shifts. However, little is known about the interaction between these successional trajectories and habitat filters. Harsh habitat filters could affect biofilm successional trajectories by strengthening niche-based processes and weakening stochastic processes. We used mesocosms to track successional trajectories in bacterial communities associated with the striped shore crab (Pachygrapsus transversus). We followed replicated microbial communities under strong and weak habitat filters associated with the crab's gut and carapace. For bacteria, colonization of the crab's gut is constrained by strong chemical and physical filtering, while the carapace remains relatively open for colonization. Consistent with successional models of bacterial biofilms, carapace microbial communities initially converged in community composition at day 8 and diverged thereafter. We expected gut microbial communities to deviate from the trajectory in the carapace and converge towards a subset of tolerant species. Instead, bacterial communities in the gut exhibited low richness, unchanging similarity in composition and turnover in species identities throughout the duration of our study. These habitat filter effects were linked with weak species interactions and low influence from colonization in the gut. If these findings are representative of differences in filter strength in a continuum of successional trajectories, habitat filters may provide basis for predictions that link successional models and habitat types.

Species-specific differences determine responses to a resource pulse and predation.

The effects of resource pulses on natural communities are known to vary with the type of pulse. However, less is known about mechanisms that determine the responses of different species to the same pulse. We hypothesized that these differences are related to the size of the species, as increasing size may be correlated with increasing competitive ability and decreasing tolerance to predation. A factorial experiment quantified the magnitude and timing of species' responses to a resource pulse using the aquatic communities found in the leaves of the carnivorous pitcher plant, Sarracenia purpurea. We added prey to leaves and followed the abundances of bacteria and bacterivores (protozoa and rotifers) in the presence and absence of a top predator, larvae of the mosquito Wyeomyia smithii. Resource pulses had significant positive effects on species abundances and diversity in this community; however, the magnitude and timing of responses varied among the bacterivore species and was not related to body size. Larger bacterivores were significantly suppressed by predators, while smaller bacterivores were not; predation also significantly reduced bacterivore species diversity. There were no interactions between the effects of the resource pulse and predation on protozoa abundances. Over 67 days, some species returned to pre-pulse abundances quickly, others did not or did so very slowly, resulting in new community states for extended periods of time. This study demonstrates that species-specific differences in responses to resource pulses and predation are complex and may not be related to simple life history trade-offs associated with size.

Key colonist pools and habitat filters mediate the composition of fiddler crab-associated bacterial communities.

The diversity and composition of local communities depends strongly on the pool of species that have been able to colonize that community from elsewhere. Typically this is thought to depend on a larger regional species pool that is subject to local environmental constraints that act as "filters." Often, however, colonists arrive from multiple sources that differ in habitat conditions and have therefore already experienced distinct "prefiltering." Consequently, it is the interaction of species from these distinct pools that determine the composition of local communities. This interaction is particularly important when certain colonist pools provide keystone species with disproportionate roles on community assembly. We propose to identify these key colonist pools and their interaction with local habitat filters by quantifying community-level responses to colonist pool manipulation. We tested this framework to assess the contribution of surface and burrow sediment bacteria to bacterial communities associated with the fiddler crab, Uca panacea. In a mesocosm experiment, we combined normal and autoclaved surface and burrow sediment in a factorial experimental design, and we evaluated the community-level responses of carapace and gut microbial assemblages to sediment treatments with next-generation sequencing of the 16S rRNA gene. Results from carapace bacterial communities indicate that burrow sediments contribute most recruits, but surface sediments provide a few key colonizers that become established in the carapace community. In contrast, the composition of gut-associated microbial communities responded only to surface bacteria manipulation, despite being highly dissimilar from the community composition in both the surface and burrow source pools. These results suggest that assembly in the gut depends primarily on colonization from the surface sediment and regulation by habitat filtering. For fiddler crab-associated bacteria, we can conclude that key colonist pools and habitat filters regulate the influence of multiple colonist pools. Incorporating and distinguishing the contribution of multiple sources of species, rather than a single regional species pool, may better explain community dynamics in many systems, especially those with weak habitat filters.

Multiple colonist pools shape fiddler crab-associated bacterial communities.

Colonization is a key component of community assembly because it continuously contributes new species that can potentially establish and adds individuals to established populations in local communities. Colonization is determined by the regional species pool, which is typically viewed as stable at ecological time scales. Yet, many natural communities including plants, birds and microbes, are exposed to several distinct and dynamic sources of colonists and how multiple colonist pools interact to shape local communities remains unclear. Using a 16S rRNA amplicon survey, we profiled bacteria within surface, subsurface and burrow sediments and assessed their role as colonist pools for fiddler crab-associated bacteria. We found significant differences in composition among sediment types, driven by halophilic taxa in the surface, and different Desulfobacteraceae taxa in the subsurface and burrow. Bacteria from burrow sediment colonized the crab carapace whereas gut bacterial communities were colonized by burrow and surface sediment bacteria. Despite distinct colonist pools influencing gut bacteria, variation in composition across gut samples did not lead to significant clusters. In contrast, carapace bacterial communities clustered in six distinct groups loosely associated with crab species. Our findings suggest that multiple colonist pools can influence local communities but factors explaining variation in community composition depend on local habitats. Recognizing multiple colonist pools expands our understanding of the interaction between regional and local processes driving community structure and diversity.

Predator identity more than predator richness structures aquatic microbial assemblages in Sarracenia purpurea leaves.

The importance of predators in influencing community structure is a well-studied area of ecology. However, few studies test ecological hypotheses of predation in multi-predator microbial communities. The phytotelmic community found within the water-filled leaves of the pitcher plant, Sarracenia purpurea, exhibits a simple trophic structure that includes multiple protozoan predators and microbial prey. Using this system, we sought to determine whether different predators target distinct microorganisms, how interactions among protozoans affect resource (microorganism) use, and how predator diversity affects prey community diversity. In particular, we endeavored to determine if protozoa followed known ecological patterns such as keystone predation or generalist predation. For these experiments, replicate inquiline microbial communities were maintained for seven days with five protozoan species. Microbial community structure was determined by 16S rRNA gene amplicon sequencing (iTag) and analysis. Compared to the control (no protozoa), two ciliates followed patterns of keystone predation by increasing microbial evenness. In pairwise competition treatments with a generalist flagellate, prey communities resembled the microbial communities of the respective keystone predator in monoculture. The relative abundance of the most common bacterial Operational Taxonomic Unit (OTU) in our system decreased compared to the control in the presence of these ciliates. This OTU was 98% similar to a known chitin degrader and nitrate reducer, important functions for the microbial community and the plant host. Collectively, the data demonstrated that predator identity had a greater effect on prey diversity and composition than overall predator diversity.

A shift from exploitation to interference competition with increasing density affects population and community dynamics.

Intraspecific competition influences population and community dynamics and occurs via two mechanisms. Exploitative competition is an indirect effect that occurs through use of a shared resource and depends on resource availability. Interference competition occurs by obstructing access to a resource and may not depend on resource availability. Our study tested whether the strength of interference competition changes with protozoa population density. We grew experimental microcosms of protozoa and bacteria under different combinations of protozoan density and basal resource availability. We then solved a dynamic predator-prey model for parameters of the functional response using population growth rates measured in our experiment. As population density increased, competition shifted from exploitation to interference, and competition was less dependent on resource levels. Surprisingly, the effect of resources was weakest when competition was the most intense. We found that at low population densities, competition was largely exploitative and resource availability had a large effect on population growth rates, but the effect of resources was much weaker at high densities. This shift in competitive mechanism could have implications for interspecific competition, trophic interactions, community diversity, and natural selection. We also tested whether this shift in the mechanism of competition with protozoa density affected the structure of the bacterial prey community. We found that both resources and protozoa density affected the structure of the bacterial prey community, suggesting that competitive mechanism may also affect trophic interactions.