The Effects of Geography, Environment and Phylogeny on Community Assembly and Gene Flow Dynamics

It is increasingly evident that evolutionary processes play a role in how ecological communities are assembled. However the extend to which evolution influences how plants respond to spatial and environmental gradients and interact with each other is less clear. In this dissertation I leverage evolutionary tools and thinking to understand how space and environment affect community composition and patterns of gene flow in a unique system of Atlantic rainforest and restinga (sandy coastal plains) habitats in Southeastern Brazil.

In chapter one I investigate how space and environment affect the population genetic structure and gene flow of Aechmea nudicaulis, a bromeliad species that co-occurs in forest and restinga habitats. I genotyped seven microsatellite loci and sequenced one chloroplast DNA region for individuals collected in 7 pairs of forest / restinga sites. Bayesian genetic clustering analyses show that populations of A. nudicaulis are geographically structured in northern and southern populations, a pattern consistent with broader scale phylogeographic dynamics of the Atlantic rainforest. On the other hand, explicit migration models based on the coalescent estimate that inter-habitat gene flow is less common than gene flow between populations in the same habitat type, despite their geographic discontinuity. I conclude that there is evidence for repeated colonization of the restingas from forest populations even though the steep environmental gradient between habitats is a stronger barrier to gene flow than geographic distance.

In chapter two I use data on 2800 individual plants finely mapped in a restinga plot and on first-year survival of 500 seedlings to understand the roles of phylogeny, functional traits and abiotic conditions in the spatial structuring of that community. I demonstrate that phylogeny is a poor predictor of functional traits in and that convergence in these traits is pervasive. In general, the community is not phylogenetically structured, with at best 14% of the plots deviating significantly from the null model. The functional traits SLA, leaf dry matter content (LDMC), and maximum height also showed no clear pattern of spatial structuring. On the other hand, leaf area is strongly overdispersed across all spatial scales. Although leaf area overdispersion would be generally taken as evidence of competition, I argue that interpretation is probably misleading. Finally, I show that seedling survival is dramatically increased when they grow shaded by an adult individual, suggesting that seedlings are being facilitated. Phylogenetic distance to their adult neighbor has no influence on rates of survival though. Taken together, these results indicate that phylogeny has very limited influence on the fine scale assembly of restinga communities.

Plant community assembly at small scales: spatial versus environmental factors in a central European grassland

Dispersal limitation and environmental conditions are crucial drivers of plant species distribution and establishment. As these factors operate at different spatial scales, we asked: Do the environmental factors known to determine community assembly at broad scales operate at fine scales (few meters)? How much do these factors account for community variation at fine scales? In which way do biotic and abiotic interactions drive changes in species composition? We surveyed the plant community within a dry grassland along a very steep gradient of soil characteristics like pH and nutrients. We used a spatially explicit sampling design, based on three replicated macroplots of 15x15, 12x12 and 12x12 meters in extent. Soil samples were taken to quantify several soil properties (carbon, nitrogen, plant available phosphorus, pH, water content and dehydrogenase activity as a proxy for overall microbial activity). We performed variance partitioning to assess the effect of these variables on plant composition and statistically controlled for spatial autocorrelation via eigenvector mapping. We also applied null model analysis to test for non-random patterns in species co-occurrence using randomization schemes that account for patterns expected under species interactions. At a fine spatial scale, environmental factors explained 18% of variation when controlling for spatial autocorrelation in the distribution of plant species, whereas purely spatial processes accounted for 14% variation. Null model analysis showed that species spatially segregated in a non-random way and these spatial patterns could be due to a combination of environmental filtering and biotic interactions. Our grassland study suggests that environmental factors found to be directly relevant in broad scale studies are present also at small scales, but are supplemented by spatial processes and more direct interactions like competition.

Species divergence and trait convergence in experimental plant community assembly

Despite decades of research, it remains controversial whether ecological communities converge towards a common structure determined by environmental conditions irrespective of assembly history. Here, we show experimentally that the answer depends on the level of community organization considered. In a 9-year grassland experiment, we manipulated initial plant composition on abandoned arable land and subsequently allowed natural colonization. Initial compositional variation caused plant communities to remain divergent in species identities, even though these same communities converged strongly in species traits. This contrast between species divergence and trait convergence could not be explained by dispersal limitation or community neutrality alone. Our results show that the simultaneous operation of trait-based assembly rules and species-level priority effects drives community assembly, making it both deterministic and historically contingent, but at different levels of community organization.

Exploring community assembly through an individual-based model for trophic interactions

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

Trait contributions to fish community assembly emerge from trophic interactions in an individual-based model

Community ecology seeks to understand and predict the characteristics of communities that can develop under different environmental conditions, but most theory has been built on analytical models that are limited in the diversity of species traits that can be considered simultaneously. We address that limitation with an individual-based model to simulate assembly of fish communities characterized by life history and trophic interactions with multiple physiological tradeoffs as constraints on species performance. Simulation experiments were carried out to evaluate the distribution of 6 life history and 4 feeding traits along gradients of resource productivity and prey accessibility. These experiments revealed that traits differ greatly in importance for species sorting along the gradients. Body growth rate emerged as a key factor distinguishing community types and defining patterns of community stability and coexistence, followed by egg size and maximum body size. Dominance by fast-growing, relatively large, and fecund species occurred more frequently in cases where functional responses were saturated (i.e. high productivity and/or prey accessibility). Such dominance was associated with large biomass fluctuations and priority effects, which prevented richness from increasing with productivity and may have limited selection on secondary traits, such as spawning strategies and relative size at maturation. Our results illustrate that the distribution of species traits and the consequences for community dynamics are intimately linked and strictly dependent on how the benefits and costs of these traits are balanced across different conditions. © 2012 Elsevier B.V.

Using plant functional traits and phylogenies to understand patterns of plant community assembly in a seasonal tropical forest in Lao PDR

Plant functional traits reflect different evolutionary responses to environmental variation, and among extant species determine the outcomes of interactions between plants and their environment, including other plant species. Thus, combining phylogenetic and trait-based information can be a powerful approach for understanding community assembly processes across a range of spatial scales. We used this approach to investigate tree community composition at Phou Khao Khouay National Park (18°14’-18°32’N; 102°38’- 102°59’E), Laos, where several distinct forest types occur in close proximity. The aim of our study was to examine patterns of plant community assembly across the strong environmental gradients evident at our site. We hypothesized that differences in tree community composition were being driven by an underlying gradient in soil conditions. Thus, we predicted that environmental filtering would predominate at the site and that the filtering would be strongest on sandier soil with low pH, as these are the conditions least favorable to plant growth. We surveyed eleven 0.25 ha (50x50 m) plots for all trees above 10 cm dbh (1221 individual trees, including 47 families, 70 genera and 123 species) and sampled soils in each plot. For each species in the community, we measured 11 commonly studied plant functional traits covering both the leaf and wood economic spectrum traits and we reconstructed a phylogenetic tree for 115 of the species in the community using rbcL and matK sequences downloaded from Genebank (other species were not available). Finally we compared the distribution of trait values and species at two scales (among plots and 10x10m subplots) to examine trait and phylogenetic community structures. Although there was strong evidence that an underlying soil gradient was determining patterns of species composition at the site, our results did not support the hypothesis that the environmental filtering dominated community assembly processes. For the measured plant functional traits there was no consistent pattern of trait dispersion across the site, either when traits were considered individually or when combined in a multivariate analysis. However, there was a significant correlation between the degree of phylogenetic dispersion and the first principle component axis (PCA1) for the soil parameters.Moreover, the more phylogenetically clustered plots were on sandier soils with lower pH. Hence, we suggest that the community assembly processes across our sitemay reflect the influence ofmore conserved traits that we did not measure. Nevertheless, our results are equivocal and other interpretations are possible. Our study illustrates some difficulties in combining trait and phylogenetic approaches that may result from the complexities of integrating spatial and evolutionary processes that vary at different scales.

Species interactions and random dispersal rather than habitat filtering drive community assembly during early plant succession

Theory on plant succession predicts a temporal increase in the complexity of spatial community structure and of competitive interactions: initially random occurrences of early colonising species shift towards spatially and competitively structured plant associations in later successional stages. Here we use long-term data on early plant succession in a German post mining area to disentangle the importance of random colonisation, habitat filtering, and competition on the temporal and spatial development of plant community structure. We used species co-occurrence analysis and a recently developed method for assessing competitive strength and hierarchies (transitive versus intransitive competitive orders) in multispecies communities. We found that species turnover decreased through time within interaction neighbourhoods, but increased through time outside interaction neighbourhoods. Successional change did not lead to modular community structure. After accounting for species richness effects, the strength of competitive interactions and the proportion of transitive competitive hierarchies increased through time. Although effects of habitat filtering were weak, random colonization and subsequent competitive interactions had strong effects on community structure. Because competitive strength and transitivity were poorly correlated with soil characteristics, there was little evidence for context dependent competitive strength associated with intransitive competitive hierarchies.

Trait Contributions to Fish Community Assembly Emerge From Trophic Interactions in an Individual-Based Model

Community ecology seeks to understand and predict the characteristics of communities that can develop under different environmental conditions, but most theory has been built on analytical models that are limited in the diversity of species traits that can be considered simultaneously. We address that limitation with an individual-based model to simulate assembly of fish communities characterized by life history and trophic interactions with multiple physiological tradeoffs as constraints on species performance. Simulation experiments were carried out to evaluate the distribution of 6 life history and 4 feeding traits along gradients of resource productivity and prey accessibility. These experiments revealed that traits differ greatly in importance for species sorting along the gradients. Body growth rate emerged as a key factor distinguishing community types and defining patterns of community stability and coexistence, followed by egg size and maximum body size. Dominance by fast-growing, relatively large, and fecund species occurred more frequently in cases where functional responses were saturated (i.e. high productivity and/or prey accessibility). Such dominance was associated with large biomass fluctuations and priority effects, which prevented richness from increasing with productivity and may have limited selection on secondary traits, such as spawning strategies and relative size at maturation. Our results illustrate that the distribution of species traits and the consequences for community dynamics are intimately linked and strictly dependent on how the benefits and costs of these traits are balanced across different conditions.

Examining the effects of species richness on community stability: an assembly model approach

We build dynamic models of community assembly by starting with one species in our model ecosystem and adding colonists. We find that the number of species present first increases, then fluctuates about some level. We ask: how large are these fluctuations and how can we characterize them statistically? As in Robert May's work, communities with weaker interspecific interactions permit a greater number of species to coexist on average. We find that as this average increases, however, the relative variation in the number of species and return times to mean community levels decreases. In addition, the relative frequency of large extinction events to small extinction events decreases as mean community size increases. While the model reproduces several of May's results, it also provides theoretical support for Charles Elton's idea that diverse communities such as those found in the tropics should be less variable than depauperate communities such as those found in arctic or agricultural settings.

Positive Relationships between Association Strength and Phenotypic Similarity Characterize the Assembly of Mixed-Species Bird Flocks Worldwide

Competition theory predicts that local communities should consist of species that are more dissimilar than expected by chance. We find a strikingly different pattern in a multicontinent data set (55 presence-absence matrices from 24 locations) on the composition of mixed-species bird flocks, which are important sub-units of local bird communities the world over. By using null models and randomization tests followed by meta-analysis, we find the association strengths of species in flocks to be strongly related to similarity in body size and foraging behavior and higher for congeneric compared with noncongeneric species pairs. Given the local spatial scales of our individual analyses, differences in the habitat preferences of species are unlikely to have caused these association patterns; the patterns observed are most likely the outcome of species interactions. Extending group-living and social-information-use theory to a heterospecific context, we discuss potential behavioral mechanisms that lead to positive interactions among similar species in flocks, as well as ways in which competition costs are reduced. Our findings highlight the need to consider positive interactions along with competition when seeking to explain community assembly.

Primary assembly of soil communities: disentangling the effect of dispersal and local environment

It has long been recognised that dispersal abilities and environmental factors are important in shaping invertebrate communities, but their relative importance for primary soil community assembly has not yet been disentangled. By studying soil communities along chronosequences on four recently emerged nunataks (ice-free land in glacial areas) in Iceland, we replicated environmental conditions spatially at various geographical distances. This allowed us to determine the underlying factors of primary community assembly with the help of metacommunity theories that predict different levels of dispersal constraints and effects of the local environment. Comparing community assembly of the nunataks with that of non-isolated deglaciated areas indicated that isolation of a few kilometres did not affect the colonisation of the soil invertebrates. When accounting for effects of geographical distances, soil age and plant richness explained a significant part of the variance observed in the distribution of the oribatid mites and collembola communities, respectively. Furthermore, null model analyses revealed less co-occurrence than expected by chance and also convergence in the body size ratio of co-occurring oribatids, which is consistent with species sorting. Geographical distances influenced species composition, indicating that the community is also assembled by dispersal, e.g. mass effect. When all the results are linked together, they demonstrate that local environmental factors are important in structuring the soil community assembly, but are accompanied with effects of dispersal that may "override" the visible effect of the local environment.

Relative role of deterministic and stochastic determinants of soil animal community: a spatially explicit analysis of oribatid mites

1. Ecologists are debating the relative role of deterministic and stochastic determinants of community structure. Although the high diversity and strong spatial structure of soil animal assemblages could provide ecologists with an ideal ecological scenario, surprisingly little information is available on these assemblages.
2. We studied species-rich soil oribatid mite assemblages from a Mediterranean beech forest and a grassland. We applied multivariate regression approaches and analysed spatial autocorrelation at multiple spatial scales using Moran's eigenvectors. Results were used to partition community variance in terms of the amount of variation uniquely accounted for by environmental correlates (e.g. organic matter) and geographical position. Estimated neutral diversity and immigration parameters were also applied to a soil animal group for the first time to simulate patterns of community dissimilarity expected under neutrality, thereby testing neutral predictions.
3. After accounting for spatial autocorrelation, the correlation between community structure and key environmental parameters disappeared: about 40% of community variation consisted of spatial patterns independent of measured environmental variables such as organic matter. Environmentally independent spatial patterns encompassed the entire range of scales accounted for by the sampling design (from tens of cm to 100 m). This spatial variation could be due to either unmeasured but spatially structured variables or stochastic drift mediated by dispersal. Observed levels of community dissimilarity were significantly different from those predicted by neutral models.
4. Oribatid mite assemblages are dominated by processes involving both deterministic and stochastic components and operating at multiple scales. Spatial patterns independent of the measured environmental variables are a prominent feature of the targeted assemblages, but patterns of community dissimilarity do not match neutral predictions. This suggests that either niche-mediated competition or environmental filtering or both are contributing to the core structure of the community. This study indicates new lines of investigation for understanding the mechanisms that determine the signature of the deterministic component of animal community assembly.

Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale

Extreme arid regions in the worlds' major deserts are typified by quartz pavement terrain. Cryptic hypolithic communities colonize the ventral surface of quartz rocks and this habitat is characterized by a relative lack of environmental and trophic complexity. Combined with readily identifiable major environmental stressors this provides a tractable model system for determining the relative role of stochastic and deterministic drivers in community assembly. Through analyzing an original, worldwide data set of 16S rRNA-gene defined bacterial communities from the most extreme deserts on the Earth, we show that functional assemblages within the communities were subject to different assembly influences. Null models applied to the photosynthetic assemblage revealed that stochastic processes exerted most effect on the assemblage, although the level of community dissimilarity varied between continents in a manner not always consistent with neutral models. The heterotrophic assemblages displayed signatures of niche processes across four continents, whereas in other cases they conformed to neutral predictions. Importantly, for continents where neutrality was either rejected or accepted, assembly drivers differed between the two functional groups. This study demonstrates that multi-trophic microbial systems may not be fully described by a single set of niche or neutral assembly rules and that stochasticity is likely a major determinant of such systems, with significant variation in the influence of these determinants on a global scale.

The community-level effect of light on germination timing in relation to seed mass: a source of regeneration niche differentiation

Within a community, species may germinate at different times so as to mitigate competition and to take advantage of different aspects of the seasonal environment (temporal niche differentiation). We illustrated a hypothesis of the combined effects of abiotic and biotic competitive factors on germination timing and the subsequent upscale effects on community assembly. We estimated the germination timing (GT) for 476 angiosperm species of the eastern Tibetan Plateau grasslands under two light treatments in the field: high (i.e. natural) light and low light. We also measured the shift in germination timing (SGT) across treatments for all species. Furthermore, we used phylogenetic comparative methods to test if GT and SGT were associated with seed mass, an important factor in competitive interactions. We found a significant positive correlation between GT and seed mass in both light treatments. Additionally, small seeds (early germinating seeds) tended to germinate later and large seeds (late germinating seeds) tended to germinate earlier under low light vs high light conditions. Low light availability can reduce temporal niche differentiation by increasing the overlap in germination time between small and large seeds. In turn, reduced temporal niche differentiation may increase competition in the process of community assembly.