James C. Stegen

Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist.

A recent increase in studies of β diversity has yielded a confusing array of concepts, measures and methods. Here, we provide a roadmap of the most widely used and ecologically relevant approaches for analysis through a series of mission statements. We distinguish two types of β diversity: directional turnover along a gradient vs. non-directional variation. Different measures emphasize different properties of ecological data. Such properties include the degree of emphasis on presence/absence vs. relative abundance information and the inclusion vs. exclusion of joint absences. Judicious use of multiple measures in concert can uncover the underlying nature of patterns in β diversity for a given dataset. A case study of Indonesian coral assemblages shows the utility of a multi-faceted approach. We advocate careful consideration of relevant questions, matched by appropriate analyses. The rigorous application of null models will also help to reveal potential processes driving observed patterns in β diversity.

Disentangling the Drivers of β Diversity Along Latitudinal and Elevational Gradients

Increases in species turnover of woody plants at low latitudes and elevations are explained by the size of species pools alone. Understanding spatial variation in biodiversity along environmental gradients is a central theme in ecology. Differences in species compositional turnover among sites (β diversity) occurring along gradients are often used to infer variation in the processes structuring communities. Here, we show that sampling alone predicts changes in β diversity caused simply by changes in the sizes of species pools. For example, forest inventories sampled along latitudinal and elevational gradients show the well-documented pattern that β diversity is higher in the tropics and at low elevations. However, after correcting for variation in pooled species richness (γ diversity), these differences in β diversity disappear. Therefore, there is no need to invoke differences in the mechanisms of community assembly in temperate versus tropical systems to explain these global-scale patterns of β diversity.

Stochastic and deterministic assembly processes in subsurface microbial communities

A major goal of microbial community ecology is to understand the forces that structure community composition. Deterministic selection by specific environmental factors is sometimes important, but in other cases stochastic or ecologically neutral processes dominate. Lacking is a unified conceptual framework aiming to understand why deterministic processes dominate in some contexts but not others. Here we work toward such a framework. By testing predictions derived from general ecological theory we aim to uncover factors that govern the relative influences of deterministic and stochastic processes. We couple spatiotemporal data on subsurface microbial communities and environmental parameters with metrics and null models of within and between community phylogenetic composition. Testing for phylogenetic signal in organismal niches showed that more closely related taxa have more similar habitat associations. Community phylogenetic analyses further showed that ecologically similar taxa coexist to a greater degree than expected by chance. Environmental filtering thus deterministically governs subsurface microbial community composition. More importantly, the influence of deterministic environmental filtering relative to stochastic factors was maximized at both ends of an environmental variation gradient. A stronger role of stochastic factors was, however, supported through analyses of phylogenetic temporal turnover. Although phylogenetic turnover was on average faster than expected, most pairwise comparisons were not themselves significantly non-random. The relative influence of deterministic environmental filtering over community dynamics was elevated, however, in the most temporally and spatially variable environments. Our results point to general rules governing the relative influences of stochastic and deterministic processes across micro- and macro-organisms.

The Gut Microbiota of Rural Papua New Guineans: Composition, Diversity Patterns, and Ecological Processes

Although recent research revealed an impact of westernization on diversity and composition of the human gut microbiota, the exact consequences on metacommunity characteristics are insufficiently understood, and the underlying ecological mechanisms have not been elucidated. Here, we have compared the fecal microbiota of adults from two non-industrialized regions in Papua New Guinea (PNG) with that of United States (US) residents. Papua New Guineans harbor communities with greater bacterial diversity, lower inter-individual variation, vastly different abundance profiles, and bacterial lineages undetectable in US residents. A quantification of the ecological processes that govern community assembly identified bacterial dispersal as the dominant process that shapes the microbiome in PNG but not in the US. These findings suggest that the microbiome alterations detected in industrialized societies might arise from modern lifestyle factors limiting bacterial dispersal, which has implications for human health and the development of strategies aimed to redress the impact of westernization.

Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes.

Increasing evidence has emerged for non-random spatial distributions of microbes, but knowledge of the processes that cause variation in microbial assemblage among ecosystems is lacking. For instance, some studies showed that deterministic processes such as habitat specialization are important, while other studies hold that bacterial communities are assembled by stochastic forces. Here we examine the relative influence of deterministic and stochastic processes for bacterial communities from subsurface environments, stream biofilm, lake water, lake sediment and soil using pyrosequencing of the 16S ribosomal RNA gene. We show that there is a general pattern in phylogenetic signal in species ecological niches across recent evolutionary time for all studied habitats, enabling us to infer the influences of community assembly processes from patterns of phylogenetic turnover in community composition. The phylogenetic dissimilarities among-habitat types were significantly higher than within them, and the communities were clustered according to their original habitat types. For communities within-habitat types, the highest phylogenetic turnover rate through space was observed in subsurface environments, followed by stream biofilm on mountainsides, whereas the sediment assemblages across regional scales showed the lowest turnover rate. Quantifying phylogenetic turnover as the deviation from a null expectation suggested that measured environmental variables imposed strong selection on bacterial communities for nearly all sample groups. For three sample groups, spatial distance reflected unmeasured environmental variables that impose selection, as opposed to spatial isolation. Such characterization of spatial and environmental variables proved essential for proper interpretation of partial Mantel results based on observed beta diversity metrics. In summary, our results clearly indicate a dominant role of deterministic processes on bacterial assemblages and highlight that bacteria show strong habitat associations that have likely emerged through evolutionary adaptation.

Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession.

Significance Across ecology, and particularly within microbial ecology, there is limited understanding of the mechanisms governing the relative influences of stochastic and deterministic processes. Filling this knowledge gap is a major challenge that requires the development of novel conceptual paradigms, experiments, and ecological models. Here we (i) present a conceptual model that couples the stochastic/deterministic balance to primary and secondary ecological succession, thereby integrating previously isolated conceptual domains; (ii) evaluate this model over 105 years of ecosystem development, revealing a systematic shift in the type and strength of ecological selection; and (iii) couple empirical data with a new simulation model to elucidate underlying mechanisms and characterize their scale dependency. The insights and conceptual framework provided here represent a nexus for cross-system integration. Ecological succession and the balance between stochastic and deterministic processes are two major themes within microbial ecology, but these conceptual domains have mostly developed independent of each other. Here we provide a framework that integrates shifts in community assembly processes with microbial primary succession to better understand mechanisms governing the stochastic/deterministic balance. Synthesizing previous work, we devised a conceptual model that links ecosystem development to alternative hypotheses related to shifts in ecological assembly processes. Conceptual model hypotheses were tested by coupling spatiotemporal data on soil bacterial communities with environmental conditions in a salt marsh chronosequence spanning 105 years of succession. Analyses within successional stages showed community composition to be initially governed by stochasticity, but as succession proceeded, there was a progressive increase in deterministic selection correlated with increasing sodium concentration. Analyses of community turnover among successional stages—which provide a larger spatiotemporal scale relative to within stage analyses—revealed that changes in the concentration of soil organic matter were the main predictor of the type and relative influence of determinism. Taken together, these results suggest scale-dependency in the mechanisms underlying selection. To better understand mechanisms governing these patterns, we developed an ecological simulation model that revealed how changes in selective environments cause shifts in the stochastic/deterministic balance. Finally, we propose an extended—and experimentally testable—conceptual model integrating ecological assembly processes with primary and secondary succession. This framework provides a priori hypotheses for future experiments, thereby facilitating a systematic approach to understand assembly and succession in microbial communities across ecosystems.

Quantifying community assembly processes and identifying features that impose them

Spatial turnover in the composition of biological communities is governed by (ecological) Drift, Selection and Dispersal. Commonly applied statistical tools cannot quantitatively estimate these processes, nor identify abiotic features that impose these processes. For interrogation of subsurface microbial communities distributed across two geologically distinct formations of the unconfined aquifer underlying the Hanford Site in southeastern Washington State, we developed an analytical framework that advances ecological understanding in two primary ways. First, we quantitatively estimate influences of Drift, Selection and Dispersal. Second, ecological patterns are used to characterize measured and unmeasured abiotic variables that impose Selection or that result in low levels of Dispersal. We find that (i) Drift alone consistently governs ∼25% of spatial turnover in community composition; (ii) in deeper, finer-grained sediments, Selection is strong (governing ∼60% of turnover), being imposed by an unmeasured but spatially structured environmental variable; (iii) in shallower, coarser-grained sediments, Selection is weaker (governing ∼30% of turnover), being imposed by vertically and horizontally structured hydrological factors;(iv) low levels of Dispersal can govern nearly 30% of turnover and be caused primarily by spatial isolation resulting from limited exchange between finer and coarser-grain sediments; and (v) highly permeable sediments are associated with high levels of Dispersal that homogenize community composition and govern over 20% of turnover. We further show that our framework provides inferences that cannot be achieved using preexisting approaches, and suggest that their broad application will facilitate a unified understanding of microbial communities.

Testing the metabolic theory of ecology

The metabolic theory of ecology (MTE) predicts the effects of body size and temperature on metabolism through considerations of vascular distribution networks and biochemical kinetics. MTE has also been extended to characterise processes from cellular to global levels. MTE has generated both enthusiasm and controversy across a broad range of research areas. However, most efforts that claim to validate or invalidate MTE have focused on testing predictions. We argue that critical evaluation of MTE also requires strong tests of both its theoretical foundations and simplifying assumptions. To this end, we synthesise available information and find that MTEs original derivations require additional assumptions to obtain the full scope of attendant predictions. Moreover, although some of MTEs simplifying assumptions are well supported by data, others are inconsistent with empirical tests and even more remain untested. Further, although many predictions are empirically supported on average, work remains to explain the often large variability in data. We suggest that greater effort be focused on evaluating MTEs underlying theory and simplifying assumptions to help delineate the scope of MTE, generate new theory and shed light on fundamental aspects of biological form and function.

Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes

• It has long been believed that plant species from the tropics have higher levels of traits associated with resistance to herbivores than do species from higher latitudes. A meta-analysis recently showed that the published literature does not support this theory. However, the idea has never been tested using data gathered with consistent methods from a wide range of latitudes. • We quantified the relationship between latitude and a broad range of chemical and physical traits across 301 species from 75 sites world-wide. • Six putative resistance traits, including tannins, the concentration of lipids (an indicator of oils, waxes and resins), and leaf toughness were greater in high-latitude species. Six traits, including cyanide production and the presence of spines, were unrelated to latitude. Only ash content (an indicator of inorganic substances such as calcium oxalates and phytoliths) and the properties of species with delayed greening were higher in the tropics. • Our results do not support the hypothesis that tropical plants have higher levels of resistance traits than do plants from higher latitudes. If anything, plants have higher resistance toward the poles. The greater resistance traits of high-latitude species might be explained by the greater cost of losing a given amount of leaf tissue in low-productivity environments.

Temporal turnover in the composition of tropical tree communities: functional determinism and phylogenetic stochasticity

The degree to which turnover in biological communities is structured by deterministic or stochastic factors and the identities of influential deterministic factors are fundamental, yet unresolved, questions in ecology. Answers to these questions are particularly important for projecting the fate of forests with diverse disturbance histories worldwide. To uncover the processes governing turnover we use species-level molecular phylogenies and functional trait data sets for two long-term tropical forest plots with contrasting disturbance histories: one forest is older-growth, and one was recently disturbed. Having both phylogenetic and functional information further allows us to parse out the deterministic influences of different ecological filters. With the use of null models we find that compositional turnover was random with respect to phylogeny on average, but highly nonrandom with respect to measured functional traits. Furthermore, as predicted by a deterministic assembly process, the older-growth and disturbed forests were characterized by less than and greater than expected functional turnover, respectively. These results suggest that the abiotic environment, which changes due to succession in the disturbed forest, strongly governs the temporal dynamics of disturbed and undisturbed tropical forests. Predicting future changes in the composition of disturbed and undisturbed forests may therefore be tractable when using a functional-trait-based approach.