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bioRxiv2017

On the Stability Landscape of the Human Gut Microbiome: Implications for Microbiome-based Therapies

Understanding how gut microbial species determine their abundances is crucial in developing any microbiome-based therapy. Towards that end, we show that the compositions of our gut microbiota have characteristic and attractive steady states, and hence respond to perturbations in predictable ways. This is achieved by developing a new method to analyze the stability landscape of the human gut microbiome. In order to illustrate the efficacy of our method and its ecological interpretation in terms of asymptotic stability, this novel method is applied to various human cohorts, including large cross-sectional studies, long longitudinal studies with frequent sampling, and perturbation studies via fecal microbiota transplantation, antibiotic and probiotic treatments. These findings will facilitate future ecological modeling efforts in human microbiome research. Moreover, the method allows for the prediction of the compositional shift of the gut microbiome during the fecal microbiota transplantation process. This result holds promise for translational applications, such as, personalized donor selection when performing fecal microbiota transplantations.\n\nOne Sentence SummaryA new method for analyzing the stability landscape of the human gut microbiome and predicting its steady-state composition is developed.

ecology↗

bioRxiv2017

Conserving amphibians in the face of land development: integrating field experiments as a planning tool

Regulations designed to guide development practices inadequately reflect ecological understanding and fall short of preserving viable habitats. Environmental consultants use rapid assessments and monitoring on individual ponds to rank pond habitat quality, relying on coarse proxies, including vegetative indicators, soil characteristics, hydroperiod, and breeding evidence in obligate species. Planners incorporate these rankings to inform the layout of neighborhoods, roadways, infrastructure and housing. However, important drivers of amphibian survival and fecundity--including metapopulation dynamics, habitat connectivity, watershed health, terrestrial density dependence, and environmental gradients--are often poorly measured and regulated. Given that development proceeds regardless, what options exists improve land development practices?\n\nIntegrating experimentation into the planning process can inform land development and improve amphibian conservation. Working as part of the design team we employed an adaptive approach called designed experiment to inform development practices. We manipulated Ambystoma opacum larvae within enclosures to test the effects of inter-pond conditions (versus intra-pond density dependence) on the survival and fecundity of conspecifics, Rana sylvatica and Ambystoma maculatum. While the A. maculatum populations were decimated with only 1.5 % survival. For A. opacum and R. sylvatica results indicate habitat variation between ponds accounted for 63.7% and 50.3% of the variance in survival rates of larvae, respectively, and are not predicted by the presence and abundance of egg masses, while density effects accounted for 3.5% and 2.8% of the variation in survival. The results suggest that ponds ranked as high value based on egg mass counts may actually function as habitat sinks. This study illustrates the potential value of assessment approaches that emphasize habitat quality across pond clusters to guide mitigation, conservation, regulations, and to establish sites and funding for ecological research.

ecology↗

bioRxiv2017

Effects of anthropogenic wildfire activity in low elevation Pacific island vegetation communities in French Polynesia

Anthropogenic (or human-caused) wildfire is an increasingly important driver of ecological change on Pacific islands including southeastern Polynesia, but fire ecology studies are almost completely absent for this region. Where observations do exist, they mostly represent descriptions of fire effects on plant communities before the introduction of invasive species in the modern era. Understanding the effects of wildfire in southeastern Polynesian island vegetation communities can elucidate which species may become problematic invasives with continued wildfire activity. We investigate the effects of wildfire on vegetation in three low-elevation sites (45-379 m) on the island of Moorea in the Society Islands, French Polynesia, which are already heavily impacted by past human land use and invasive exotic plants, but retain some native flora. In six study areas (3 burned and 3 unburned comparisons), we placed 30 transects across sites and collected species and abundance information at 390 points. We analyzed each local community of plants in three categories: natives, those introduced by Polynesians before European contact (1767 C.E.), and those introduced since European contact. Burned areas had the same or lower mean species richness than paired comparison sites. Although wildfire did not affect the proportions of native and introduced species, it may increase the abundance of introduced species on some sites. Non-metric multidimensional scaling indicates that (not recently modified) comparison plant communities are more distinct from one another than are those on burned sites. We discuss conservation concerns for particular native plants absent from burned sites, as well as invasive species (including Lantana camara and Paraserianthes falcataria) that may be promoted by fire in the Pacific.

ecology↗

bioRxiv2017

An agent-based model of the Foraging Ascomycete Hypothesis

Most trees host hundreds of species of fungi asymptomatically in their internal tissues, known collectively as fungal endophytes. The Foraging Ascomycete (FA) hypothesis proposes that some fungal endophytes inhabit the internal leaf tissue of forest trees in order to enhance dispersal to substrates on the forest floor, by using leaves as vectors and as refugia during periods of environmental stress. This dispersal strategy has been termed viaphytism. Following the FA hypothesis, many fungi may therefore be in continuous and cyclical flux between life stages as endophytes in the forest canopy and as wood-decomposing fungi on the forest floor. This cycle may represent a very common and previously-ignored process in the ecology of forests, with implications for forest health. The ecological consequences of the FA hypothesis are complex, so we constructed an agent-based model of the FA hypothesis. Our model is intended to serve as both an explicit conceptual explanation of the FA hypothesis, and as an exploration of the conditions in which a strategy of endophytism accompanied by leaf dispersal may be advantageous for fungi. In a scenario of a viaphytic fungal species on a model forest landscape, without fungal competitors, viaphytism is predicted to be a plausible alternative to dispersal to substrates by spores alone, allowing the fungus to persist reliably on the landscape. In a scenario that allows competition from aggressively dispersed non-viaphytic fungi, the model predicts some competitive benefits to fungal dispersal via leaves. However, these benefits are conditional, requiring sufficient retention through time of endophyte infections by host trees, and sufficient host trees on the landscape. In the model, loss of these fungal populations can result from increased local disturbances of forest canopy, and deforestation.

ecology↗

bioRxiv2017

Do priority effects outweigh environmental filtering in a guild of dominant freshwater macroinvertebrates?

Abiotic conditions have long been considered essential in structuring freshwater macroinvertebrate communities. Ecological drift, dispersal, and biotic interactions also structure communities, and although these mechanisms are more difficult to detect, they may be of equal importance in natural communities. Here, we conducted repeated surveys of locally-dominant amphipod species across ten naturally replicated stream catchments. We then used a hierarchical joint species distribution model to assess the influence of different drivers on species co-occurrences. The species had unique environmental requirements, but a distinct spatial structure in their distributions was unrelated to habitat. Species co-occurred much less frequently than predicted by their niches, which was surprising because laboratory and field evidence suggests they are capable of coexisting in equal densities. We suggest that niche preemption may limit their distribution and that a blocking effect determines which species colonizes and dominates a given stream catchment, thus resolving a long-standing conundrum in freshwater ecology.

ecology↗

bioRxiv2017

Study mortality with hazard rates, not probabilities

O_LIMortality is a key process in ecology and evolution, and much effort is spent on statistical and theoretical modelling of this process. Mortality hazard rates describe individuals instantaneous ability to survive at different times, whereas survival probabilities are defined for time-intervals of a given length. In this commentary, we argue that it is often more meaningful to model and interpret interval-specific time-averaged mortality hazard rates than survival probabilities, also when using discrete-time models.\nC_LIO_LIWe discuss three topics where the concept of hazard rates is essential for sound biological inference, but nevertheless often not used: (i) modelling of covariate effects on survival probabilities or mortality hazard rates, (ii) modelling of multiple sources of mortality and competing risks, and (iii) elasticity analyses of population growth rate to demographic parameters. To facilitate estimation of cause-specific mortality hazard rates, we provide amendments to R package marked.\nC_LIO_LIBy focusing on modelling mortality hazard rates, one avoids several inherent problems of comparing survival or mortality probabilities. In particular, interpretations about relative differences between mortality hazard rates (measurements on a ratio scale), or effects of relative changes in mortality hazard rates on population growth (elasticities), are more meaningful than similar interpretations involving survival (or mortality) probabilities or odds (measurements on an absolute scale).\nC_LIO_LIThe concept of hazard rates is essential for understanding ecological and evolutionary processes and we give an intuitive explanation for this, using several examples. We provide some practical guidelines and suggestions for further methods developments.\nC_LI

ecology↗

bioRxiv2017

Robustness of early warning signals for catastrophic and non-catastrophic transitions

Early warning signals (EWS) are statistical indicators that a rapid regime shift may be forthcoming. Their development has given ecologists hope of predicting rapid regime shifts before they occur. Accurate predictions, however, rely on the signals being appropriate to the system in question. Most of the EWS commonly applied in ecology have been studied in the context of one specific type of regime shift (the type brought on by a saddle-node bifurcation, at which one stable equilibrium point collides with an unstable equilibrium and disappears) under one particular perturbation scheme (temporally uncorrelated noise that perturbs the net population growth rate in a density independent way). Whether and when these EWS can be applied to other ecological situations remains relatively unknown, and certainly underappreciated. We study a range of models with different types of dynamical transitions (including rapid regime shifts) and several perturbation schemes (density-dependent uncorrelated or temporally-correlated noise) and test the ability of EWS to warn of an approaching transition. We also test the sensitivity of our results to the amount of available pre-transition data and various decisions that must be made in the analysis (i.e. the rolling window size and smoothing bandwidth used to compute the EWS). We find that EWS generally work well to signal an impending saddle-node bifurcation, regardless of the autocorrelation or intensity of the noise. However, EWS do not reliably appear as expected for other types of transition. EWS were often very sensitive to the length of the pre-transition time series analyzed, and usually less sensitive to other decisions. We conclude that the EWS perform well for saddle-node bifurcation in a range of noise environments, but different methods should be used to predict other types of regime shifts. As a consequence, knowledge of the mechanism behind a possible regime shift is needed before EWS can be used to predict it.

ecology↗

bioRxiv2017

GMSE: an R package for generalised management strategy evaluation

O_LIManagement strategy evaluation (MSE) is a powerful tool for simulating all key aspects of natural resource management under conditions of uncertainty.\nC_LIO_LIWe present the R package GMSE, which applies genetic algorithms to provide a generalised tool for simulating adaptive decision-making management scenarios between stakeholders with competing objectives under complex social-ecological interactions and uncertainty.\nC_LIO_LIGMSE models can be agent-based and spatially explicit, incorporating a high degree of realism through mechanistic modelling of links and feedbacks among stakeholders and with the ecosystem; additionally, user-defined sub-models can also be incorporated as functions into the broader GMSE framework.\nC_LIO_LIWe show how GMSE simulates a social-ecological system using the example of an adaptively managed waterfowl population on an agricultural landscape; simulated waterfowl exploit agricultural land, causing conflict between conservation interests and the interest of food producers maximising their crop yield.\nC_LIO_LIThe R package GMSE is open source under GNU Public License; source code and documents are freely available on GitHub.\nC_LI

ecology↗

bioRxiv2017

A temperature dependent trophic cascade modifies temperature dependence of ecosystem function

Ecological communities and their ecosystem functions are sensitive to temperature, and aquatic habitats worldwide continue to experience unprecedented warming. Understanding ecological effects of warming requires linking empirical evidence to theories that allow projection to unobserved conditions. Metabolic scaling theory and its tests suggest that warming accelerates ecosystem functions (e.g., oxygen flux), yet this prediction apparently contradicts community-level studies suggesting warming is a stressor that can reduce ecosystem function. We sought to reconcile these predictions with an experimental test of the hypothesis that cascading trophic interactions modify the temperature-dependence of community structure and ecosystem fluxes. In a series of independent freshwater ecosystems exposed to a thermal gradient, we found that warmer temperatures strengthened the trophic cascade increased and indirectly changed community structure by altering grazer species composition and phytoplankton biomass. Temperature-driven community shifts only modestly affected the temperature dependence of net ecosystem oxygen fluxes. Over the 10 {degrees}C thermal gradient, NPP and ER increased [~]2.7-fold among ecosystems, while standing phytoplankton biomass declined by 85-95%. The exponential increase in oxygen flux over the thermal gradient, as well as monotonic declines in phytoplankton standing stock, suggested no threshold effects of warming across systems. We also observed temperature variation over time, within ecosystems. For phytoplankton biomass, temporal variation had the opposite effect to spatial variation, suggesting that within-community temporal change in community structure was not predicted by space-for-time substitution. We conclude that food chain length can modify effects of temperature on ecosystem fluxes, but that temperature can still have continuous and positive effects on ecosystem fluxes, consistent with patterns based on large-scale, macroecological comparisons. Changes in community structure, including temperature dependent trophic cascades, may be compatible with prevailing and predictable effects of temperature on ecosystem functions related to fundamental effects of temperature on metabolism.\n\nStatement of authorshipJG & MIO designed the study, MIO & US provided materials, JG & SJC performed research and collected data, JG performed zooplankton analysis, SJC performed phytoplankton analysis, JG & MIO performed modeling work, analyzed data output, and wrote the first draft, and all authors contributed substantially to reviews

ecology↗

bioRxiv2018

Larger legume plants host a greater diversity of symbiotic nitrogen-fixing bacteria

A major goal in microbial ecology is to understand the factors that structure bacterial communities across space and time. For microbes that have symbiotic relationships with plants, an important factor that may influence their communities is host size or age, yet this has received little attention.\n\nUsing tree diameter size as a proxy for age, we quantified the diversity of rhizobia that associate with an endemic legume, Acacia acuminata, of variable size across a climate gradient in southwest Australia. We examined the 16S rRNA diversity (V1-V3 hypervariable region) of rhizobia at the taxonomic level and at higher sequence level diversity within taxonomic groups.\n\nWe identified 3 major taxonomic clades that associated with Acacia acuminata: Bradyrhizobiaceae, Rhizobiaceae, and Burkholderiaceae. Within these groups, we found extensive genetic variability, especially within Bradyrhizobiaceae. Using binomial multivariate statistical models that controlled for other factors that affect plant size and rhizobia community structure (climate and local soil characteristics), we determined that soil sampled at the base of larger Acacia trees was much more likely to contain a greater number of taxonomic clades and cryptic genetic variants within the Rhizobiaceae clade.\n\nDespite strong influences of climate and highly heterogeneous soil conditions on rhizobial diversity, our results show that host tree size is a prominent factor in structuring nitrogen-fixing symbionts diversity across a large landscape. The identification of a positive relationship between plant host size and microbial diversity raise interesting questions about the role of plant host size in driving ecological processes that govern microbial community assembly. Specifically, our results suggest that hosts may modify the habitat of their surrounding soil to enhance growth (niche construction hypothesis) or that symbiotic microbes have large differences in dispersal capability. Our results also suggest that host plants may be analogous to islands, where larger legume hosts may accumulate diversity over time, through migration opportunities or in situ diversification. From a practical perspective, including plant size as an additional variable may assist sampling and analyses designs of future soil microbial studies.

ecology↗

bioRxiv2018

A plant biodiversity effect resolved to a single locus

Despite extensive evidence that biodiversity promotes plant community productivity, progress towards understanding the mechanistic basis of this effect remains slow, impeding the development of predictive ecological theory and agricultural applications. Here, we analysed non-additive interactions between genetically divergent Arabidopsis accessions in experimental plant communities. By combining methods from ecology and genetics, we identified a major effect locus at which allelic differences between individuals increases above-ground productivity of communities. In experiments with near-isogenic lines, we show that this diversity effect acts independently of other genomic regions and can be resolved to a single region representing less than 0.3% of the genome. Using plant-soil-feedback experiments, we also demonstrate that allelic diversity causes genotype-specific soil legacy responses in a consecutive growing period, even after the original community has disappeared. Our work thus suggests that positive diversity effects can be linked to single Mendelian factors, and that a range of complex community properties can have a simple cause. This may pave the way to a better understanding of diversity effects, and to novel breeding strategies, focussing on phenotypic properties that manifest themselves beyond isolated individuals, i.e. at a higher level of biological organisation.

ecology↗

bioRxiv2018

Ubiquitous abundance distribution of non-dominant plankton across the world’s ocean

Species Abundance Distributions (SADs) bear the imprint of ecological processes that shape biological communities, and are therefore used to discriminate among different scenarios of community assembly. Even though empirical distributions appear to follow a handful of qualitative laws, it is still unclear if and how quantitative variation in SADs reflects peculiar features of the communities and their environmental context. Here, we use the extensive dataset generated by the Tara Oceans expedition for marine microbial eukaryotes (protists) and an adaptive algorithm to explore how SADs vary across plankton communities in the global ocean. We show that the decay in abundance of non-dominant OTUs, comprising over 99% of local richness, is commonly governed by a power-law. The power-law exponent varies by less than 10% across locations and shows no biogeographical signature, but is weakly modulated by cell size. Our findings suggest that large-scale ubiquitous ecological processes govern the assembly of non-dominant plankton throughout the global ocean.

ecology↗

bioRxiv2018

One man’s trash is another man’s treasure - the effect of bacteria on phytoplankton-zooplankton interactions in chemostat systems

Chemostat experiments are employed to study predator-prey and other trophic interactions, frequently using phytoplankton-zooplankton systems. These experiments often use population dynamics as fingerprints of ecological and evolutionary processes, assuming that the contributions of all major actors to these dynamics are known. However, bacteria are often neglected although they are frequently present. We argue that even without external carbon sources bacteria may affect the experimental outcomes depending on experimental conditions and the physiological traits of bacteria, phytoplankton and zooplankton. Using a static carbon flux model and a dynamic simulation model we predict the minimum and maximum impact of bacteria on phytoplankton-zooplankton population dynamics. Under bacteria-suppressing conditions, we find that the effect of bacteria is indeed negligible and their omission justified. Under bacteria-favouring conditions, however, bacteria may strongly affect average biomasses. Furthermore, the population dynamics may become highly complex resulting in wrong conclusions if bacteria are not considered. Our model results provide suggestions to reduce the bacterial impact experimentally. Next to optimizing experimental conditions (e.g. the dilution rate) the appropriate choice of the zooplankton predator is decisive. Counterintuitively, bacteria have a larger impact if they are not ingested by the predator as high bacterial biomasses and complex population dynamics arise via competition for nutrients with the phytoplankton. Only if the predator is at least partly bacterivorous the impact of bacteria is minimized. Our results help to improve both the design of chemostat experiments and their interpretation and thus advance the study of ecological and evolutionary processes in aquatic food webs.

ecology↗

bioRxiv2018

Both functional trait divergence and trait plasticity confer polyploid advantage in changing environments

Polyploidy, or whole genome duplication, exists in all eukaryotes and is thought to drive ecological and evolutionary success especially in plants. The mechanisms of polyploid success in ecologically relevant contexts, however, remain largely unknown. Here we conducted an extensive test of functional trait divergence and trait plasticity in conferring polyploid fitness advantage in changing environments by growing clonal replicates of a worldwide genotype collection of six polyploid and five diploid wild strawberry (Fragaria) species in three climatically different common gardens. Among leaf functional traits, we detected divergence in means but not plasticities between polyploids and diploids, suggesting that increased genomic redundancy does not necessarily translate into broader phenotypic amplitude in polyploids. Across the heterogeneous garden environments, however, polyploids exhibited fitness advantage, which was conferred by both trait means and adaptive trait plasticities, supporting a jack-and-master hypothesis for polyploids. Our findings provide unparalleled insight into the prevalence and persistence of polyploidization.

ecology↗

bioRxiv2018

Understanding biodiversity at the pondscape using environmental DNA: a focus on great crested newts

Environmental DNA (eDNA) metabarcoding is revolutionising biodiversity monitoring, but has unrealised potential for ecological hypothesis generation and testing. Here, we validate this potential in a large-scale analysis of vertebrate community data generated by eDNA metabarcoding of 532 UK ponds. We test biotic associations between the threatened great crested newt (Triturus cristatus) and other vertebrates as well as abiotic factors influencing T. cristatus detection at the pondscape. Furthermore, we test the status of T. cristatus as an umbrella species for pond conservation by assessing whether vertebrate species richness is greater in ponds with T. cristatus and higher T. cristatus Habitat Suitability Index (HSI) scores. T. cristatus detection was positively correlated with amphibian and waterfowl species richness. Specifically, T. cristatus was positively associated with smooth newt (Lissotriton vulgaris), common coot (Fulica atra), and common moorhen (Gallinula chloropus), but negatively associated with common toad (Bufo bufo). T. cristatus detection did not significantly decrease as fish species richness increased, but negative associations with common carp (Cyprinus carpio), three-spined stickleback (Gasterosteus aculeatus) and ninespine stickleback (Pungitius pungitius) were identified. T. cristatus detection was negatively correlated with mammal species richness, and T. cristatus was negatively associated with grey squirrel (Sciurus carolinensis). T. cristatus detection was negatively correlated with larger pond area, presence of inflow, and higher percentage of shading, but positively correlated with HSI score, supporting its application to T. cristatus survey. Vertebrate species richness was significantly higher in T. cristatus ponds and broadly increased as T. cristatus HSI scores increased. We reaffirm reported associations (e.g. T. cristatus preference for smaller ponds) but also provide novel insights, including a negative effect of pond inflow on T. cristatus. Our findings demonstrate the prospects of eDNA metabarcoding for ecological hypothesis generation and testing at landscape scale, and dramatic enhancement of freshwater conservation, management, monitoring and research.

ecology↗

bioRxiv2018

A microcalorimetric approach for investigating stoichiometric constraints on the standard metabolic rate of a small invertebrate

1: Understanding the determinant of metabolism is a core ecological topic since it permits to link individuals energetic requirements to the ecology of communities and ecosystems. Yet, besides temperature, the effects of environmental factors on metabolism remain poorly understood. For example, dietary stoichiometric constraints have been hypothesized to increase maintenance metabolism of small invertebrates, yet experimental support remains scarce.\n\n2: Here, we used microcalorimetric heat flow measurements to determine the standard metabolic rate (SMR) of Daphnia magna throughout its ontogeny when fed stoichiometrically balanced (C/P ratio:166) or imbalanced (C/P ratio:1439) diets.\n\n3: When fed a stoichiometrically imbalanced diet, daphnids were able to maintain the stoichiometric homeostasis within narrow boundaries. However, they consistently increased their SMR while decreasing their somatic growth rate. Our measurements unequivocally demonstrate that homeostatic regulation implies higher metabolic costs and thereby reduces the portion of energy that can be allocated to growth.\n\n4: Our study demonstrates that microcalorimetry is a powerful and precise tool for measuring the metabolic rate of small-sized organisms and opens promising perspectives for understanding how environmental factors, such as nutritional constraints, affect organismal metabolism.

ecology↗

bioRxiv2018

Cohesiveness in microbial community coalescence

Microbial invasions exhibit many unique properties; notably, entire microbial communities often invade one another, a phenomenon known as community coalescence. In spite of the potential importance of this process for the dynamics and stability of microbiome assembly, our understanding of it is still very limited. Recent theoretical and empirical work has proposed that large microbial communities may exhibit an emergent cohesiveness, as a result of collective consumer-resource interactions and metabolic feedbacks between microbial growth and the environment. A fundamental prediction of this proposal is the presence of ecological co-selection during community coalescence, where the invasion success of a given taxon is determined by its community members. To establish the generality of this prediction in experimental microbiomes, we have performed over one hundred invasion and coalescence experiments with environmental communities of different origins that had spontaneously and stably assembled in two different synthetic aerobic environments. We show that the dominant species of the coalesced communities can both recruit their community members (top-down co-selection) and be recruited by them (bottom-up co-selection) into the coalesced communities. Our results provide direct evidence that collective invasions generically produce ecological co-selection of interacting species, emphasizing the importance of community-level interactions during microbial community assembly.

ecology↗

bioRxiv2018

On the variability of Species Abundance Distributions with trophic guild and community structure

Species Abundance Distributions (SADs) are one of the most studied properties of ecological communities, and their variability has been studied mostly in the context of horizontal communities, i.e. sets of species from a particular trophic guild. However, virtually all ecological communities encompass several trophic guilds, and the trophic interactions between them are key for explaining the persistence and abundance of individual species. Here I ask whether trophic interactions are also important in shaping Species Abundance Distributions of the different guilds of a community. I analyze the variation in SAD shape across trophic guilds in model and empirical communities. For that, I use a theoretical model that allows tracking the variations in abundances across trophic levels. The relationship between SAD shape and (1) trophic level, and (2) degree of predator specialization is analyzed using mixed-effect models. I combine this approach with an analysis of 4676 empirical datasets spanning terrestrial, marine and freshwater habitats, for which the variation in SAD shape is related to (1) trophic guild, and (2) habitat type. The evenness of model SADs is positively correlated to the trophic level of the guild considered, and also to the number of prey species per predator. These findings are confirmed by the empirical data: there is a significant relationship between SAD evenness and trophic guild, whereby primary producers display the most uneven SADs and pure carnivores the most even ones. Furthermore, regardless of trophic guild, SADs from marine habitats are the most even ones, with terrestrial SADs being the most uneven.

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