Divergent ecological responses to typhoon disturbance revealed via landscape-scale acoustic monitoring.

Climate change is increasing the frequency, intensity, and duration of extreme weather events across the globe. Understanding the capacity for ecological communities to withstand and recover from such events is critical. Typhoons are extreme weather events that are expected to broadly homogenize ecological dynamics through structural damage to vegetation and longer-term effects of salinization. Given their unpredictable nature, monitoring ecological responses to typhoons is challenging, particularly for mobile animals such as birds. Here, we report spatially variable ecological responses to typhoons across terrestrial landscapes. Using a high temporal resolution passive acoustic monitoring network across 24 sites on the subtropical island of Okinawa, Japan, we found that typhoons elicit divergent ecological responses among Okinawa's diverse terrestrial habitats, as indicated by increased spatial variability of biological sound production (biophony) and individual species detections. This suggests that soniferous communities are capable of a diversity of different responses to typhoons. That is, spatial insurance effects among local ecological communities provide resilience to typhoons at the landscape scale. Even though site-level typhoon impacts on soundscapes and bird detections were not particularly strong, monitoring at scale with high temporal resolution across a broad spatial extent nevertheless enabled detection of spatial heterogeneity in typhoon responses. Further, species-level responses mirrored those of acoustic indices, underscoring the utility of such indices for revealing insight into fundamental questions concerning disturbance and stability. Our findings demonstrate the significant potential of landscape-scale acoustic sensor networks to capture the understudied ecological impacts of unpredictable extreme weather events.

Coexistence barriers confine the poleward range of a globally distributed plant.

In the study of factors shaping species' poleward range boundaries, climatic constraints are often assigned greater importance than biotic interactions such as competition. However, theory suggests competition can truncate a species' fundamental niche in harsh environments. We test this by challenging a mechanistic niche model - containing explicit competition terms - to predict the poleward range boundaries of two globally distributed, ecologically similar aquatic plant species. Mechanistic competition models accurately predicted the northern range limits of our study species, outperforming competition-free mechanistic models and matching the predictive ability of statistical niche models fit to occurrence records. Using the framework of modern coexistence theory, we found that relative nonlinearity in competitors' responses to temperature fluctuations maintains their coexistence boundary, highlighting the importance of this fluctuation-dependent mechanism. Our results support a more nuanced, interactive role of climate and competition in determining range boundaries, and illustrate a practical, process-based approach to understanding the determinants of range limits.

Invasive plants exert disproportionately negative allelopathic effects on the growth and physiology of the earthworm Eisenia fetida.

Exotic invasive plants possess the capacity to disrupt and extirpate populations of native species. Native plants' increased sensitivity to invaders' allelochemicals is a mechanism by which this can occur. However, it is not clear whether and how the allelopathic effects of invasive plants affect members of the soil faunal community - particularly the important functional guild of earthworms. We used the model earthworm Eisenia fetida to investigate the responses to extracts from the widely invasive Asterids (Ageratina adenophora, Bidens pilosa, Erigeron annuus) and closely-related native species in a greenhouse experiment. We observed declines in body mass and respiration, and increases in oxidative and DNA damage biomarkers in the native earthworm E. fetida when grown under root and leaf extracts from these invasive plants. These effects were concentration-dependent, and worm growth and physiology was most negatively affected under the highest concentrations of leaf extracts. Most importantly, extracts from invasive plants caused significantly more negative effects on E. fetida than did extracts from native plant species, indicating allelopathy from invasive plants may inhibit earthworm physiological functioning. These results expand the domain of the novel weapons hypothesis to the earthworm guild and demonstrate the utility of E. fetida as a bioindicator for plant allelochemicals.

How sample heterogeneity can obscure the signal of microbial interactions.

Microbial community data are commonly subjected to computational tools such as correlation networks, null models, and dynamic models, with the goal of identifying the ecological processes structuring microbial communities. A major assumption of these methods is that the signs and magnitudes of species interactions and vital rates can be reliably parsed from observational data on species' (relative) abundances. However, we contend that this assumption is violated when sample units contain any underlying spatial structure. Here, we show how three phenomena-Simpson's paradox, context-dependence, and nonlinear averaging-can lead to erroneous conclusions about population parameters and species interactions when samples contain heterogeneous mixtures of populations or communities. At the root of this issue is the fundamental mismatch between the spatial scales of species interactions (micrometers) and those of typical microbial community samples (millimeters to centimetres). These issues can be overcome by measuring and accounting for spatial heterogeneity at very small scales, which will lead to more reliable inference of the ecological mechanisms structuring natural microbial communities.

Negative frequency-dependent growth underlies the stable coexistence of two cosmopolitan aquatic plants.

Identifying and quantifying the mechanisms influencing species coexistence remains a major challenge for the study of community ecology. These mechanisms, which stem from species' differential responses to competition and their environments, promote coexistence if they give each species a growth advantage when rare. Yet despite the widespread assumption that co-occurring species stably coexist, there have been few empirical demonstrations in support of this claim. Likewise, coexistence is often assumed to result from interspecific differences in life-history traits, but the relative contributions of these trait differences to coexistence are rarely quantified, particularly across environmental gradients. Using two widely co-occurring and ecologically similar species of freshwater duckweed plants (Spirodela polyrhiza and Lemna minor), we tested hypotheses that interspecific differences in facultative dormancy behaviors, thermal reaction norms, and density-dependent growth promote coexistence between these species, and that their relative influences on coexistence change as average temperatures and fluctuations around them vary. In competition experiments, we found strong evidence for negative frequency-dependent growth across a range of both static and fluctuating temperatures, suggesting a critical role of fluctuation-independent stabilization in coexistence. This negative frequency dependence could be explained by our observation that for both species, intraspecific competition was over 1.5 times stronger than interspecific competition, granting each species a low-density growth advantage. Using an empirically parameterized competition model, we found that while coexistence was facilitated by environmental fluctuations, fluctuation-independent stabilization via negative frequency dependence was crucial for coexistence. Conversely, the temporal storage effect, an important fluctuation-dependent mechanism, was relatively weak in comparison. Contrary to expectations, differences in the species' thermal reaction norms and dormancy behaviors did not significantly promote coexistence in fluctuating environments. Our results highlight how coexistence in two ubiquitous and ostensibly similar aquatic plants is not necessarily a product of their most obvious interspecific differences, and instead results from subtle niche differences causing negative frequency-dependent growth, which acts consistently on both species across environmental gradients.

Linking the development and functioning of a carnivorous pitcher plant's microbial digestive community.

Ecosystem development theory predicts that successional turnover in community composition can influence ecosystem functioning. However, tests of this theory in natural systems are made difficult by a lack of replicable and tractable model systems. Using the microbial digestive associates of a carnivorous pitcher plant, I tested hypotheses linking host age-driven microbial community development to host functioning. Monitoring the yearlong development of independent microbial digestive communities in two pitcher plant populations revealed a number of trends in community succession matching theoretical predictions. These included mid-successional peaks in bacterial diversity and metabolic substrate use, predictable and parallel successional trajectories among microbial communities, and convergence giving way to divergence in community composition and carbon substrate use. Bacterial composition, biomass, and diversity positively influenced the rate of prey decomposition, which was in turn positively associated with a host leaf's nitrogen uptake efficiency. Overall digestive performance was greatest during late summer. These results highlight links between community succession and ecosystem functioning and extend succession theory to host-associated microbial communities.

Bacteria facilitate prey retention by the pitcher plant Darlingtonia californica.

Bacteria are hypothesized to provide a variety of beneficial functions to plants. Many carnivorous pitcher plants, for example, rely on bacteria for digestion of captured prey. This bacterial community may also be responsible for the low surface tensions commonly observed in pitcher plant digestive fluids, which might facilitate prey capture. I tested this hypothesis by comparing the physical properties of natural pitcher fluid from the pitcher plant Darlingtonia californica and cultured 'artificial' pitcher fluids and tested these fluids' prey retention capabilities. I found that cultures of pitcher leaves' bacterial communities had similar physical properties to raw pitcher fluids. These properties facilitated the retention of insects by both fluids and hint at a previously undescribed class of plant-microbe interaction.

Time-variant species pools shape competitive dynamics and biodiversity-ecosystem function relationships.

Biodiversity-ecosystem function (BEF) experiments routinely employ common garden designs, drawing samples from a local biota. The communities from which taxa are sampled may not, however, be at equilibrium. To test for temporal changes in BEF relationships, I assembled the pools of aquatic bacterial strains isolated at different time points from leaves on the pitcher plant Darlingtonia californica in order to evaluate the strength, direction and drivers of the BEF relationship across a natural host-associated successional gradient. I constructed experimental communities using bacterial isolates from each time point and measured their respiration rates and competitive interactions. Communities assembled from mid-successional species pools showed the strongest positive relationships between community richness and respiration rates, driven primarily by linear additivity among isolates. Diffuse competition was common among all communities but greatest within mid-successional isolates. These results demonstrate the dependence of the BEF relationship on the temporal dynamics of the local species pool, implying that ecosystems may respond differently to the addition or removal of taxa at different points in time during succession.

The cobra's tongue: Rethinking the function of the "fishtail appendage" on the pitcher plant Darlingtonia californica.

PREMISE OF STUDY: Carnivorous pitcher plants employ a variety of putative adaptations for prey attraction and capture. One example is the peculiar forked "fishtail appendage", a foliar structure widely presumed to function as a prey attractant on adult leaves of Darlingtonia californica (Sarraceniaceae). This study tests the prediction that the presence of the appendage facilitates prey capture and can be considered an example of an adaptation to the carnivorous syndrome. METHODS: In a field experiment following a cohort of Darlingtonia leaves over their growing season, before the pitcher traps opened, the fishtail appendages from half of the leaves were removed. Additionally, all appendages were removed from every plant at two small, isolated populations. After 54 and 104 d, prey items were collected to determine whether differences in prey composition and biomass existed between experimental and unmanipulated control leaves. KEY RESULTS: Removal of the fishtail appendage did not reduce pitcher leaves' prey biomass nor alter their prey composition at either the level of individual leaves or entire populations. Fishtail appendages on plants growing in shaded habitats contained significantly greater chlorophyll concentrations than those on plants growing in full sun. CONCLUSIONS: These results call into question the longstanding assumption that the fishtail appendage on Darlingtonia is an adaptation critical for the attraction and capture of prey. I suggest alternative evolutionary explanations for the role of the fishtail structure and repropose a hypothesis on the mutualistic nature of pitcher plant-arthropod trophic interactions.

Experimental evidence for a time-integrated effect of productivity on diversity.

The time-area-productivity hypothesis is a proposed explanation for global biodiversity gradients. It predicts that a bioregion's modern diversity is the product of its area and productivity, integrated over evolutionary time. I performed the first experimental test of the time-area-productivity hypothesis using a model system for adaptive radiation - the bacterium Pseudomonas fluorescens SBW25. I initiated hundreds of independent radiations under culture conditions spanning a variety of productivities, spatial extents and temporal extents. Time-integrated productivity was the single best predictor of extant phenotypic diversity and richness. In contrast, 'snapshots' of modern environmental variables at the time of sampling were less useful predictors of diversity patterns. These results were best explained by marked variation in population growth parameters under different productivity treatments and the long periods over which standing diversity could persist in unproductive habitats. These findings provide the first experimental support for time-integrated productivity as a putative driver of regional biodiversity patterns.

Utilizing novel diversity estimators to quantify multiple dimensions of microbial biodiversity across domains.

BACKGROUND: Microbial ecologists often employ methods from classical community ecology to analyze microbial community diversity. However, these methods have limitations because microbial communities differ from macro-organismal communities in key ways. This study sought to quantify microbial diversity using methods that are better suited for data spanning multiple domains of life and dimensions of diversity. Diversity profiles are one novel, promising way to analyze microbial datasets. Diversity profiles encompass many other indices, provide effective numbers of diversity (mathematical generalizations of previous indices that better convey the magnitude of differences in diversity), and can incorporate taxa similarity information. To explore whether these profiles change interpretations of microbial datasets, diversity profiles were calculated for four microbial datasets from different environments spanning all domains of life as well as viruses. Both similarity-based profiles that incorporated phylogenetic relatedness and naïve (not similarity-based) profiles were calculated. Simulated datasets were used to examine the robustness of diversity profiles to varying phylogenetic topology and community composition. RESULTS: Diversity profiles provided insights into microbial datasets that were not detectable with classical univariate diversity metrics. For all datasets analyzed, there were key distinctions between calculations that incorporated phylogenetic diversity as a measure of taxa similarity and naïve calculations. The profiles also provided information about the effects of rare species on diversity calculations. Additionally, diversity profiles were used to examine thousands of simulated microbial communities, showing that similarity-based and naïve diversity profiles only agreed approximately 50% of the time in their classification of which sample was most diverse. This is a strong argument for incorporating similarity information and calculating diversity with a range of emphases on rare and abundant species when quantifying microbial community diversity. CONCLUSIONS: For many datasets, diversity profiles provided a different view of microbial community diversity compared to analyses that did not take into account taxa similarity information, effective diversity, or multiple diversity metrics. These findings are a valuable contribution to data analysis methodology in microbial ecology.

Millimeter-scale patterns of phylogenetic and trait diversity in a salt marsh microbial mat.

Intertidal microbial mats are comprised of distinctly colored millimeter-thick layers whose communities organize in response to environmental gradients such as light availability, oxygen/sulfur concentrations, and redox potential. Here, slight changes in depth correspond to sharp niche boundaries. We explore the patterns of biodiversity along this depth gradient as it relates to functional groups of bacteria, as well as trait-encoding genes. We used molecular techniques to determine how the mat's layers differed from one another with respect to taxonomic, phylogenetic, and trait diversity, and used these metrics to assess potential drivers of community assembly. We used a range of null models to compute the degree of phylogenetic and functional dispersion for each layer. The SSU-rRNA reads were dominated by Cyanobacteria and Chromatiales, but contained a high taxonomic diversity. The composition of each mat core was significantly different for developmental stage, year, and layer. Phylogenetic richness and evenness positively covaried with depth, and trait richness tended to decrease with depth. We found evidence for significant phylogenetic clustering for all bacteria below the surface layer, supporting the role of habitat filtering in the assembly of mat layers. However, this signal disappeared when the phylogenetic dispersion of particular functional groups, such as oxygenic phototrophs, was measured. Overall, trait diversity measured by orthologous genes was also lower than would be expected by chance, except for genes related to photosynthesis in the topmost layer. Additionally, we show how the choice of taxa pools, null models, spatial scale, and phylogenies can impact our ability to test hypotheses pertaining to community assembly. Our results demonstrate that given the appropriate physiochemical conditions, strong phylogenetic, and trait variation, as well as habitat filtering, can occur at the millimeter-scale.

A method to solve the forward problem in magnetic induction tomography based on the weakly coupled field approximation.

Magnetic induction tomography (MIT) is a noninvasive modality for imaging the complex conductivity (kappa = sigma + jomegaepsilon) or the magnetic permeability (mu) of a target under investigation. Because MIT employs noncontact coils for excitation and detection, MIT may be suitable for imaging biological tissues. In medical applications where high resolutions are sought, image reconstruction is a time and memory consuming task because the associated inverse problem is nonlinear and ill-posed. The time and memory constraints are mainly imposed by the solution of the forward problem within the iterative image reconstruction procedure. This paper investigates the application of a weakly coupled approximation to the solution of the forward problem and examines the accuracy against the computation time and memory gained in adopting this approximation. Initially, an analytical solution for mutual impedance change of a coil pair due to a large planar conductive object is presented based on a full wave theory and used to demonstrate a 10 MHz frequency excitation as an acceptable upper frequency limit under which the approximation is valid. Subsequently, a numerical impedance method adopting the approximation is presented. Here the impedance method is used to solve the forward problem, which employs electrical circuit analogues to mesh the target into a network that can be solved using circuit analysis and sparse matrix technique. The error due to the approximation is further estimated numerically with the impedance method against a commercial finite-element package (commercial FE solver, COMSOL) and results show at 10 MHz excitation a 0.4% of tolerance is achieved for conductivities in the range <0.5 S/m. The results also show the method can be applied for low conductivity medical applications and is computationally efficient compared to equivalent finite-element methods.