Synthesis of recovery patterns in microbial communities across environments.

BACKGROUND: Disturbances alter the diversity and composition of microbial communities. Yet a generalized empirical assessment of microbiome responses to disturbance across different environments is needed to understand the factors driving microbiome recovery, and the role of the environment in driving these patterns. RESULTS: To this end, we combined null models with Bayesian generalized linear models to examine 86 time series of disturbed mammalian, aquatic, and soil microbiomes up to 50 days following disturbance. Overall, disturbances had the strongest effect on mammalian microbiomes, which lost taxa and later recovered their richness, but not their composition. In contrast, following disturbance, aquatic microbiomes tended away from their pre-disturbance composition over time. Surprisingly, across all environments, we found no evidence of increased compositional dispersion (i.e., variance) following disturbance, in contrast to the expectations of the Anna Karenina Principle. CONCLUSIONS: This is the first study to systematically compare secondary successional dynamics across disturbed microbiomes, using a consistent temporal scale and modeling approach. Our findings show that the recovery of microbiomes is environment-specific, and helps to reconcile existing, environment-specific research into a unified perspective. Video Abstract.

Synthesis reveals approximately balanced biotic differentiation and homogenization.

It is commonly thought that the biodiversity crisis includes widespread declines in the spatial variation of species composition, called biotic homogenization. Using a typology relating homogenization and differentiation to local and regional diversity changes, we synthesize patterns across 461 metacommunities surveyed for 10 to 91 years, and 64 species checklists (13 to 500+ years). Across all datasets, we found that no change was the most common outcome, but with many instances of homogenization and differentiation. A weak homogenizing trend of a 0.3% increase in species shared among communities/year on average was driven by increased numbers of widespread (high occupancy) species and strongly associated with checklist data that have longer durations and large spatial scales. At smaller spatial and temporal scales, we show that homogenization and differentiation can be driven by changes in the number and spatial distributions of both rare and common species. The multiscale perspective introduced here can help identify scale-dependent drivers underpinning biotic differentiation and homogenization.

Widespread shifts in body size within populations and assemblages.

Biotic responses to global change include directional shifts in organismal traits. Body size, an integrative trait that determines demographic rates and ecosystem functions, is thought to be shrinking in the Anthropocene. Here, we assessed the prevalence of body size change in six taxon groups across 5025 assemblage time series spanning 1960 to 2020. Using the Price equation to partition this change into within-species body size versus compositional changes, we detected prevailing decreases in body size through time driven primarily by fish, with more variable patterns in other taxa. We found that change in assemblage composition contributes more to body size changes than within-species trends, but both components show substantial variation in magnitude and direction. The biomass of assemblages remains quite stable as decreases in body size trade off with increases in abundance.

Looking back on biodiversity change: lessons for the road ahead.

Estimating biodiversity change across the planet in the context of widespread human modification is a critical challenge. Here, we review how biodiversity has changed in recent decades across scales and taxonomic groups, focusing on four diversity metrics: species richness, temporal turnover, spatial beta-diversity and abundance. At local scales, change across all metrics includes many examples of both increases and declines and tends to be centred around zero, but with higher prevalence of declining trends in beta-diversity (increasing similarity in composition across space or biotic homogenization) and abundance. The exception to this pattern is temporal turnover, with changes in species composition through time observed in most local assemblages. Less is known about change at regional scales, although several studies suggest that increases in richness are more prevalent than declines. Change at the global scale is the hardest to estimate accurately, but most studies suggest extinction rates are probably outpacing speciation rates, although both are elevated. Recognizing this variability is essential to accurately portray how biodiversity change is unfolding, and highlights how much remains unknown about the magnitude and direction of multiple biodiversity metrics at different scales. Reducing these blind spots is essential to allow appropriate management actions to be deployed. This article is part of the theme issue 'Detecting and attributing the causes of biodiversity change: needs, gaps and solutions'.

Understanding 'it depends' in ecology: a guide to hypothesising, visualising and interpreting statistical interactions.

Ecologists routinely use statistical models to detect and explain interactions among ecological drivers, with a goal to evaluate whether an effect of interest changes in sign or magnitude in different contexts. Two fundamental properties of interactions are often overlooked during the process of hypothesising, visualising and interpreting interactions between drivers: the measurement scale - whether a response is analysed on an additive or multiplicative scale, such as a ratio or logarithmic scale; and the symmetry - whether dependencies are considered in both directions. Overlooking these properties can lead to one or more of three inferential errors: misinterpretation of (i) the detection and magnitude (Type-D error), and (ii) the sign of effect modification (Type-S error); and (iii) misidentification of the underlying processes (Type-A error). We illustrate each of these errors with a broad range of ecological questions applied to empirical and simulated data sets. We demonstrate how meta-analysis, a widely used approach that seeks explicitly to characterise context dependence, is especially prone to all three errors. Based on these insights, we propose guidelines to improve hypothesis generation, testing, visualisation and interpretation of interactions in ecology.

Six years of demography data for 11 reef coral species.

Scleractinian corals are colonial animals with a range of life-history strategies, making up diverse species assemblages that define coral reefs. We tagged and tracked ~30 colonies from each of 11 species during seven trips spanning 6 years (2009-2015) to measure their vital rates and competitive interactions on the reef crest at Trimodal Reef, Lizard Island, Australia. Pairs of species were chosen from five growth forms in which one species of the pair was locally rare (R) and the other common (C). The sampled growth forms were massive (Goniastrea pectinata [R] and G. retiformis [C]), digitate (Acropora humilis [R] and A. cf. digitifera [C]), corymbose (A. millepora [R] and A. nasuta [C]), tabular (A. cytherea [R] and A. hyacinthus [C]) and arborescent (A. robusta [R] and A. intermedia [C]). An extra corymbose species with intermediate abundance, A. spathulata was included when it became apparent that A. millepora was too rare on the reef crest, making the 11 species in total. The tagged colonies were visited each year in the weeks prior to spawning. During visits, two or more observers each took two or three photographs of each tagged colony from directly above and on the horizontal plane with a scale plate to track planar area. Dead or missing colonies were recorded and new colonies tagged to maintain ~30 colonies per species throughout the 6 years of the study. In addition to tracking tagged corals, 30 fragments were collected from neighboring untagged colonies of each species for counting numbers of eggs per polyp (fecundity); and fragments of untagged colonies were brought into the laboratory where spawned eggs were collected for biomass and energy measurements. We also conducted surveys at the study site to generate size structure data for each species in several of the years. Each tagged colony photograph was digitized by at least two people. Therefore, we could examine sources of error in planar area for both photographers and outliners. Competitive interactions were recorded for a subset of species by measuring the margins of tagged colony outlines interacting with neighboring corals. The study was abruptly ended by Tropical Cyclone Nathan (Category 4) that killed all but nine of the more than 300 tagged colonies in early 2015. Nonetheless, these data will be of use to other researchers interested in coral demography and coexistence, functional ecology, and parametrizing population, community, and ecosystem models. The data set is not copyright restricted, and users should cite this paper when using the data.

Regional occupancy increases for widespread species but decreases for narrowly distributed species in metacommunity time series.

While human activities are known to elicit rapid turnover in species composition through time, the properties of the species that increase or decrease their spatial occupancy underlying this turnover are less clear. Here, we used an extensive dataset of 238 metacommunity time series of multiple taxa spread across the globe to evaluate whether species that are more widespread (large-ranged species) differed in how they changed their site occupancy over the 10-90 years the metacommunities were monitored relative to species that are more narrowly distributed (small-ranged species). We found that on average, large-ranged species tended to increase in occupancy through time, whereas small-ranged species tended to decrease. These relationships were stronger in marine than in terrestrial and freshwater realms. However, in terrestrial regions, the directional changes in occupancy were less extreme in protected areas. Our findings provide evidence for systematic decreases in occupancy of small-ranged species, and that habitat protection could mitigate these losses in the face of environmental change.

Linking changes in species composition and biomass in a globally distributed grassland experiment.

Global change drivers, such as anthropogenic nutrient inputs, are increasing globally. Nutrient deposition simultaneously alters plant biodiversity, species composition and ecosystem processes like aboveground biomass production. These changes are underpinned by species extinction, colonisation and shifting relative abundance. Here, we use the Price equation to quantify and link the contributions of species that are lost, gained or that persist to change in aboveground biomass in 59 experimental grassland sites. Under ambient (control) conditions, compositional and biomass turnover was high, and losses (i.e. local extinctions) were balanced by gains (i.e. colonisation). Under fertilisation, the decline in species richness resulted from increased species loss and decreases in species gained. Biomass increase under fertilisation resulted mostly from species that persist and to a lesser extent from species gained. Drivers of ecological change can interact relatively independently with diversity, composition and ecosystem processes and functions such as aboveground biomass due to the individual contributions of species lost, gained or persisting.

How does variation in total and relative abundance contribute to gradients of species diversity?

Patterns of biodiversity provide insights into the processes that shape biological communities around the world. Variation in species diversity along biogeographical or ecological gradients, such as latitude or precipitation, can be attributed to variation in different components of biodiversity: changes in the total abundance (i.e., more-individual effects) and changes in the regional species abundance distribution (SAD). Rarefaction curves can provide a tool to partition these sources of variation on diversity, but first must be converted to a common unit of measurement. Here, we partition species diversity gradients into components of the SAD and abundance using the effective number of species (ENS) transformation of the individual-based rarefaction curve. Because the ENS curve is unconstrained by sample size, it can act as a standardized unit of measurement when comparing effect sizes among different components of biodiversity change. We illustrate the utility of the approach using two data sets spanning latitudinal diversity gradients in trees and marine reef fish and find contrasting results. Whereas the diversity gradient of fish was mostly associated with variation in abundance (86%), the tree diversity gradient was mostly associated with variation in the SAD (59%). These results suggest that local fish diversity may be limited by energy through the more-individuals effect, while species pool effects are the larger determinant of tree diversity. We suggest that the framework of the ENS-curve has the potential to quantify the underlying factors influencing most aspects of diversity change.

Local biodiversity change reflects interactions among changing abundance, evenness, and richness.

Biodiversity metrics often integrate data on the presence and abundance of multiple species. Yet our understanding of covariation between changes to the numbers of individuals, the evenness of species relative abundances, and the total number of species remains limited. Using individual-based rarefaction curves, we show how expected positive relationships among changes in abundance, evenness and richness arise, and how they can break down. We then examined interdependencies between changes in abundance, evenness and richness in more than 1100 assemblages sampled either through time or across space. As predicted, richness changes were greatest when abundance and evenness changed in the same direction, and countervailing changes in abundance and evenness acted to constrain the magnitude of changes in species richness. Site-to-site differences in abundance, evenness, and richness were often decoupled, and pairwise relationships between these components across assemblages were weak. In contrast, changes in species richness and relative abundance were strongly correlated for assemblages varying through time. Temporal changes in local biodiversity showed greater inertia and stronger relationships between the component changes when compared to site-to-site variation. Overall, local variation in assemblage diversity was rarely due to repeated passive samples from an approximately static species abundance distribution. Instead, changing species relative abundances often dominated local variation in diversity. Moreover, how changing relative abundances combined with changes to total abundance frequently determined the magnitude of richness changes. Embracing the interdependencies between changing abundance, evenness and richness can provide new information to better understand biodiversity change in the Anthropocene.

Long-term changes in temperate marine fish assemblages are driven by a small subset of species.

The species composition of plant and animal assemblages across the globe has changed substantially over the past century. How do the dynamics of individual species cause this change? We classified species into seven unique categories of temporal dynamics based on the ordered sequence of presences and absences that each species contributes to an assemblage time series. We applied this framework to 14,434 species trajectories comprising 280 assemblages of temperate marine fishes surveyed annually for 20 or more years. Although 90% of the assemblages diverged in species composition from the baseline year, this compositional change was largely driven by only 8% of the species' trajectories. Quantifying the reorganization of assemblages based on species shared temporal dynamics should facilitate the task of monitoring and restoring biodiversity. We suggest ways in which our framework could provide informative measures of compositional change, as well as leverage future research on pattern and process in ecological systems.

A synthesis of land use impacts on stream biodiversity across metrics and scales.

While land use intensification is a major driver of biodiversity change in streams, the nature of such changes, and at which scales they occur, have not been synthesized. To synthesize how land use change has altered multiple components of stream biodiversity across scales, we compiled data from 37 studies where comparative data were available for species' total and relative abundances from multiple locations including reference (less impacted) streams to those surrounded by different land use types (urban, forestry, and agriculture). We found that each type of land use reduced multiple components of within-stream biodiversity across scales, but that urbanization consistently had the strongest effects. However, we found that ß-diversity among streams in modified landscapes did not differ from ß-diversity observed among reference streams, suggesting little evidence for biotic homogenization. Nevertheless, assemblage composition did experience considerable species turnover between reference and modified streams. Our results emphasize that to understand how anthropogenic factors such as land use alter biodiversity, multiple components of biodiversity within and among sites must be simultaneously considered at multiple scales.

Effects of site-selection bias on estimates of biodiversity change.

Estimates of biodiversity change are essential for the management and conservation of ecosystems. Accurate estimates rely on selecting representative sites, but monitoring often focuses on sites of special interest. How such site-selection biases influence estimates of biodiversity change is largely unknown. Site-selection bias potentially occurs across four major sources of biodiversity data, decreasing in likelihood from citizen science, museums, national park monitoring, and academic research. We defined site-selection bias as a preference for sites that are either densely populated (i.e., abundance bias) or species rich (i.e., richness bias). We simulated biodiversity change in a virtual landscape and tracked the observed biodiversity at a sampled site. The site was selected either randomly or with a site-selection bias. We used a simple spatially resolved, individual-based model to predict the movement or dispersal of individuals in and out of the chosen sampling site. Site-selection bias exaggerated estimates of biodiversity loss in sites selected with a bias by on average 300-400% compared with randomly selected sites. Based on our simulations, site-selection bias resulted in positive trends being estimated as negative trends: richness increase was estimated as 0.1 in randomly selected sites, whereas sites selected with a bias showed a richness change of -0.1 to -0.2 on average. Thus, site-selection bias may falsely indicate decreases in biodiversity. We varied sampling design and characteristics of the species and found that site-selection biases were strongest in short time series, for small grains, organisms with low dispersal ability, large regional species pools, and strong spatial aggregation. Based on these findings, to minimize site-selection bias, we recommend use of systematic site-selection schemes; maximizing sampling area; calculating biodiversity measures cumulatively across plots; and use of biodiversity measures that are less sensitive to rare species, such as the effective number of species. Awareness of the potential impact of site-selection bias is needed for biodiversity monitoring, the design of new studies on biodiversity change, and the interpretation of existing data.

Efectos del Sesgo en la Selección de Sitio sobre las Estimaciones del Cambio en la Biodiversidad Resumen Las estimaciones del cambio en la biodiversidad son esenciales para el manejo y la conservación de los ecosistemas. Las estimaciones precisas dependen de la selección de sitios representativos pero su monitoreo con frecuencia se enfoca en los sitios de interés especial. En su mayoría se desconoce cómo influyen tales sesgos en la selección de sitios sobre las estimaciones del cambio en la biodiversidad. El sesgo en la selección de sitios ocurre potencialmente en cuatro fuentes principales de datos sobre biodiversidad, disminuyendo en probabilidad cuando los datos vienen de la ciencia ciudadana, museos, el monitoreo de los parques nacionales y la investigación académica. Definimos al sesgo en la selección de sitios como la preferencia por sitios que están densamente poblados (es decir, sesgo por abundancia) o que son ricos en especies (es decir, sesgo por riqueza). Simulamos el cambio en la biodiversidad en un paisaje virtual y le dimos seguimiento a la biodiversidad observada en un sitio muestreado. El sitio fue seleccionado al azar o con un sesgo en la selección de sitio. Usamos un modelo simple basado en los individuos y resuelto espacialmente para predecir el movimiento o la dispersión de los individuos dentro y fuera del sitio de muestreo elegido. El sesgo en la selección de sitio exageró las estimaciones de la pérdida de la biodiversidad en los sitios seleccionados con un sesgo en promedio de 300-400% en comparación con sitios seleccionados al azar. Con base en nuestras simulaciones, el sesgo en la selección de sitio derivó en que las tendencias positivas se estimaran como tendencias negativas: se estimó que el incremento en la riqueza fue de 0.1 en sitios seleccionados al azar, mientras que en los sitios seleccionados con un sesgo mostraron un cambio en la riqueza de −0.1 a −0.2 en promedio. Así, el sesgo en la selección de sitio puede indicar erróneamente la existencia de disminuciones en la biodiversidad. Variamos el diseño del muestreo y las características de las especies y encontramos que los sesgos en la selección de sitio estaban más consolidados en las series de tiempo corto, para los granos pequeños, organismos con una baja habilidad de dispersión, grandes patrimonios genéticos de especies regionales y una agregación espacial fuerte. Con base en estos resultados, para lograr minimizar el sesgo en la selección de sitio, recomendamos usar esquemas sistemáticos de selección de sitio; maximizar el área de muestreo; calcular las medidas de biodiversidad acumulativamente en los lotes; y usar las medidas de biodiversidad que son menos sensibles a las especies raras, como el número efectivo de especies. Se necesita tener conciencia sobre el impacto potencial del sesgo en la selección de sitio para el monitoreo de la biodiversidad, el diseño de nuevos estudios sobre el cambio en la biodiversidad y la interpretación de los datos existentes.

A multiscale framework for disentangling the roles of evenness, density, and aggregation on diversity gradients.

Disentangling the drivers of diversity gradients can be challenging. The Measurement of Biodiversity (MoB) framework decomposes scale-dependent changes in species diversity into three components of community structure: species abundance distribution (SAD), total community abundance, and within-species spatial aggregation. Here we extend MoB from categorical treatment comparisons to quantify variation along continuous geographic or environmental gradients. Our approach requires sites along a gradient, each consisting of georeferenced plots of abundance-based species composition data. We demonstrate our method using a case study of ants sampled along an elevational gradient of 28 sites in a mixed deciduous forest of the Great Smoky Mountains National Park, USA. MoB analysis revealed that decreases in ant species richness along the elevational gradient were associated with decreasing evenness and total number of species, which counteracted the modest increase in richness associated with decreasing spatial aggregation along the gradient. Total community abundance had a negligible effect on richness at all but the finest spatial grains, SAD effects increased in importance with sampling effort, and the aggregation effect had the strongest effect at coarser spatial grains. These results do not support the more-individuals hypothesis, but they are consistent with a hypothesis of stronger environmental filtering at coarser spatial grains. Our extension of MoB has the potential to elucidate how components of community structure contribute to changes in diversity along environmental gradients and should be useful for a variety of assemblage-level data collected along gradients.

A geometric basis for surface habitat complexity and biodiversity.

Structurally complex habitats tend to contain more species and higher total abundances than simple habitats. This ecological paradigm is grounded in first principles: species richness scales with area, and surface area and niche density increase with three-dimensional complexity. Here we present a geometric basis for surface habitats that unifies ecosystems and spatial scales. The theory is framed by fundamental geometric constraints between three structure descriptors-surface height, rugosity and fractal dimension-and explains 98% of surface variation in a structurally complex test system: coral reefs. Then, we show how coral biodiversity metrics (species richness, total abundance and probability of interspecific encounter) vary over the theoretical structure descriptor plane, demonstrating the value of the theory for predicting the consequences of natural and human modifications of surface structure.

Ecosystem decay exacerbates biodiversity loss with habitat loss.

Although habitat loss is the predominant factor leading to biodiversity loss in the Anthropocene1,2, exactly how this loss manifests-and at which scales-remains a central debate3-6. The 'passive sampling' hypothesis suggests that species are lost in proportion to their abundance and distribution in the natural habitat7,8, whereas the 'ecosystem decay' hypothesis suggests that ecological processes change in smaller and more-isolated habitats such that more species are lost than would have been expected simply through loss of habitat alone9,10. Generalizable tests of these hypotheses have been limited by heterogeneous sampling designs and a narrow focus on estimates of species richness that are strongly dependent on scale. Here we analyse 123 studies of assemblage-level abundances of focal taxa taken from multiple habitat fragments of varying size to evaluate the influence of passive sampling and ecosystem decay on biodiversity loss. We found overall support for the ecosystem decay hypothesis. Across all studies, ecosystems and taxa, biodiversity estimates from smaller habitat fragments-when controlled for sampling effort-contain fewer individuals, fewer species and less-even communities than expected from a sample of larger fragments. However, the diversity loss due to ecosystem decay in some studies (for example, those in which habitat loss took place more than 100 years ago) was less than expected from the overall pattern, as a result of compositional turnover by species that were not originally present in the intact habitats. We conclude that the incorporation of non-passive effects of habitat loss on biodiversity change will improve biodiversity scenarios under future land use, and planning for habitat protection and restoration.

Reducing dispersal limitation via seed addition increases species richness but not above-ground biomass.

Seed dispersal limitation, which can be exacerbated by a number of anthropogenic causes, can result in local communities having fewer species than they might potentially support, representing a potential diversity deficit. The link between processes that shape natural variation in diversity, such as dispersal limitation, and the consequent effects on productivity is less well known. Here, we synthesised data from 12 seed addition experiments in grassland communities to examine the influence of reducing seed dispersal limitation (from 1 to 60 species added across experiments) on species richness and productivity. For every 10 species of seed added, we found that species richness increased by about two species. However, the increase in species richness by overcoming seed limitation did not lead to a concomitant increase in above-ground biomass production. This highlights the need to consider the relationship between biodiversity and ecosystem functioning in a pluralistic way that considers both the processes that shape diversity and productivity simultaneously in naturally assembled communities.

Landscape-scale forest loss as a catalyst of population and biodiversity change.

Global biodiversity assessments have highlighted land-use change as a key driver of biodiversity change. However, there is little empirical evidence of how habitat transformations such as forest loss and gain are reshaping biodiversity over time. We quantified how change in forest cover has influenced temporal shifts in populations and ecological assemblages from 6090 globally distributed time series across six taxonomic groups. We found that local-scale increases and decreases in abundance, species richness, and temporal species replacement (turnover) were intensified by as much as 48% after forest loss. Temporal lags in population- and assemblage-level shifts after forest loss extended up to 50 years and increased with species' generation time. Our findings that forest loss catalyzes population and biodiversity change emphasize the complex biotic consequences of land-use change.

Temperature-related biodiversity change across temperate marine and terrestrial systems.

Climate change is reshaping global biodiversity as species respond to changing temperatures. However, the net effects of climate-driven species redistribution on local assemblage diversity remain unknown. Here, we relate trends in species richness and abundance from 21,500 terrestrial and marine assemblage time series across temperate regions (23.5-60.0° latitude) to changes in air or sea surface temperature. We find a strong coupling between biodiversity and temperature changes in the marine realm, where species richness mostly increases with warming. However, biodiversity responses are conditional on the baseline climate, such that in initially warmer locations richness increase is more pronounced while abundance declines with warming. In contrast, we do not detect systematic temperature-related richness or abundance trends on land, despite a greater magnitude of warming. As the world is committed to further warming, substantial challenges remain in maintaining local biodiversity amongst the non-uniform inflow and outflow of 'climate migrants'. Temperature-driven community restructuring is especially evident in the ocean, whereas climatic debt may be accumulating on land.

The geography of biodiversity change in marine and terrestrial assemblages.

Human activities are fundamentally altering biodiversity. Projections of declines at the global scale are contrasted by highly variable trends at local scales, suggesting that biodiversity change may be spatially structured. Here, we examined spatial variation in species richness and composition change using more than 50,000 biodiversity time series from 239 studies and found clear geographic variation in biodiversity change. Rapid compositional change is prevalent, with marine biomes exceeding and terrestrial biomes trailing the overall trend. Assemblage richness is not changing on average, although locations exhibiting increasing and decreasing trends of up to about 20% per year were found in some marine studies. At local scales, widespread compositional reorganization is most often decoupled from richness change, and biodiversity change is strongest and most variable in the oceans.