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A practical guide to understanding and validating complex models using data simulations

Biologists routinely fit novel and complex statistical models to push the limits of our understanding. Examples include, but are not limited to, flexible Bayesian approaches (e.g. BUGS, stan), frequentist and likelihood-based approaches (e.g. packages lme4 ) and machine learning methods. These software and programs afford the user greater control and flexibility in tailoring complex hierarchical models. However, this level of control and flexibility places a higher degree of responsibility on the user to evaluate the robustness of their statistical inference. To determine how often biologists are running model diagnostics on hierarchical models, we reviewed 50 recently published papers in 2021 in the journal Nature Ecology & Evolution , and we found that the majority of published papers did not report any validation of their hierarchical models, making it difficult for the reader to assess the robustness of their inference. This lack of reporting likely stems from a lack of standardized guidance for best practices and standard methods. Here, we provide a guide to understanding and validating complex models using data simulations. To determine how often biologists use data simulation techniques, we also reviewed 50 recently published papers in 2021 in the journal Methods Ecology & Evolution . We found that 78% of the papers that proposed a new estimation technique, package or model used simulations or generated data in some capacity (18 of 23 papers); but very few of those papers (5 of 23 papers) included either a demonstration that the code could recover realistic estimates for a dataset with known parameters or a demonstration of the statistical properties of the approach. To distil the variety of simulations techniques and their uses, we provide a taxonomy of simulation studies based on the intended inference. We also encourage authors to include a basic validation study whenever novel statistical models are used, which in general, is easy to implement. Simulating data helps a researcher gain a deeper understanding of the models and their assumptions and establish the reliability of their estimation approaches. Wider adoption of data simulations by biologists can improve statistical inference, reliability and open science practices.

Methods in Ecology and Evolution

Paleoclimate ocean conditions shaped the evolution of corals and their skeletal composition through deep time

Identifying how past environmental conditions shaped the evolution of corals and their skeletal traits provides a framework for predicting their persistence and that of their non-calcifying relatives under impending global warming and ocean acidification. Here we show that ocean geochemistry, particularly aragonite–calcite seas, drives patterns of morphological evolution in anthozoans (corals, sea anemones) by examining skeletal traits in the context of a robust, time-calibrated phylogeny. The lability of skeletal composition among octocorals suggests a greater ability to adapt to changes in ocean chemistry compared with the homogeneity of the aragonitic skeleton of scleractinian corals. Pulses of diversification in anthozoans follow mass extinctions and reef crises, with sea anemones and proteinaceous corals filling empty niches as tropical reef builders went extinct. Changing environmental conditions will likely diminish aragonitic reef-building scleractinians, but the evolutionary history of the Anthozoa suggests other groups will persist and diversify in their wake.

Nature Ecology & Evolution

Signals of impending change

Society has an increasing awareness that there are finite limits to what we can expect the planet to absorb and still provide goods and services at current rates 1 . Both historical reconstructions and contemporary events continue to remind us that ecological regime changes are often abrupt rather than gradual. This reality motivates researchers who seek to discover leading indicators for impending ecosystem change. Berdugo et al . 2 report an important advance in our ability to anticipate the conversion of arid lands from self-organized, self-maintaining and productive ecosystems, to a state characterized by disorganization and low functionality. Such conversions have important implications for our understanding of ‘desertification’ — which is a shift from arid to desert-like conditions. Theoretical studies have suggested that patterns in the patchiness of vegetation might indicate how close a system is to making an abrupt change to desert-like conditions 3 , 4 , 5 . Empirical studies, however, have tended to show instead that simply the total cover of vegetation, rather than its arrangement, often foretells the state of the system 4 , 5 , 6 , 7 , 8 , 9 . Berdugo et al . 2 combine these competing ideas into one integrated perspective. They show how major environmental drivers, such as aridity, influence both vegetation cover and patchiness, as well as where self-organizing, stabilizing forces in the vegetation are likely to be found.

Nature Ecology & Evolution

A decade of insights into grassland ecosystem responses to global environmental change

Earth’s biodiversity and carbon uptake by plants, or primary productivity, are intricately interlinked, underlie many essential ecosystem processes, and depend on the interplay among environmental factors, many of which are being changed by human activities. While ecological theory generalizes across taxa and environments, most empirical tests of factors controlling diversity and productivity have been observational, single-site experiments, or meta-analyses, limiting our understanding of variation among site-level responses and tests of general mechanisms. A synthesis of results from ten years of a globally distributed, coordinated experiment, the Nutrient Network (NutNet), demonstrates that species diversity promotes ecosystem productivity and stability, and that nutrient supply and herbivory control diversity via changes in composition, including invasions of non-native species and extinction of native species. Distributed experimental networks are a powerful tool for tests and integration of multiple theories and for generating multivariate predictions about the effects of global changes on future ecosystems.

Nature Ecology & Evolution

Global hotspots and correlates of alien species richness across taxonomic groups

Human-mediated transport beyond biogeographic barriers has led to the introduction and establishment of alien species in new regions worldwide. However, we lack a global picture of established alien species richness for multiple taxonomic groups. Here, we assess global patterns and potential drivers of established alien species richness across eight taxonomic groups (amphibians, ants, birds, freshwater fishes, mammals, vascular plants, reptiles and spiders) for 186 islands and 423 mainland regions. Hotspots of established alien species richness are predominantly island and coastal mainland regions. Regions with greater gross domestic product per capita, human population density, and area have higher established alien richness, with strongest effects emerging for islands. Ants and reptiles, birds and mammals, and vascular plants and spiders form pairs of taxonomic groups with the highest spatial congruence in established alien richness, but drivers explaining richness differ between the taxa in each pair. Across all taxonomic groups, our results highlight the need to prioritize prevention of further alien species introductions to island and coastal mainland regions globally.

Nature Ecology & Evolution

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.

Nature Ecology & Evolution

New interventions are needed to save coral reefs

Since 2014, coral reefs worldwide have been subjected to the most extensive, prolonged and damaging heat wave in recorded history1. Large sections of Australia’s Great Barrier Reef (GBR) bleached in response to heat stress in 2016 and 2017 — the first back-to-back event on record. Such severe coral bleaching results in widespread loss of reef habitat and biodiversity. Globally, we are facing catastrophic decline of these ecosystems, which sustain services valued at around $US 10 trillion per year2, are home to over a million species3, and feed and support the livelihoods of hundreds of millions of people4. Model predictions indicate that mass coral bleaching could become the new norm by 2050 (ref. 5). Critically, even if global warming can be kept within 1.5⁰C above preindustrial levels, shallow tropical seas would warm at least 0.4°C in coming decades, triggering frequent bleaching of the most sensitive habitat-forming coral species6. This outlook poses a time-critical decision challenge for management and conservation. Existing conservation approaches, despite innovative governance arrangements7, could simply become insufficient to protect coral reefs under any expected climate future. Thus, for coral reefs to remain resilient and their services sustained, we argue that new and potentially riskier interventions must be implemented alongside conventional management efforts and strong action to curb global warming. We build the case for this strategy below.

Nature Ecology & Evolution

Change in dominance determines herbivore effects on plant biodiversity

Herbivores alter plant biodiversity (species richness) in many of the world’s ecosystems, but the magnitude and the direction of herbivore effects on biodiversity vary widely within and among ecosystems. One current theory predicts that herbivores enhance plant biodiversity at high productivity but have the opposite effect at low productivity. Yet, empirical support for the importance of site productivity as a mediator of these herbivore impacts is equivocal. Here, we synthesize data from 252 large-herbivore exclusion studies, spanning a 20-fold range in site productivity, to test an alternative hypothesis—that herbivore-induced changes in the competitive environment determine the response of plant biodiversity to herbivory irrespective of productivity. Under this hypothesis, when herbivores reduce the abundance (biomass, cover) of dominant species (for example, because the dominant plant is palatable), additional resources become available to support new species, thereby increasing biodiversity. By contrast, if herbivores promote high dominance by increasing the abundance of herbivory-resistant, unpalatable species, then resource availability for other species decreases reducing biodiversity. We show that herbivore-induced change in dominance, independent of site productivity or precipitation (a proxy for productivity), is the best predictor of herbivore effects on biodiversity in grassland and savannah sites. Given that most herbaceous ecosystems are dominated by one or a few species, altering the competitive environment via herbivores or by other means may be an effective strategy for conserving biodiversity in grasslands and savannahs globally.

Nature Ecology & Evolution

Migratory coupling between predators and prey

Animal migrations act to couple ecosystems and are undertaken by some of the world’s most endangered taxa. Predators often exploit migrant prey, but the movements taken by these consumers are rarely studied or understood. We define such movements, where migrant prey induce large-scale movements of predators, as migratory coupling. Migratory coupling can have ecological consequences for the participating prey, predators and the communities they traverse across the landscape. We review examples of migratory coupling in the literature and provide hypotheses regarding conditions favourable for their occurrence. We also provide a framework for interactions induced by migratory coupling and demonstrate their potential community-level impacts by examining other forms of spatial shifts in predators. Migratory coupling integrates the fields of landscape, movement, food web and community ecologies, and represents an understudied frontier in ecology.

Nature Ecology & Evolution

Towards common ground in the biodiversity–disease debate

The disease ecology community has struggled to come to consensus on whether biodiversity reduces or increases infectious disease risk, a question that directly affects policy decisions for biodiversity conservation and public health. Here, we summarize the primary points of contention regarding biodiversity–disease relationships and suggest that vector-borne, generalist wildlife and zoonotic pathogens are the types of parasites most likely to be affected by changes to biodiversity. One synthesis on this topic revealed a positive correlation between biodiversity and human disease burden across countries, but as biodiversity changed over time within these countries, this correlation became weaker and more variable. Another synthesis—a meta-analysis of generally smaller-scale experimental and field studies—revealed a negative correlation between biodiversity and infectious diseases (a dilution effect) in various host taxa. These results raise the question of whether biodiversity–disease relationships are more negative at smaller spatial scales. If so, biodiversity conservation at the appropriate scales might prevent wildlife and zoonotic diseases from increasing in prevalence or becoming problematic (general proactive approaches). Further, protecting natural areas from human incursion should reduce zoonotic disease spillover. By contrast, for some infectious diseases, managing particular species or habitats and targeted biomedical approaches (targeted reactive approaches) might outperform biodiversity conservation as a tool for disease control. Importantly, biodiversity conservation and management need to be considered alongside other disease management options. These suggested guiding principles should provide common ground that can enhance scientific and policy clarity for those interested in simultaneously improving wildlife and human health.

Nature Ecology & Evolution

Dryland mechanisms could widely control ecosystem functioning in a drier and warmer world

Responses of terrestrial ecosystems to climate change have been explored in many regions worldwide. While continued drying and warming may alter process rates and deteriorate the state and performance of ecosystems, it could also lead to more fundamental changes in the mechanisms governing ecosystem functioning. Here we argue that climate change will induce unprecedented shifts in these mechanisms in historically wetter climatic zones, towards mechanisms currently prevalent in dry regions, which we refer to as ‘dryland mechanisms’. We discuss 12 dryland mechanisms affecting multiple processes of ecosystem functioning, including vegetation development, water flow, energy budget, carbon and nutrient cycling, plant production and organic matter decomposition. We then examine mostly rare examples of the operation of these mechanisms in non-dryland regions where they have been considered irrelevant at present. Current and future climate trends could force microclimatic conditions across thresholds and lead to the emergence of dryland mechanisms and their increasing control over ecosystem functioning in many biomes on Earth.

Nature Ecology & Evolution

A global biodiversity observing system to unite monitoring and guide action

The rate and extent of global biodiversity change is surpassing our ability to measure, monitor and forecast trends. We propose an interconnected worldwide system of observation networks — a global biodiversity observing system (GBiOS) — to coordinate monitoring worldwide and inform action to reach international biodiversity targets.

Nature Ecology & Evolution

Climate-induced tree-mortality pulses are obscured by broad-scale and long-term greening

Vegetation greening has been suggested to be a dominant trend over recent decades, but severe pulses of tree mortality in forests after droughts and heatwaves have also been extensively reported. These observations raise the question of to what extent the observed severe pulses of tree mortality induced by climate could affect overall vegetation greenness across spatial grains and temporal extents. To address this issue, here we analyse three satellite-based datasets of detrended growing-season normalized difference vegetation index (NDVI GS ) with spatial resolutions ranging from 30 m to 8 km for 1,303 field-documented sites experiencing severe drought- or heat-induced tree-mortality events around the globe. We find that severe tree-mortality events have distinctive but localized imprints on vegetation greenness over annual timescales, which are obscured by broad-scale and long-term greening. Specifically, although anomalies in NDVI GS (ΔNDVI) are negative during tree-mortality years, this reduction diminishes at coarser spatial resolutions (that is, 250 m and 8 km). Notably, tree-mortality-induced reductions in NDVI GS (|ΔNDVI|) at 30-m resolution are negatively related to native plant species richness and forest height, whereas topographic heterogeneity is the major factor affecting ΔNDVI differences across various spatial grain sizes. Over time periods of a decade or longer, greening consistently dominates all spatial resolutions. The findings underscore the fundamental importance of spatio-temporal scales for cohesively understanding the effects of climate change on forest productivity and tree mortality under both gradual and abrupt changes.

Nature Ecology & Evolution

Neonatal antipredator tactics shape female movement patterns in large herbivores

Caring for newborn offspring hampers resource acquisition of mammalian females, curbing their ability to meet the high energy expenditure of early lactation. Newborns are particularly vulnerable, and large herbivores have evolved a continuum of neonatal anti-predator tactics, ranging from immobile hider to highly mobile follower offspring. How these tactics constrain female movements around parturition is unknown, particularly within the current context of increasing habitat fragmentation and earlier plant phenology caused by global warming. Using a analysis across 54 populations of 23 species of large herbivores, we show that mothers adjust their movements to variation in resource productivity and heterogeneity according to their offspring’s neonatal tactic. Mothers with hider offspring are unable to exploit environments where the variability of resources occurs at a broad scale, which might alter resource allocation compared to mothers with follower offspring. Our findings reveal that the overlooked neonatal tactic plays a key role for predicting how species are coping with environmental variation.

Nature Ecology & Evolution

Species diversity links land consolidation to rodent disease

Four decades of data on rodent species composition and hantavirus prevalence across a changing urban–agricultural landscape demonstrate that long-term data are key for understanding links between biodiversity loss and disease dynamics

Nature Ecology & Evolution

Shotgun sequencing of airborne eDNA achieves rapid assessment of whole biomes, population genetics and genomic variation

Biodiversity and its associated genetic diversity are being lost at an unprecedented rate. Simultaneously, the distributions of flora, fauna, fungi, microbes and pathogens are rapidly changing. Novel technology can help to capture and record genetic diversity before it is lost and to measure population shifts and pathogen distributions. Here we report the rapid application of shotgun long-read environmental DNA (eDNA) analysis for non-invasive biodiversity, genetic diversity and pathogen assessments from air. We also compared air eDNA with water and soil eDNA. Coupling long-read sequencing with established cloud-based biodiversity pipelines enabled a 2-day turnaround from airborne sample collection to completed analysis by a single investigator. To determine the full utility of airborne eDNA, we also conducted a local bioinformatic analysis and deep short-read shotgun sequencing. From outdoor air eDNA alone, comprehensive genetic analysis was performed, including population genetics (phylogenetic placement) of a charismatic mammal (bobcat, Lynx rufus ) and a venomous spider (golden silk orb weaver, Trichonephila clavipes ), and haplotyping humans ( Homo sapiens ) from natural complex community settings, such as subtropical forests and temperate locations. The rich datasets also enabled deeper analysis of specific species and genomic regions of interest, including viral variant calling, human variant analysis and antimicrobial resistance gene surveillance from airborne DNA. Our results highlight the speed, versatility and specificity of pan-biodiversity monitoring via non-invasive eDNA sampling using current benchtop/portable and cloud-based approaches. Furthermore, they reveal the future feasibility of scaling down (equipment and temporally) these approaches for near real-time analysis. Together these approaches can enable rapid simultaneous detection of all life and its genetic diversity from air, water and sediment samples for unbiased non-targeted information-rich genomics-empowered (1) biodiversity monitoring, (2) population genetics, (3) pathogen and disease-vector genomic surveillance, (4) allergen and narcotic surveillance, (5) antimicrobial resistance surveillance and (6) bioprospecting.

Nature Ecology & Evolution

Vibrio pectenicida strain FHCF-3 is a causative agent of sea star wasting disease

More than 10 years following the onset of the sea star wasting disease (SSWD) epidemic, affecting over 20 asteroid species from Mexico to Alaska, the causative agent has been elusive. SSWD killed billions of the most susceptible species, sunflower sea stars ( Pycnopodia helianthoides ), initiating a trophic cascade involving unchecked urchin population growth and the widespread loss of kelp forests. Identifying the causative agent underpins the development of recovery strategies. Here we induced disease and subsequent mortality in exposure experiments using tissue extracts, coelomic fluid and effluent water from wasting sunflower sea stars, with no mortality in controls. Deep sequencing of diseased sea star coelomic fluid samples from experiments and field outbreaks revealed a dominant proportion of reads assigned to the bacterium Vibrio pectenicida . Fulfilling Koch’s postulates, V. pectenicida strain FHCF-3, cultured from the coelomic fluid of a diseased sunflower sea star, caused disease and mortality in exposed sunflower sea stars, demonstrating that it is a causative agent of SSWD. This discovery will enable recovery efforts for sea stars and the ecosystems affected by their decline by facilitating culture-based experimental research and broad-scale screening for pathogen presence and abundance in the laboratory and field.

Nature Ecology & Evolution

Best practices for genetic and genomic data archiving

Genetic and genomic data are collected for a vast array of scientific and applied purposes. Despite mandates for public archiving, data are typically used only by the generating authors. The reuse of genetic and genomic datasets remains uncommon because it is difficult, if not impossible, due to non-standard archiving practices and lack of contextual metadata. But as the new field of macrogenetics is demonstrating, if genetic data and their metadata were more accessible and FAIR (findable, accessible, interoperable and reusable) compliant, they could be reused for many additional purposes. We discuss the main challenges with existing genetic and genomic data archives, and suggest best practices for archiving genetic and genomic data. Recognizing that this is a longstanding issue due to little formal data management training within the fields of ecology and evolution, we highlight steps that research institutions and publishers could take to improve data archiving.

Nature, Ecology and Evolution