Restoring spatiotemporal variability to enhance the capacity for dispersal-limited species to track climate change.

Climate refugia are areas where species can persist through climate change with little to no movement. Among the factors associated with climate refugia are high spatial heterogeneity, such that there is only a short distance between current and future optimal climates, as well as biotic or abiotic environmental factors that buffer against variability in time. However, these types of climate refugia may be declining due to anthropogenic homogenization of environments and degradation of environmental buffers. To quantify the potential for restoration of refugia-like environmental conditions to increase population persistence under climate change, we simulated a population's capacity to track their temperature over space and time given different levels of spatial and temporal variability in temperature. To determine how species traits affected the efficacy of restoring heterogeneity, we explored an array of values for species' dispersal ability, thermal tolerance, and fecundity. We found that species were more likely to persist in environments with higher spatial heterogeneity and lower environmental stochasticity. When simulating a management action that increased the spatial heterogeneity of a previously homogenized environment, species were more likely to persist through climate change, and population sizes were generally higher, but there was little effect with mild temperature change. The benefits of heterogeneity restoration were greatest for species with limited dispersal ability. In contrast, species with longer dispersal but lower fecundity were more likely to benefit from a reduction in environmental stochasticity than an increase in spatial heterogeneity. Our results suggest that restoring environments to refugia-like conditions could promote species' persistence under the influence of climate change in addition to conservation strategies such as assisted migration, corridors, and increased protection.

Early warning signals have limited applicability to empirical lake data.

Research aimed at identifying indicators of persistent abrupt shifts in ecological communities, a.k.a regime shifts, has led to the development of a suite of early warning signals (EWSs). As these often perform inaccurately when applied to real-world observational data, it remains unclear whether critical transitions are the dominant mechanism of regime shifts and, if so, which EWS methods can predict them. Here, using multi-trophic planktonic data on multiple lakes from around the world, we classify both lake dynamics and the reliability of classic and second generation EWSs methods to predict whole-ecosystem change. We find few instances of critical transitions, with different trophic levels often expressing different forms of abrupt change. The ability to predict this change is highly processing dependant, with most indicators not performing better than chance, multivariate EWSs being weakly superior to univariate, and a recent machine learning model performing poorly. Our results suggest that predictive ecology should start to move away from the concept of critical transitions, developing methods suitable for predicting resilience loss not limited to the strict bounds of bifurcation theory.

Phenotypic response to different predator strategies can be mediated by temperature.

Temperature change affects biological systems in multifaceted ways, including the alteration of species interaction strengths, with implications for the stability of populations and communities. Temperature-dependent changes to antipredatory responses are an emerging mechanism of destabilization and thus there is a need to understand how prey species respond to predation pressures in the face of changing temperatures. Here, using ciliate protozoans, we assess whether temperature can alter the strength of phenotypic antipredator responses in a prey species and whether this relationship depends on the predator's hunting behavior. We exposed populations of the ciliate Paramecium caudatum to either (i) a sit-and-wait generalist predator (Homalozoon vermiculare) or (ii) a specialized active swimmer predator (Didinium nasutum) across two different temperature regimes (15 and 25°C) to quantify the temperature dependence of antipredator responses over a 24-h period. We utilized a novel high-throughput automated robotic monitoring system to track changes in the behavior (swimming speed) and morphology (cell size) of P. caudatum at frequencies and resolutions previously unachievable by manual sampling. The change in swimming speed through the 24 h differed between the two temperatures but was not altered by the presence of the predators. In contrast, P. caudatum showed a substantial temperature-dependent morphological response to the presence of D. nasutum (but not H. vermiculare), changing cell shape toward a more elongated morph at 15°C (but not at 25°C). Our findings suggest that temperature can have strong effects on prey morphological responses to predator presence, but that this response is potentially dependent on the predator's feeding strategy. This suggests that greater consideration of synergistic antipredator behavioral and physiological responses is required in species and communities subject to environmental changes.

Corridor quality buffers extinction under extreme droughts in experimental metapopulations.

Corridors with good-quality habitats maintain the spatial dynamics of metapopulations by promoting dispersal between habitat patches, potentially buffering populations, and communities against continued global change. However, this function is threatened by habitats becoming increasingly fragmented, and habitat matrices becoming increasingly inhospitable, potentially reducing the resilience and persistence of populations. Yet, we lack a clear understanding of how reduced corridor quality interacts with rates of environmental change to destabilize populations. Using laboratory microcosms containing metapopulations of the Collembola Folsomia candida, we investigate the impact of corridor quality on metapopulation persistence under a range of simulated droughts, a key stressor for this species. We manipulated both drought severity and the number of patches affected by drought across landscapes connected by either good- or poor-quality corridors. We measured the time of metapopulation extinction, the maximum rate of metapopulation decline, and the variability of abundance among patches as criteria to evaluate the persistence ability of metapopulations. We show that while drought severity negatively influenced the time of metapopulation extinction and the increase in drought patches caused metapopulation decline, these results were mitigated by good-quality corridors, which increased metapopulation persistence time and decreased both how fast metapopulations declined and the interpatch variability in abundances. Our results suggest that enhancing corridor quality can increase the persistence of metapopulations, increasing the time available for conservation actions to take effect, and/or for species to adapt or move in the face of continued stress. Given that fragmentation increases the isolation of habitats, improving the quality of habitat corridors may provide a useful strategy to enhance the resistance of spatially structured populations.

A predictive timeline of wildlife population collapse.

Contemporary rates of biodiversity decline emphasize the need for reliable ecological forecasting, but current methods vary in their ability to predict the declines of real-world populations. Acknowledging that stressor effects start at the individual level, and that it is the sum of these individual-level effects that drives populations to collapse, shifts the focus of predictive ecology away from using predominantly abundance data. Doing so opens new opportunities to develop predictive frameworks that utilize increasingly available multi-dimensional data, which have previously been overlooked for ecological forecasting. Here, we propose that stressed populations will exhibit a predictable sequence of observable changes through time: changes in individuals' behaviour will occur as the first sign of increasing stress, followed by changes in fitness-related morphological traits, shifts in the dynamics (for example, birth rates) of populations and finally abundance declines. We discuss how monitoring the sequential appearance of these signals may allow us to discern whether a population is increasingly at risk of collapse, or is adapting in the face of environmental change, providing a conceptual framework to develop new forecasting methods that combine multi-dimensional (for example, behaviour, morphology, life history and abundance) data.

Planktonic functional diversity changes in synchrony with lake ecosystem state.

Managing ecosystems to effectively preserve function and services requires reliable tools that can infer changes in the stability and dynamics of a system. Conceptually, functional diversity (FD) appears as a sensitive and viable monitoring metric stemming from suggestions that FD is a universally important measure of biodiversity and has a mechanistic influence on ecological processes. It is however unclear whether changes in FD consistently occur prior to state responses or vice versa, with no current work on the temporal relationship between FD and state to support a transition towards trait-based indicators. There is consequently a knowledge gap regarding when functioning changes relative to biodiversity change and where FD change falls in that sequence. We therefore examine the lagged relationship between planktonic FD and abundance-based metrics of system state (e.g. biomass) across five highly monitored lake communities using both correlation and cutting edge non-linear empirical dynamic modelling approaches. Overall, phytoplankton and zooplankton FD display synchrony with lake state but each lake is idiosyncratic in the strength of relationship. It is therefore unlikely that changes in plankton FD are identifiable before changes in more easily collected abundance metrics. These results highlight the power of empirical dynamic modelling in disentangling time lagged relationships in complex multivariate ecosystems, but suggest that FD cannot be generically viable as an early indicator. Individual lakes therefore require consideration of their specific context and any interpretation of FD across systems requires caution. However, FD still retains value as an alternative state measure or a trait representation of biodiversity when considered at the system level.

Spatiotemporal thermal variation drives diversity trends in experimental landscapes.

Temperature is a fundamental driver of species' vital rates and thus coexistence, extinctions and community composition. While temperature is neither static in space nor in time, little work has incorporated spatiotemporal dynamics into community-level investigations of thermal variation. We conducted a microcosm experiment using ciliate protozoa to test the effects of temperatures fluctuating synchronously or asynchronously on communities in two-patch landscapes connected by short or long corridors. We monitored the abundance of each species for 4 weeks-equivalent to ~28 generations-measuring the effects of four temperature regimes and two corridor lengths on community diversity and composition. While corridor length significantly altered the trajectory of diversity change in the communities, this did not result in different community structures at the end of the experiment. The type of thermal variation significantly affected both the temporal dynamics of diversity change and final community composition, with synchronous fluctuation causing deterministic extinctions that were consistent across replicates and spatial variation causing the greatest diversity declines. Our results suggest that the presence and type of thermal variation can play an important role in structuring ecological communities, especially when it interacts with dispersal between habitat patches.

Towards the fully automated monitoring of ecological communities.

High-resolution monitoring is fundamental to understand ecosystems dynamics in an era of global change and biodiversity declines. While real-time and automated monitoring of abiotic components has been possible for some time, monitoring biotic components-for example, individual behaviours and traits, and species abundance and distribution-is far more challenging. Recent technological advancements offer potential solutions to achieve this through: (i) increasingly affordable high-throughput recording hardware, which can collect rich multidimensional data, and (ii) increasingly accessible artificial intelligence approaches, which can extract ecological knowledge from large datasets. However, automating the monitoring of facets of ecological communities via such technologies has primarily been achieved at low spatiotemporal resolutions within limited steps of the monitoring workflow. Here, we review existing technologies for data recording and processing that enable automated monitoring of ecological communities. We then present novel frameworks that combine such technologies, forming fully automated pipelines to detect, track, classify and count multiple species, and record behavioural and morphological traits, at resolutions which have previously been impossible to achieve. Based on these rapidly developing technologies, we illustrate a solution to one of the greatest challenges in ecology: the ability to rapidly generate high-resolution, multidimensional and standardised data across complex ecologies.

Community structure determines the predictability of population collapse.

Early warning signals (EWS) are phenomenological tools that have been proposed as predictors of the collapse of biological systems. Although a growing body of work has shown the utility of EWS based on either statistics derived from abundance data or shifts in phenotypic traits such as body size, so far this work has largely focused on single species populations. However, to predict reliably the future state of ecological systems, which inherently could consist of multiple species, understanding how reliable such signals are in a community context is critical. Here, reconciling quantitative trait evolution and Lotka-Volterra equations, which allow us to track both abundance and mean traits, we simulate the collapse of populations embedded in mutualistic and multi-trophic predator-prey communities. Using these simulations and warning signals derived from both population- and community-level data, we showed the utility of abundance-based EWS, as well as metrics derived from stability-landscape theory (e.g. width and depth of the basin of attraction), were fundamentally linked. Thus, the depth and width of such stability-landscape curves could be used to identify which species should exhibit the strongest EWS of collapse. The probability a species displays both trait and abundance-based EWS was dependent on its position in a community, with some species able to act as indicator species. In addition, our results also demonstrated that in general trait-based EWS were less reliable in comparison with abundance-based EWS in forecasting species collapses in our simulated communities. Furthermore, community-level abundance-based EWS were fairly reliable in comparison with their species-level counterparts in forecasting species-level collapses. Our study suggests a holistic framework that combines abundance-based EWS and metrics derived from stability-landscape theory that may help in forecasting species loss in a community context.

Landscape configuration affects probability of apex predator presence and community structure in experimental metacommunities.

Biodiversity is declining at an unprecedented rate, highlighting the urgent requirement for well-designed protected areas. Design tactics previously proposed to promote biodiversity include enhancing the number, connectivity, and heterogeneity of reserve patches. However, how the importance of these features changes depending on what the conservation objective is remains poorly understood. Here we use experimental landscapes containing ciliate protozoa to investigate how the number and heterogeneity in size of habitat patches, rates of dispersal between neighbouring patches, and mortality risk of dispersal across the non-habitat 'matrix' interact to affect a number of diversity measures. We show that increasing the number of patches significantly increases γ diversity and reduces the overall number of extinctions, whilst landscapes with heterogeneous patch sizes have significantly higher γ diversity than those with homogeneous patch sizes. Furthermore, the responses of predators depended on their feeding specialism, with generalist predator presence being highest in a single large patch, whilst specialist predator presence was highest in several-small patches with matrix dispersal. Our evidence emphasises the importance of considering multiple diversity measures to disentangle community responses to patch configuration.

Machine learning methods trained on simple models can predict critical transitions in complex natural systems.

Forecasting sudden changes in complex systems is a critical but challenging task, with previously developed methods varying widely in their reliability. Here we develop a novel detection method, using simple theoretical models to train a deep neural network to detect critical transitions-the Early Warning Signal Network (EWSNet). We then demonstrate that this network, trained on simulated data, can reliably predict observed real-world transitions in systems ranging from rapid climatic change to the collapse of ecological populations. Importantly, our model appears to capture latent properties in time series missed by previous warning signals approaches, allowing us to not only detect if a transition is approaching, but critically whether the collapse will be catastrophic or non-catastrophic. These novel properties mean EWSNet has the potential to serve as an indicator of transitions across a broad spectrum of complex systems, without requiring information on the structure of the system being monitored. Our work highlights the practicality of deep learning for addressing further questions pertaining to ecosystem collapse and has much broader management implications.

Global patterns of resilience decline in vertebrate populations.

Maintaining the resilience of natural populations, their ability to resist and recover from disturbance, is crucial to prevent biodiversity loss. However, the lack of appropriate data and quantitative tools has hampered our understanding of the factors determining resilience on a global scale. Here, we quantified the temporal trends of two key components of resilience-resistance and recovery-in >2000 population time-series of >1000 vertebrate species globally. We show that the number of threats to which a population is exposed is the main driver of resilience decline in vertebrate populations. Such declines are driven by a non-uniform loss of different components of resilience (i.e. resistance and recovery). Increased anthropogenic threats accelerating resilience loss through a decline in the recovery ability-but not resistance-of vertebrate populations. These findings suggest we may be underestimating the impacts of global change, highlighting the need to account for the multiple components of resilience in global biodiversity assessments.

Early warning signal reliability varies with COVID-19 waves.

Early warning signals (EWSs) aim to predict changes in complex systems from phenomenological signals in time series data. These signals have recently been shown to precede the emergence of disease outbreaks, offering hope that policymakers can make predictive rather than reactive management decisions. Here, using a novel, sequential analysis in combination with daily COVID-19 case data across 24 countries, we suggest that composite EWSs consisting of variance, autocorrelation and skewness can predict nonlinear case increases, but that the predictive ability of these tools varies between waves based upon the degree of critical slowing down present. Our work suggests that in highly monitored disease time series such as COVID-19, EWSs offer the opportunity for policymakers to improve the accuracy of urgent intervention decisions but best characterize hypothesized critical transitions.

Scaling the extinction vortex: Body size as a predictor of population dynamics close to extinction events.

Mutual reinforcement between abiotic and biotic factors can drive small populations into a catastrophic downward spiral to extinction-a process known as the "extinction vortex." However, empirical studies investigating extinction dynamics in relation to species' traits have been lacking.We assembled a database of 35 vertebrate populations monitored to extirpation over a period of at least ten years, represented by 32 different species, including 25 birds, five mammals, and two reptiles. We supplemented these population time series with species-specific mean adult body size to investigate whether this key intrinsic trait affects the dynamics of populations declining toward extinction.We performed three analyses to quantify the effects of adult body size on three characteristics of population dynamics: time to extinction, population growth rate, and residual variability in population growth rate.Our results provide support for the existence of extinction vortex dynamics in extirpated populations. We show that populations typically decline nonlinearly to extinction, while both the rate of population decline and variability in population growth rate increase as extinction is approached. Our results also suggest that smaller-bodied species are particularly prone to the extinction vortex, with larger increases in rates of population decline and population growth rate variability when compared to larger-bodied species.Our results reaffirm and extend our understanding of extinction dynamics in real-life extirpated populations. In particular, we suggest that smaller-bodied species may be at greater risk of rapid collapse to extinction than larger-bodied species, and thus, management of smaller-bodied species should focus on maintaining higher population abundances as a priority.

Corridor quality affects net movement, size of dispersers, and population growth in experimental microcosms.

Corridors are expected to increase species dispersal in fragmented habitats. However, it remains unclear how the quality of corridors influences the dispersal process, and how it interacts with corridor length and width. Here we investigate these factors using a small-scale laboratory system where we track the dispersal of the model organism Collembola Folsomia candida. Using this system, we study the effects of corridor length, width, and quality on the probability of dispersal, net movement, body size of dispersers, and the rate of change in population size after colonization. We show that corridor quality positively affected dispersal probability, net movement, and the rate of change in population size in colonised patches. Moreover, corridor quality significantly affected the size of dispersers, with only larger individuals dispersing through poor quality corridors. The length and width of corridors affected both the rate at which populations increased in colonised patches and the net number of individuals which dispersed, suggesting that these physical properties may be important in maintaining the flow of individuals in space. Our results thus suggest that corridor quality can have an important role in determining not only the probability of dispersal occurs but also the phenotypes of the individuals which disperse, with concomitant effects on the net movement of individuals and the rate of change in population size in the colonised patches.

Imperfect detection alters the outcome of management strategies for protected areas.

Designing protected area configurations to maximise biodiversity is a critical conservation goal. The configuration of protected areas can significantly impact the richness and identity of the species found there; one large patch supports larger populations but can facilitate competitive exclusion. Conversely, many small habitats spreads risk but may exclude predators that typically require large home ranges. Identifying how best to design protected areas is further complicated by monitoring programs failing to detect species. Here we test the consequences of different protected area configurations using multi-trophic level experimental microcosms. We demonstrate that for a given total size, many small patches generate higher species richness, are more likely to contain predators, and have fewer extinctions compared to single large patches. However, the relationship between the size, number of patches, and species richness was greatly affected by insufficient monitoring, and could lead to incorrect conservation decisions, especially for higher trophic levels.

Eco-evolutionary processes underlying early warning signals of population declines.

Environmental change can impact the stability of ecological systems and cause rapid declines in populations. Abundance-based early warning signals have been shown to precede such declines, but detection prior to wild population collapses has had limited success, leading to the development of warning signals based on shifts in distribution of fitness-related traits such as body size. The dynamics of population abundances and traits in response to external environmental perturbations are controlled by a range of underlying factors such as reproductive rate, genetic variation and plasticity. However, it remains unknown how such ecological and evolutionary factors affect the stability landscape of populations and the detectability of abundance and trait-based early warning signals. Here, we apply a trait-based demographic approach and investigate both trait and population dynamics in response to gradual and increasing changes in the environment. We explore a range of ecological and evolutionary constraints under which stability of a population may be affected. We show both analytically and with simulations that strength of abundance- and trait-based warning signals are affected by ecological and evolutionary factors. Finally, we show that combining trait- and abundance-based information improves our ability to predict population declines. Our study suggests that the inclusion of trait dynamic information alongside generic warning signals should provide more accurate forecasts of the future state of biological systems.

Early warning signals of recovery in complex systems.

Early warning signals (EWSs) offer the hope that patterns observed in data can predict the future states of ecological systems. While a large body of research identifies such signals prior to the collapse of populations, the prediction that such signals should also be present before a system's recovery has thus far been overlooked. We assess whether EWSs are present prior to the recovery of overexploited marine systems using a trait-based ecological model and analysis of real-world fisheries data. We show that both abundance and trait-based signals are independently detectable prior to the recovery of stocks, but that combining these two signals provides the best predictions of recovery. This work suggests that the efficacy of conservation interventions aimed at restoring systems which have collapsed may be predicted prior to the recovery of the system, with direct relevance for conservation planning and policy.

When Do Shifts in Trait Dynamics Precede Population Declines?

Predicting population responses to environmental change is an ongoing challenge in ecology. Studies investigating the links between fitness-related phenotypic traits and demography have shown that trait dynamic responses to environmental change can sometimes precede population dynamic responses and thus can be used as an early warning signal. However, it is still unknown under which ecological and evolutionary circumstances shifts in fitness-related traits can precede population responses to environmental perturbation. Here, we take a trait-based demographic approach and investigate both trait and population dynamics in a density-regulated population in response to a gradual change in the environment. We explore the ecological and evolutionary constraints under which shifts in fitness-related traits precede a decline in population size. We show both analytically and with experimental data that under medium to slow rates of environmental change, shifts in a trait value can precede population decline. We further show the positive influence of environmental predictability, net reproductive rate, plasticity, and genetic variation on shifts in trait dynamics preceding potential population declines. These results still hold under nonconstant genetic variation and environmental stochasticity. Our study highlights ecological and evolutionary circumstances under which a fitness-related trait can be used as an early warning signal of an impending population decline.