Uncovering Broad Macroecological Patterns by Comparing the Shape of Species' Distributions along Environmental Gradients.

AbstractSpecies' distributions can take many different forms. For example, fat-tailed or skewed distributions are very common in nature, as these can naturally emerge as a result of individual variability and asymmetric environmental tolerances, respectively. Studying the basic shape of distributions can teach us a lot about the ways climatic processes and historical contingencies shape ecological communities. Yet we still lack a general understanding of how their shapes and properties compare to each other along gradients. Here, we use Bayesian nonlinear models to quantify range shape properties in empirical plant distributions. With this approach, we are able to distil the shape of plant distributions and compare them along gradients and across species. Studying the relationship between distribution properties, we revealed the existence of broad macroecological patterns along environmental gradients-such as those expected from Rapoport's rule and the abiotic stress limitation hypothesis. We also find that some aspects of the shape of observed ranges-such as kurtosis and skewness of the distributions-could be intrinsic properties of species or the result of their historical contexts. Overall, our modeling approach and results untangle the general shape of plant distributions and provide a mapping of how this changes along environmental gradients.

Deep learning to extract the meteorological by-catch of wildlife cameras.

Microclimate-proximal climatic variation at scales of metres and minutes-can exacerbate or mitigate the impacts of climate change on biodiversity. However, most microclimate studies are temperature centric, and do not consider meteorological factors such as sunshine, hail and snow. Meanwhile, remote cameras have become a primary tool to monitor wild plants and animals, even at micro-scales, and deep learning tools rapidly convert images into ecological data. However, deep learning applications for wildlife imagery have focused exclusively on living subjects. Here, we identify an overlooked opportunity to extract latent, ecologically relevant meteorological information. We produce an annotated image dataset of micrometeorological conditions across 49 wildlife cameras in South Africa's Maloti-Drakensberg and the Swiss Alps. We train ensemble deep learning models to classify conditions as overcast, sunshine, hail or snow. We achieve 91.7% accuracy on test cameras not seen during training. Furthermore, we show how effective accuracy is raised to 96% by disregarding 14.1% of classifications where ensemble member models did not reach a consensus. For two-class weather classification (overcast vs. sunshine) in a novel location in Svalbard, Norway, we achieve 79.3% accuracy (93.9% consensus accuracy), outperforming a benchmark model from the computer vision literature (75.5% accuracy). Our model rapidly classifies sunshine, snow and hail in almost 2 million unlabelled images. Resulting micrometeorological data illustrated common seasonal patterns of summer hailstorms and autumn snowfalls across mountains in the northern and southern hemispheres. However, daily patterns of sunshine and shade diverged between sites, impacting daily temperature cycles. Crucially, we leverage micrometeorological data to demonstrate that (1) experimental warming using open-top chambers shortens early snow events in autumn, and (2) image-derived sunshine marginally outperforms sensor-derived temperature when predicting bumblebee foraging. These methods generate novel micrometeorological variables in synchrony with biological recordings, enabling new insights from an increasingly global network of wildlife cameras.

Compensatory responses of vital rates attenuate impacts of competition on population growth and promote coexistence.

Competition is among the most important factors regulating plant population and community dynamics, but we know little about how different vital rates respond to competition and jointly determine population growth and species coexistence. We conducted a field experiment and parameterised integral projection models to model the population growth of 14 herbaceous plant species in the absence and presence of neighbours across an elevation gradient (284 interspecific pairs). We found that suppressed individual growth and seedling establishment contributed the most to competition-induced declines in population growth, although vital rate contributions varied greatly between species and with elevation. In contrast, size-specific survival and flowering probability and seed production were frequently enhanced under competition. These compensatory vital rate responses were nearly ubiquitous (occurred in 92% of species pairs) and significantly reduced niche overlap and stabilised coexistence. Our study highlights the importance of demographic processes for regulating population and community dynamics, which has often been neglected by classic coexistence theories.

Ecological lags govern the pace and outcome of plant community responses to 21st-century climate change.

Forecasting the trajectories of species assemblages in response to ongoing climate change requires quantifying the time lags in the demographic and ecological processes through which climate impacts species' abundances. Since experimental climate manipulations are typically abrupt, the observed species responses may not match their responses to gradual climate change. We addressed this problem by transplanting alpine grassland turfs to lower elevations, recording species' demographic responses to climate and competition, and using these data to parameterise community dynamics models forced by scenarios of gradual climate change. We found that shifts in community structure following an abrupt climate manipulation were not simply accelerated versions of shifts expected under gradual warming, as the former missed the transient rise of species benefiting from moderate warming. Time lags in demography and species interactions controlled the pace and trajectory of changing species' abundances under simulated 21st-century climate change, and thereby prevented immediate diversity loss.

Global maps of soil temperature.

Research in global change ecology relies heavily on global climatic grids derived from estimates of air temperature in open areas at around 2 m above the ground. These climatic grids do not reflect conditions below vegetation canopies and near the ground surface, where critical ecosystem functions occur and most terrestrial species reside. Here, we provide global maps of soil temperature and bioclimatic variables at a 1-km2 resolution for 0-5 and 5-15 cm soil depth. These maps were created by calculating the difference (i.e. offset) between in situ soil temperature measurements, based on time series from over 1200 1-km2 pixels (summarized from 8519 unique temperature sensors) across all the world's major terrestrial biomes, and coarse-grained air temperature estimates from ERA5-Land (an atmospheric reanalysis by the European Centre for Medium-Range Weather Forecasts). We show that mean annual soil temperature differs markedly from the corresponding gridded air temperature, by up to 10°C (mean = 3.0 ± 2.1°C), with substantial variation across biomes and seasons. Over the year, soils in cold and/or dry biomes are substantially warmer (+3.6 ± 2.3°C) than gridded air temperature, whereas soils in warm and humid environments are on average slightly cooler (-0.7 ± 2.3°C). The observed substantial and biome-specific offsets emphasize that the projected impacts of climate and climate change on near-surface biodiversity and ecosystem functioning are inaccurately assessed when air rather than soil temperature is used, especially in cold environments. The global soil-related bioclimatic variables provided here are an important step forward for any application in ecology and related disciplines. Nevertheless, we highlight the need to fill remaining geographic gaps by collecting more in situ measurements of microclimate conditions to further enhance the spatiotemporal resolution of global soil temperature products for ecological applications.

Moths complement bumblebee pollination of red clover: a case for day-and-night insect surveillance.

Recent decades have seen a surge in awareness about insect pollinator declines. Social bees receive the most attention, but most flower-visiting species are lesser known, non-bee insects. Nocturnal flower visitors, e.g. moths, are especially difficult to observe and largely ignored in pollination studies. Clearly, achieving balanced monitoring of all pollinator taxa represents a major scientific challenge. Here, we use time-lapse cameras for season-wide, day-and-night pollinator surveillance of Trifolium pratense (L.; red clover) in an alpine grassland. We reveal the first evidence to suggest that moths, mainly Noctua pronuba (L.; large yellow underwing), pollinate this important wildflower and forage crop, providing 34% of visits (bumblebees: 61%). This is a remarkable finding; moths have received no recognition throughout a century of T. pratense pollinator research. We conclude that despite a non-negligible frequency and duration of nocturnal flower visits, nocturnal pollinators of T. pratense have been systematically overlooked. We further show how the relationship between visitation and seed set may only become clear after accounting for moth visits. As such, population trends in moths, as well as bees, could profoundly affect T. pratense seed yield. Ultimately, camera surveillance gives fair representation to non-bee pollinators and lays a foundation for automated monitoring of species interactions in future.

Earlier phenology of a nonnative plant increases impacts on native competitors.

Adaptation to climate is expected to increase the performance of invasive species and their community-level impacts. However, while the fitness gains from adaptation should, in general, promote invader competitive ability, empirical demonstrations of this prediction are scarce. Furthermore, climate adaptation, in the form of altered timing of life cycle transitions, should affect the phenological overlap between nonnative and native competitors, with potentially large, but poorly tested, impacts on native species persistence. We evaluated these predictions by growing native California grassland plants in competition with nonnative Lactuca serriola, a species that flowers earlier in parts of its nonnative range that are drier than its putative European source region. In common garden experiments in southern California with L. serriola populations differing in phenology, plants originating from arid climates bolted up to 48 d earlier than plants from more mesic climates, and selection favored early flowering, supporting an adaptive basis for the phenology cline. The per capita competitive effects of L. serriola from early flowering populations on five early flowering native species were greater than the effects of L. serriola from later flowering populations. Consequently, the ability of the native species to increase when rare in competition with L. serriola, as inferred from field-parameterized competition models, declined with earlier L. serriola phenology. Indeed, changes to L. serriola phenology affected whether or not one native species was predicted to persist in competition with L. serriola Our results suggest that evolution in response to new climatic conditions can have important consequences for species interactions, and enhance the impacts of biological invasions on natural communities.

Drivers of local extinction risk in alpine plants under warming climate.

The scarcity of local plant extinctions following recent climate change has been explained by demographic inertia and lags in the displacement of resident species by novel species, generating an 'extinction debt'. We established a transplant experiment to disentangle the contribution of these processes to the local extinction risk of four alpine plants in the Swiss Alps. Projected population growth (λ) derived from integral projection models was reduced by 0.07/°C of warming on average, whereas novel species additionally decreased λ by 0.15 across warming levels. Effects of novel species on predicted extinction time were greatest at warming < 2 °C for two species. Projected population declines under both warming and with novel species were primarily driven by increased mortality. Our results suggest that extinction debt can be explained by a combination of demographic inertia and lags in novel species establishment, with the latter being particularly important for some species under low levels of warming.

Novel competitors shape species' responses to climate change.

Understanding how species respond to climate change is critical for forecasting the future dynamics and distribution of pests, diseases and biological diversity. Although ecologists have long acknowledged species' direct physiological and demographic responses to climate, more recent work suggests that these direct responses can be overwhelmed by indirect effects mediated via other interacting community members. Theory suggests that some of the most dramatic impacts of community change will probably arise through the assembly of novel species combinations after asynchronous migrations with climate. Empirical tests of this prediction are rare, as existing work focuses on the effects of changing interactions between competitors that co-occur today. To explore how species' responses to climate warming depend on how their competitors migrate to track climate, we transplanted alpine plant species and intact plant communities along a climate gradient in the Swiss Alps. Here we show that when alpine plants were transplanted to warmer climates to simulate a migration failure, their performance was strongly reduced by novel competitors that could migrate upwards from lower elevation; these effects generally exceeded the impact of warming on competition with current competitors. In contrast, when we grew the focal plants under their current climate to simulate climate tracking, a shift in the competitive environment to novel high-elevation competitors had little to no effect. This asymmetry in the importance of changing competitor identity at the leading versus trailing range edges is best explained by the degree of functional similarity between current and novel competitors. We conclude that accounting for novel competitive interactions may be essential to predict species' responses to climate change accurately.

Lags in the response of mountain plant communities to climate change.

Rapid climatic changes and increasing human influence at high elevations around the world will have profound impacts on mountain biodiversity. However, forecasts from statistical models (e.g. species distribution models) rarely consider that plant community changes could substantially lag behind climatic changes, hindering our ability to make temporally realistic projections for the coming century. Indeed, the magnitudes of lags, and the relative importance of the different factors giving rise to them, remain poorly understood. We review evidence for three types of lag: "dispersal lags" affecting plant species' spread along elevational gradients, "establishment lags" following their arrival in recipient communities, and "extinction lags" of resident species. Variation in lags is explained by variation among species in physiological and demographic responses, by effects of altered biotic interactions, and by aspects of the physical environment. Of these, altered biotic interactions could contribute substantially to establishment and extinction lags, yet impacts of biotic interactions on range dynamics are poorly understood. We develop a mechanistic community model to illustrate how species turnover in future communities might lag behind simple expectations based on species' range shifts with unlimited dispersal. The model shows a combined contribution of altered biotic interactions and dispersal lags to plant community turnover along an elevational gradient following climate warming. Our review and simulation support the view that accounting for disequilibrium range dynamics will be essential for realistic forecasts of patterns of biodiversity under climate change, with implications for the conservation of mountain species and the ecosystem functions they provide.

Trait differentiation and adaptation of plants along elevation gradients.

Studies of genetic adaptation in plant populations along elevation gradients in mountains have a long history, but there has until now been neither a synthesis of how frequently plant populations exhibit adaptation to elevation nor an evaluation of how consistent underlying trait differences across species are. We reviewed studies of adaptation along elevation gradients (i) from a meta-analysis of phenotypic differentiation of three traits (height, biomass and phenology) from plants growing in 70 common garden experiments; (ii) by testing elevation adaptation using three fitness proxies (survival, reproductive output and biomass) from 14 reciprocal transplant experiments; (iii) by qualitatively assessing information at the molecular level, from 10 genomewide surveys and candidate gene approaches. We found that plants originating from high elevations were generally shorter and produced less biomass, but phenology did not vary consistently. We found significant evidence for elevation adaptation in terms of survival and biomass, but not for reproductive output. Variation in phenotypic and fitness responses to elevation across species was not related to life history traits or to environmental conditions. Molecular studies, which have focussed mainly on loci related to plant physiology and phenology, also provide evidence for adaptation along elevation gradients. Together, these studies indicate that genetically based trait differentiation and adaptation to elevation are widespread in plants. We conclude that a better understanding of the mechanisms underlying adaptation, not only to elevation but also to environmental change, will require more studies combining the ecological and molecular approaches.

Evolutionary responses to global change: lessons from invasive species.

Biologists have recently devoted increasing attention to the role of rapid evolution in species' responses to environmental change. However, it is still unclear what evolutionary responses should be expected, at what rates, and whether evolution will save populations at risk of extinction. The potential of biological invasions to provide useful insights has barely been realised, despite the close analogies to species responding to global change, particularly climate change; in both cases, populations encounter novel climatic and biotic selection pressures, with expected evolutionary responses occurring over similar timescales. However, the analogy is not perfect, and invasive species are perhaps best used as an upper bound on expected change. In this article, we review what invasive species can and cannot teach us about likely evolutionary responses to global change and the constraints on those responses. We also discuss the limitations of invasive species as a model and outline directions for future research.

Plant movements and climate warming: intraspecific variation in growth responses to nonlocal soils.

Most range shift predictions focus on the dispersal phase of the colonization process. Because moving populations experience increasingly dissimilar nonclimatic environmental conditions as they track climate warming, it is also critical to test how individuals originating from contrasting thermal environments can establish in nonlocal sites. We assess the intraspecific variation in growth responses to nonlocal soils by planting a widespread grass of deciduous forests (Milium effusum) into an experimental common garden using combinations of seeds and soil sampled in 22 sites across its distributional range, and reflecting movement scenarios of up to 1600 km. Furthermore, to determine temperature and forest-structural effects, the plants and soils were experimentally warmed and shaded. We found significantly positive effects of the difference between the temperature of the sites of seed and soil collection on growth and seedling emergence rates. Migrant plants might thus encounter increasingly favourable soil conditions while tracking the isotherms towards currently 'colder' soils. These effects persisted under experimental warming. Rising temperatures and light availability generally enhanced plant performance. Our results suggest that abiotic and biotic soil characteristics can shape climate change-driven plant movements by affecting growth of nonlocal migrants, a mechanism which should be integrated into predictions of future range shifts.

Assembly of nonnative floras along elevational gradients explained by directional ecological filtering.

Nonnative species richness typically declines along environmental gradients such as elevation. It is usually assumed that this is because few invaders possess the necessary adaptations to succeed under extreme environmental conditions. Here, we show that nonnative plants reaching high elevations around the world are not highly specialized stress tolerators but species with broad climatic tolerances capable of growing across a wide elevational range. These results contrast with patterns for native species, and they can be explained by the unidirectional expansion of nonnative species from anthropogenic sources at low elevations and the progressive dropping out of species with narrow elevational amplitudes--a process that we call directional ecological filtering. Independent data confirm that climatic generalists have succeeded in colonizing the more extreme environments at higher elevations. These results suggest that invasion resistance is not conferred by extreme conditions at a particular site but determined by pathways of introduction of nonnative species. In the future, increased direct introduction of nonnative species with specialized ecophysiological adaptations to mountain environments could increase the risk of invasion. As well as providing a general explanation for gradients of nonnative species richness and the importance of traits such as phenotypic plasticity for many invasive species, the concept of directional ecological filtering is useful for understanding the initial assembly of some native floras at high elevations and latitudes.

Potential sources of time lags in calibrating species distribution models.

The Anthropocene is characterized by a rapid pace of environmental change and is causing a multitude of biotic responses, including those that affect the spatial distribution of species. Lagged responses are frequent and species distributions and assemblages are consequently pushed into a disequilibrium state. How the characteristics of environmental change-for example, gradual 'press' disturbances such as rising temperatures due to climate change versus infrequent 'pulse' disturbances such as extreme events-affect the magnitude of responses and the relaxation times of biota has been insufficiently explored. It is also not well understood how widely used approaches to assess or project the responses of species to changing environmental conditions can deal with time lags. It, therefore, remains unclear to what extent time lags in species distributions are accounted for in biodiversity assessments, scenarios and models; this has ramifications for policymaking and conservation science alike. This perspective piece reflects on lagged species responses to environmental change and discusses the potential consequences for species distribution models (SDMs), the tools of choice in biodiversity modelling. We suggest ways to better account for time lags in calibrating these models and to reduce their leverage effects in projections for improved biodiversity science and policy.

When and how can we predict adaptive responses to climate change?

Predicting if, when, and how populations can adapt to climate change constitutes one of the greatest challenges in science today. Here, we build from contributions to the special issue on evolutionary adaptation to climate change, a survey of its authors, and recent literature to explore the limits and opportunities for predicting adaptive responses to climate change. We outline what might be predictable now, in the future, and perhaps never even with our best efforts. More accurate predictions are expected for traits characterized by a well-understood mapping between genotypes and phenotypes and traits experiencing strong, direct selection due to climate change. A meta-analysis revealed an overall moderate trait heritability and evolvability in studies performed under future climate conditions but indicated no significant change between current and future climate conditions, suggesting neither more nor less genetic variation for adapting to future climates. Predicting population persistence and evolutionary rescue remains uncertain, especially for the many species without sufficient ecological data. Still, when polled, authors contributing to this special issue were relatively optimistic about our ability to predict future evolutionary responses to climate change. Predictions will improve as we expand efforts to understand diverse organisms, their ecology, and their adaptive potential. Advancements in functional genomic resources, especially their extension to non-model species and the union of evolutionary experiments and "omics," should also enhance predictions. Although predicting evolutionary responses to climate change remains challenging, even small advances will reduce the substantial uncertainties surrounding future evolutionary responses to climate change.

Evolution under changing climates: climatic niche stasis despite rapid evolution in a non-native plant.

A topic of great current interest is the capacity of populations to adapt genetically to rapidly changing climates, for example by evolving the timing of life-history events, but this is challenging to address experimentally. I use a plant invasion as a model system to tackle this question by combining molecular markers, a common garden experiment and climatic niche modelling. This approach reveals that non-native Lactuca serriola originates primarily from Europe, a climatic subset of its native range, with low rates of admixture from Asia. It has rapidly refilled its climatic niche in the new range, associated with the evolution of flowering phenology to produce clines along climate gradients that mirror those across the native range. Consequently, some non-native plants have evolved development times and grow under climates more extreme than those found in Europe, but not among populations from the native range as a whole. This suggests that many plant populations can adapt rapidly to changed climatic conditions that are already within the climatic niche space occupied by the species elsewhere in its range, but that evolution to conditions outside of this range is more difficult. These findings can also help to explain the prevalence of niche conservatism among non-native species.

Rapid upwards spread of non-native plants in mountains across continents.

High-elevation ecosystems are among the few ecosystems worldwide that are not yet heavily invaded by non-native plants. This is expected to change as species expand their range limits upwards to fill their climatic niches and respond to ongoing anthropogenic disturbances. Yet, whether and how quickly these changes are happening has only been assessed in a few isolated cases. Starting in 2007, we conducted repeated surveys of non-native plant distributions along mountain roads in 11 regions from 5 continents. We show that over a 5- to 10-year period, the number of non-native species increased on average by approximately 16% per decade across regions. The direction and magnitude of upper range limit shifts depended on elevation across all regions. Supported by a null-model approach accounting for range changes expected by chance alone, we found greater than expected upward shifts at lower/mid elevations in at least seven regions. After accounting for elevation dependence, significant average upward shifts were detected in a further three regions (revealing evidence for upward shifts in 10 of 11 regions). Together, our results show that mountain environments are becoming increasingly exposed to biological invasions, emphasizing the need to monitor and prevent potential biosecurity issues emerging in high-elevation ecosystems.

Leaf metabolic traits reveal hidden dimensions of plant form and function.

The metabolome is the biochemical basis of plant form and function, but we know little about its macroecological variation across the plant kingdom. Here, we used the plant functional trait concept to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five metabolic functional traits reveals that plants vary on two major axes of leaf metabolic specialization-a leaf chemical defense spectrum and an expression of leaf longevity. Axes are similar for tropical and temperate species, with many trait combinations being viable. However, metabolic traits vary orthogonally to life-history strategies described by widely used functional traits. The metabolome thus expands the functional trait concept by providing additional axes of metabolic specialization for examining plant form and function.

Genetically based differentiation in growth of multiple non-native plant species along a steep environmental gradient.

A non-native plant species spreading along an environmental gradient may need to adjust its growth to the prevailing conditions that it encounters by a combination of phenotypic plasticity and genetic adaptation. There have been several studies of how non-native species respond to changing environmental conditions along latitudinal gradients, but much less is known about elevational gradients. We conducted a climate chamber experiment to investigate plastic and genetically based growth responses of 13 herbaceous non-native plants along an elevational gradient from 100 to 2,000 m a.s.l. in Tenerife. Conditions in the field ranged from high anthropogenic disturbance but generally favourable temperatures for plant growth in the lower half of the gradient, to low disturbance but much cooler conditions in the upper half. We collected seed from low, mid and high elevations and grew them in climate chambers under the characteristic temperatures at these three elevations. Growth of all species was reduced under lower temperatures along both halves of the gradient. We found consistent genetically based differences in growth over the upper elevational gradient, with plants from high-elevation sites growing more slowly than those from mid-elevation ones, while the pattern in the lower part of the gradient was more mixed. Our data suggest that many non-native plants might respond to climate along elevational gradients by genetically based changes in key traits, especially at higher elevations where low temperatures probably impose a stronger selection pressure. At lower elevations, where anthropogenic influences are greater, higher gene flow and frequent disturbance might favour genotypes with broad ecological amplitudes. Thus the importance of evolutionary processes for invasion success is likely to be context-dependent.