Despite the foundational role microorganisms play in sustaining life on Earth, they have been largely overlooked in global conservation agendas, driving the emergence of microbial conservation as a critical discipline. While major assessment reports successfully mobilize support for the conservation of macroscopic biodiversity by documenting its value, threats, and intervention effectiveness, comparable evidence for microbes is lacking. I provide this missing evidence by synthesizing 33,297 effect sizes across three second-order meta-analyses. These analyses (1) identified land-use and land-cover change as well as specific pollutants as the primary threats to microbial diversity, function, and community integrity, (2) demonstrated the essential ecosystem services microbes provide, and (3) revealed the insufficient microbial conservation gain achieved by existing interventions. Building on these insights, I revisit the concept of vulnerability to propose targeted microbial conservation strategies that maintain or restore microbial diversity and function. The evidence presented here underscores the urgency of integrating microbes into nature conservation, thereby protecting the very foundation of life and safeguarding ecosystem integrity and planetary health. ### Competing Interest Statement The authors have declared no competing interest.
Specialized metabolites released in the environment mediate ecological interactions across geographic scales and levels of biological organization. Whereas chemodiversity-the richness, relative abundance and disparity of specialized compounds within a blend of metabolites-has received substantial interest at the level of pairwise interactions, much less is known about how metabolites produced by multiple individuals and species merge into higher-level blends at population, community and ecosystem scales. Here we review evidence for emergent functions that arise from such higher-level chemodiversity: how blends can change in composition and functional consequence as they move through air, water and soil, and vary in time and space, thereby creating a dynamic chemodiversity landscape. We further discuss the applied potential of these chemodiversity landscapes and the threats that could compromise them. We outline key questions that will help to guide research on how higher-level chemodiversity contributes to ecological processes and functioning across scales.
1. Understanding how species interactions, such as those between plants and their pollinators, are structured in human-transformed habitats is a key challenge in modern ecology. However, the relative importance of the drivers structuring interactions may vary depending on the ecological and environmental context. 2. We investigated the influence of three ecological drivers of plant-pollinator interactions in urban landscapes of a tropical metropolis: spatiotemporal overlap (species phenology within and across sites), interaction neutrality (species abundance) and trait matching (compatibility in morphological traits). We collected floral interaction data from different pollinator groups, including bees, butterflies, flies and wasps in distinct urban landscapes. 3. We found that spatiotemporal overlap and neutrality were the primary drivers of interactions, while trait matching had minimal effect, likely reflecting the predominance of generalist species in urban environments and reducing morphological constraints on species interactions. The observed negative correlation between neutrality and trait matching indicates that as the importance of species abundances increases, the influence of trait matching decreases. 4. When examined by pollinator groups, spatiotemporal overlap also emerged as the most important driver for bees and butterflies. However, we detected a seasonal variation where spatiotemporal overlap was relatively more important during the rainy season, while neutrality played a greater role in the dry season. This contrast may arise owed to differences in floral resource availability, which are scarcer during the dry season and when some mass flowering plants attract many of the available pollinators. 5. Synthesis and applications. Our study shows that the generalized structure of urban plant-pollinator interactions is mirrored in the mechanisms that shape them, as interactions are governed primarily by less restrictive drivers such as abundance and spatiotemporal overlap rather than by trait matching. To enhance the diversity of interactions, urban landscapes with a high diversity of plant species that bloom year-round and are attractive to different pollinator groups are needed. By doing so, tropical cities can ensure pollinators across seasons and foster interactions of different pollinator groups.
The number of ovules per flower varies by orders of magnitude among angiosperms: some families show remarkable conservatism, whereas others vary widely even among close relatives. Many hypotheses explaining ovule packaging link this trait to variation in pollen receipt. Here we ask whether pollinator species richness predicts ovule number across angiosperms, as would be expected if pollinator species richness reflects among-flower variance in pollen receipt. We tested this hypothesis using literature-derived data for 191 animal-pollinated plant species across 61 families. We first assessed the association between ovule number and pollinator species richness using ordinary least squares (OLS), and then repeated the analysis using phylogenetic generalized least squares (PGLS) to account for phylogenetic non-independence. Ovule number showed strong phylogenetic constraint, and controlling for phylogeny eliminated the negative OLS association between visitor richness and ovule number. This result may indicate that apparent associations between ovule number and pollinator richness largely reflect shared evolutionary history rather than repeated adaptive responses to pollination environments.
The insurance hypothesis of biodiversity assumes that biodiversity increases ecosystem stability when functionally redundant species exhibit distinct responses to environmental changes, allowing some species to compensate for the loss of others. However, empirical evidence remains scarce. Using a novel approach to quantify the responses of 96 plant species to land use, we tested the hypothesis combining field data with a common garden experiment. By subjecting transplanted grassland plant communities to different land-use intensities, we quantified response diversity (defined as the variability of responses among species to the same environmental factor), species composition, and functionality from spectral data before and after experimental changes. Our results show that land-use intensification reduced response diversity of plant communities in the field and the common garden. Moreover, our results indicate that response diversity increases functional stability but decreases stability in terms of species composition (temporal β-diversity), that is, response-diverse communities tended to lose species with fewer replacements while response-depleted communities mainly experienced species turnover. Our work highlights that response diversity underlies multiple dimensions of ecosystem stability as it stabilizes functionality but destabilizes species composition. We further discuss future research directions to adapt the concept of response diversity under global change scenarios.
ABSTRACT Leaf shape is a fundamental trait of plant ecological strategies, influencing biotic interactions and ecosystem functioning. However, established quantitative metrics fail to capture subtle variations and irregularities, require user-based reference points or are challenging to compare among taxa with broadly different leaf shapes. In addition, established metrics typically conflate (aggregate) leaf edge complexity and macro-shape complexity, despite their independent functional significance and genetic foundations. Here, we introduce an entropy-based framework to quantify two new complexity metrics: edge complexity and macro-shape complexity. Based on three case studies, we show that these metrics outperform aggregate metrics in predicting Quercus robur chemical traits, provide more intuitive interspecific classifications, and strongly align with human perception. In addition, edge and macro-shape complexity show high complementarity, while aggregate metrics are highly redundant and typically strongly related to leaf area. Emerging as the strongest predictor of leaf chemistry and key visual cue for complexity as perceived by humans, the effects of edge complexity highlight the under-appreciated functional significance of leaf margins. Our framework and the proposed entropy-based complexity metrics thus promise to help unlock the potential of growing digital image archives of leaves, including images from herbaria and fossils, and are technically readily applicable to shapes of algae, bacteria, pollen, and beyond. The accompanying package ShapeComplexity enables the broad application of entropy-based metrics, providing a powerful tool to explore how the shape of organisms and biological structures influences ecological strategies, biotic interactions, and ecosystem functioning while tracking spatial and temporal variation.
BACKGROUND:Plants are exposed to various environmental challenges. Especially with ongoing climate change, droughts and insect outbreaks are expected to become more frequent. Plant responses to these challenges are mediated by interacting phytohormonal pathways that influence plant growth, but little is known how these responses to single and combined challenges vary across different scales, within and between species. Thus, we investigated species- and accession-specific responses to two environmental challenges in three perennial plant species and compared the responses between species. Clones of several accessions of the herbaceous species Tanacetum vulgare, the woody vine Solanum dulcamara, and the tree Populus nigra were subjected to similar control, herbivory, drought, and combined (drought and herbivory) treatments. After the exposure, foliar phytohormones and various morphological traits were quantified. RESULTS:Plants of T. vulgare did not respond in jasmonic acid (JA) levels, but showed an increase in abscisic acid (ABA) and a reduced aboveground biomass, particularly under the combined challenges. Plants of S. dulcamara exhibited similar responses, but JA levels were enhanced by all treatments. In contrast, P. nigra uniquely induced salicylic acid under the combined treatment, but showed no impacts on growth. Phenotypic plasticity reflected these species-specific patterns, with none of the phytohormones or morphological traits exhibiting uniform plasticity across species, but with substantial accession-specific pattern. Structural equation models further revealed distinct phytohormone-mediated pathways underlying morphological traits, potentially linking environmental challenges and accessions to specific plant responses within each species. Besides these species-specific differences, several traits responded consistently in all three species to the environmental challenges. Jasmonoyl-isoleucine was induced by herbivory and the combined treatment, ABA by drought and the combined treatment, and indole acetic acid by the combined treatment in all species. Root mass remained unchanged in all species. CONCLUSIONS:Our results indicate that plant responses to similar challenges include both species-specific and conserved components. The combined treatment elicited the strongest responses, suggesting that simultaneous challenges under climate change may have complex effects on plant performance. The intra- and interspecific differences revealed here highlight the need to further explore the mechanisms underlying this specificity and understand patterns of plant resilience.
Abstract Plant-associated microbial communities exhibit pronounced specificity across biological and spatial scales. While the patterns and accompanied functions have been well documented across and within plant species, the functional importance of intra-individual variation remains underexplored. Particularly in trees that experience strong environmental gradients within single crowns, stratum -specific microbiota may significantly contribute to plant performance. We experimentally tested whether variation in microbiota within the crown of Quercus robur is related to host performance. In mesocosm experiments, we transferred microbial communities derived from sun and shade leaves to germ-reduced clonal individuals of the same species and applied UV radiation simulating conditions that matched or mismatched the origin of the microbial inoculum (environmental matching). Our results demonstrate that matching microbiota-environment combinations increased plant performance compared to mismatching combinations. We infer that pronounced intra-individual variation of leaf-associated microbial communities not only reflects environmental heterogeneity along canopy strata but is functionally relevant for the plant host.
Abstract Plant trait spaces have advanced ecology by reducing the vast diversity of plant form and function to a few axes of trait variation. Yet, such frameworks remain dominated by autoecological traits related to resource acquisition and growth, while largely overlooking the traits mediating interactions with other organisms. Chemodiversity, the richness, evenness and chemical disparity of volatile organic compounds (VOCs) emitted by leaves and flowers to attract, deter, or otherwise affect biotic interaction partners, may represent such an overlooked synecological dimension of plant functional variation. By integrating the chemodiversity of floral ( n = 859 species) and vegetative ( n = 159 species) VOC profiles into the global spectrum of plant form and function, we show that chemodiversity is a) independent from the classical axis of variation in plant size and leaf economics but b) is linked to biotic interactions in organ-specific ways. Flower-visitor richness increases with floral scent chemodiversity, a pattern supported by an analysis of global interaction data and a meta-analysis of the specialization and generalization of flower-animal interactions. Vegetative VOC chemodiversity has context-dependent positive and negative effects on herbivore richness. VOC chemodiversity represents a distinct ecological strategy that defines interaction niches, thereby contributing to ecological differentiation and coexistence among otherwise functionally similar species.
Plant interactions with abiotic and biotic environments are mediated by diverse metabolites, which are crucial for stress response and defense. These metabolites can not only support diversity by shaping species niche differences but also display heritable and plastic intraspecific variation, which few studies have quantified in terms of their relative contributions. To address this shortcoming, we used untargeted metabolomics to annotate and quantify foliar metabolites and restriction-site associated DNA (RAD) sequencing to assess genetic distances among 300 individuals of 10 locally abundant species from a diverse tropical community in Southwest China. We quantified the relative contributions of relatedness and the abiotic and biotic environment to intraspecific metabolite variation, considering different biosynthetic pathways. Intraspecific variation contributed most to community-level metabolite diversity, followed by species-level variation. Biotic factors had the largest effect on total and secondary metabolites, while abiotic factors strongly influenced primary metabolites, particularly carbohydrates. The relative importance of these factors varied widely across different biosynthetic pathways and different species. Our findings highlight that intraspecific variation is an essential component of community-level metabolite diversity. Furthermore, species rely on distinct classes of metabolites to adapt to environmental pressures, with genetic, abiotic, and biotic factors playing pathway-specific roles in driving intraspecific variation.
Being uniquely adapted to extreme environmental conditions, rock-dwelling lecideoid lichens are a diverse and major component of terrestrial vegetation in Antarctica. Climate change is reshaping Antarctic ecosystems, forcing cold-adapted species to migrate to maintain their climatic niche. The study surveyed the circum-Antarctic lecideoid lichen diversity and modeled the impacts of two climate change scenarios on their distributional range shifts across Antarctica. Fungal and algal symbionts of lecideoid lichen species from a circum-Antarctic sampling were classified using classical barcoding methods. The climatic niches of nine common fungal (mycobiont) species and four algal (photobiont) OTUs were predicted, and spatial range shifts were projected across four Antarctic bioregions under three Shared Socioeconomic Pathways: (1) SSP1-2.6: sustainable development, (2) SSP3-7.0: medium–high reference scenario with high methane emissions and (3) SSP5-8.5: continued dependence on fossil fuels. DNA-barcoding revealed altogether 34 species of lecideoid lichens associated with 9 photobiont OTUs for the Antarctic continent. In addition to the already known lichen species in Antarctica, three newly detected species of the genus Lecidella could be identified. The calculated climate change scenarios across bioregions predict overall range expansion for mycobiont species and photobiont OTUs. While a reduction in suitable habitat size is expected in maritime Antarctica, species distributions are predicted to expand in continental regions, primarily due to inland shifts. These inland areas may serve as emerging climatic refugia for certain mycobiont species. Overall, these results suggest that, under future warming, lecideoid lichens undergo an overall range expansion, particularly in previously uncolonized inland areas in continental Antarctica.
Many species experience less pressure from herbivores, predators, or pathogens in their introduced range than in their native range. This phenomenon, known as enemy release, is one explanation for the success of introduced plant species worldwide. However, species experience enemy release to different extents, or not at all. Surprisingly, we have little understanding of what types of species or circumstances are associated with strong enemy release. We aimed to test whether ten defensive leaf traits that contribute to plants’ palatability to aboveground herbivores can predict the level of enemy release they experience. Our study expands upon previous work, which found enemy release occurring across 16 plant species studied at 12 sites within their native (5 sites; European) and introduced (7 sites; Australian) ranges. Contrary to all predictions, we found no evidence that enemy release was related to ash content, C:N ratio, hair density, leaf dry matter content, leaf mass per area, cyanogen presence, lipid content, phenolic compounds, oxidative activity, or combined chemical, physical, and total defences. This result demonstrates the need to further assess other traits, or environmental variables that may contribute to enemy release, so that we may more accurately predict when and where it is most likely to occur. Finding that these defensive traits do not predict enemy release in our study system brings us a step closer to understanding the mechanisms underlying successful invasion, which is increasingly important in our rapidly changing world.
Urbanization poses significant threats to pollinators, but they may respond differently to habitat modification according to their nesting and foraging requirements. Despite the diversity of pollinator groups and species found in urban areas, research often focus on bees, neglecting other groups. Whether bee response to urbanization suffice in representing the wider pollinator spectrum, however, is poorly understood. Here, we examined how urbanization impacts the interaction networks between plants and different pollinator groups and evaluated the dissimilarities of urban green spaces at both local and regional scales within a Neotropical metropolis. Recording 1,404 interactions between 262 plant and 220 pollinator species, we found that network specialization varied among pollinator groups but was not affected by urban impervious surface cover. Such lack of difference may happen owing to the prevalence of generalist species across urban environments. Importantly, urban green spaces showed high dissimilarities in species and interactions, emphasizing the heterogeneity found across the urban landscape. Plant composition also varied between urban green spaces and was strongly correlated with interaction dissimilarities, indicating that floral resources contribute to unique interactions found in different areas. Our results suggest that although important, bees alone do not represent the wider response of pollinators to urbanization. Furthermore, the high dissimilarities influenced by site specific plant-pollinator co-occurrence underscore that multiple and connected green spaces are required to safeguard plant-pollinator interaction diversity and its vital ecosystem function in cities.
The phyllosphere bacteria play a crucial role in global greenhouse gas emissions and sequestration, but the spatial interactions between phyllosphere bacterial diversity, host leaf traits and environmental variation remain poorly understood. This gap is mainly due to methodological limitations in linking the spatial pattern of bacterial diversity to leaf traits. Here, we present machine learning models based on visible and near-infrared (VIS-NIR) leaf hyperspectral proximal sensing that are used to independently predict the phyllosphere bacterial alpha-diversity indices and leaf traits under different abiotic conditions for both sides of the leaf. We demonstrate that the models can effectively represent leaf traits and bacterial alpha-diversity indices for different abiotic environmental conditions. The cross-correlation of the spatial patterns as a result of the spatial application of the independent models reveals fine-scale associations between leaf traits and bacterial colonization patterns. Our findings highlight the great potential of hyperspectral proximal sensing for understanding the relationship between leaf bacterial richness and leaf resources within the leaf microecosystem. Ultimately, this will enhance our capacity to quantify the contribution of the leaf bacteria to the greenhouse gas balance of the forest canopy in a changing climate.
Floral scents are complex blends of volatile compounds, yet the influence of floral scent chemodiversity, the richness, evenness, and functional disparity of phytochemical compounds in shaping interactions with flower visitors and microbes remains largely unexplored. Using a dataset of alpine plant species, we investigated how floral scent chemodiversity affects flower visitor and bacterial diversities on flowers. Our results reveal that high floral scent chemodiversity is associated with increased flower visitor richness but reduced bacterial richness on flowers. These findings led us to propose the 'Filthy Pollinator Hypothesis'. Our hypothesis rests on two core ideas: flowers with chemodiverse scents attract a broader range of flower visitors, thereby increasing the potential for microbial transmission; and floral scent chemodiversity acts as a selective filter, mitigating the risks of unwanted microbial colonization by preventing the establishment of detrimental microbes while still allowing the establishment of a healthy microbiome. Floral scent chemodiversity may therefore not only shape the specialization/generalization of flower visitor assemblages but also act as a regulatory mechanism for microbial communities. By highlighting the multifunctionality of chemodiversity in structuring plant-animal and plant-microbe interactions, our study advances the understanding of chemodiversity and underscores its importance in plant ecology.
Land-use changes threaten ecosystems and are a major driver of species loss. Plants may adapt or migrate to resist global change, but this can lag behind rapid anthropogenic changes to the environment. Our data show that natural modulations of the microbiome of grassland plants in response to experimental land-use change in a common garden directly affect plant phenotype and performance, thus increasing plant tolerance. In contrast, direct effects of fertilizer application and mowing on plant phenotypes were less strong. Land-use intensity-specific microbiomes caused clearly distinguishable plant phenotypes also in a laboratory experiment using gnotobiotic strawberry plants in absence of environmental variation. Therefore, natural modulations of the plant microbiome may be key to species persistence and ecosystem stability. We argue that a prerequisite for this microbiome-mediated tolerance is the availability of diverse local sources of microorganisms facilitating rapid modulations in response to change. Thus, conservation efforts must protect microbial diversity, which can help mitigate the effects of global change and facilitate environmental and human health.
Floral traits describe organs or structures directly related to plant reproduction, and they are essential to understanding plant–pollinator interactions, notably for conservation purposes. The growth of plant trait‐based approaches lies in the availability of data shared by the international research community on dedicated platforms, as well as in protocols compiled in handbooks on how to measure these traits in a standardized way. Floral traits are important pieces that are missing from these handbooks, likely due to the complexity of flower morphology. Here, we present a handbook of standardized protocols dedicated to floral traits that can be applied to a wide set of temperate plant species to quantify these traits at the scale of plant communities. The 24 floral traits are grouped into three categories: visual and olfactory cues, accessibility and resources. We also provide four additional features related to flower abundance and phenology that we recommend measuring to scale up individual species' trait values to overall plant communities. By collecting these floral traits in a standardized way, we promote applications in the context of community ecology to predict the diversity of pollinator communities, identify the effects of environmental changes and study plant–pollinator networks.
In alpine landscapes, vascular plants and also bryophytes are key biological features shaping the trajectories of primary succession following glacial retreat. Yet research on ecological successions is mainly centered around vascular plants, and potential interactions between both taxonomic groups have been largely disregarded. In this study, we examine successional processes impacting both groups across a 170-year gradient developing into a natural grassland ecosystem in the Austrian Alps. Utilizing multispectral 3D whole community phenotyping and introducing ecological dispersion as a metric reflecting a community’s ecological, calculated as the dispersion of ecological indicator values, we gain a mechanistic understanding of the interactions between bryophyte and vascular plant diversity along grassland succession. Our findings show an increase in diversity for both groups over time, with vascular plants demonstrating a transitional community composition pattern along the successional gradient. Bryophytes, in contrast, do not show a consistent pattern of community compositional change over succession and are less affected by microclimate and soil nutrients, highlighting opportunistic colonization strategies with bryophyte communities showing increased ecological dispersion over time. Structural equation modeling reveals that vascular plant growth structure, quantified via digital community features from multispectral 3D plant scanning, negatively affects bryophyte diversity and ecological dispersion, suggesting competitive interactions with vascular plants. Our research underlines the complex dynamics between bryophyte and vascular plant communities during alpine grassland succession and stresses the importance of including both groups in succession studies to fully grasp biodiversity development and succession mechanisms. ### Competing Interest Statement The authors have declared no competing interest.
Bacterial and fungal microbiomes associated with plants can significantly affect the host's phenotype. Inoculating plants with one or multiple bacterial and fungal species can affect specific plant traits, which is exploited in attempts to increase plant performance and stress tolerance by microbiome engineering. Currently, we lack a comprehensive synthesis on the generality of these effects related to different biological (e.g. plant models, plant traits, and microbial taxa) and experimental factors. In a meta-analysis, we showed that the plant trait under consideration and the microbial taxa used to inoculate plants significantly influenced the strength of the effect size. In a methodological context, experiments under sterilized conditions and short-term periods resulted in larger positive effects on plant traits than those of unsterilized and long-term experiments. We recommend that future studies should not only consider (short-term) laboratory experiments with sterilized plants and single inoculants but also and more often (long-term) field or greenhouse experiments with naturally occurring microbial communities associated with the plants and inoculated consortia including both bacteria and fungi.