The tropical dry forest is a tropical biome characterized by prolonged dry seasons, and harbors an exceptionally rich floristic biodiversity. Yet it is among the most threatened biomes and its belowground diversity remains poorly documented. Here, we analyzed the soil environmental DNA with metabarcoding to quantify the belowground diversity and composition of 11 tropical dry forest sites across four biogeographic regions in Colombia, and we provide a comparative analysis of the biogeographic drivers of soil biodiversity, including soil properties, climate, and spatial factors. We found that the soil microbial communities of tropical dry forests had high proportions of taxa associated with dry conditions, such as Actinomycetota, Glomeromycetes, and Amoebozoa, compared to other tropical forests. Soil mesofauna consisted mainly of ants, termites, and earthworms, with few enchytraeids. The soil microbial alpha and beta diversity were primarily driven by soil physicochemical and climatic drivers, bacteria being more sensitive to aridity than fungi. Macroorganisms exhibited patterns of diversity that were less well explained by the tested predictors. Rather, most of their variation was associated with the sampled region, reflecting a marked biogeographic structure and suggesting that macroorganisms are more prone to isolation-by-distance than microorganisms. Overall, the prevalence of drought-associated microbial taxa and the specific composition of soil mesofauna indicate that tropical dry forests harbour a distinctive belowground biota. These findings provide an important baseline for understanding soil biodiversity in tropical dry forests and support conservation and restoration efforts at the biome scale.
Exploring the biodiversity hidden in tropical rainforests canopies represents a major frontier in biodiversity research yet remains challenging. Environmental DNA (eDNA) can revolutionize this field as it did already in various ecosystems. Here, we test the hypothesis that eDNA contained in canopy throughfall could be used to monitor this elusive diversity and detect anthropogenic disturbance. Using custom-made, low-cost rain collectors, we sampled rainwash eDNA in a mature Amazonian forest and a nearby tree plantation. We successfully detected eDNA from tropical woody and epiphyte plants, vertebrates (mammals, birds, and amphibians), and insects (e.g., mosquitoes, ants, and beetles). The taxonomic composition and diversity reflected disturbance, with significantly lower diversity in the plantation. Crucially, rainwash eDNA integrated biodiversity over a 10-day period in passive collectors and provided a local signature. This approach has thus potential for establishing a cost-effective monitoring system for tropical moist forest canopies, applicable in impact assessments and sustainable management.
Tropical rainforests are vital for global biogeochemical cycles and human well-being and shelter a tremendous, unique, yet underexplored reservoir of biodiversity. With the increasing pressures they face, including deforestation, biological invasions, and climate change, improving methods to monitor their biodiversity is now a pressing societal demand. In recent years, the amplification and sequencing of taxonomically-informative DNA fragments from environmental samples (i.e. eDNA) has revolutionised biomonitoring. Soil, invertebrates bulk, marine and freshwater, or even air, are commonly sampled environmental matrices for such purposes, but present several caveats for the sampling of terrestrial aboveground biodiversity. Here, we explore the potential of DNA contained in rainwash water collected below the forest canopy. We show that it contains not only DNA from invertebrates, but also from the many plants and vertebrates that thrive in the forest canopy. By sampling rainwash eDNA in two 1ha-plots from a tree plantation, and an old-growth Amazonian forest, we detected 170 plant taxa, mainly trees, 72 vertebrate taxa mainly consisting of mammals, birds, and amphibians, and 313 insect taxa including mosquitoes, ants, beetles, etc. The taxonomic composition retrieved in these two plots reflected their different disturbance status. Rainwash eDNA can be efficiently collected passively and persists over ten days while providing a local picture of the diversity. These criteria are compatible with field and environmental management constraints, making the approach promising for an efficient, cost-effective large-scale biomonitoring of tropical rainforest, and more generally all forest canopies. ### Competing Interest Statement The authors have declared no competing interest.
Diatoms constitute one of the most diverse and ecologically important phytoplankton groups, yet their large-scale diversity patterns and drivers of abundance are unclear due to limited observations. Here, we utilize Tara Oceans molecular and morphological data, spanning pole to pole, to describe marine diatom diversity, abundance, and environmental adaptation and acclimation strategies. The dominance of diatoms among phytoplankton in terms of relative abundance and diversity is confirmed, and the most prevalent genera are Chaetoceros, Thalassiosira, Actinocyclus and Pseudo-nitzschia. We define 25 distinct diatom communities with varying environmental preferences illustrative of different life strategies. The Arctic Ocean stands out as a diatom hotspot with 6 of the diatom communities being exclusive to it. Light harvesting and photoprotection are among the cellular functions in which natural diatom populations invest the bulk of their transcriptional efforts. This comprehensive study sheds light on marine diatom distributions, offering insights to assess impacts of global change and oceanic anthropogenic impacts.
Our knowledge of the factors influencing the distribution of soil organisms is limited to specific taxonomic groups. Consequently, our understanding of the drivers shaping the entire soil multitrophic network is constrained. To address this gap, we conducted an extensive soil biodiversity monitoring program in the French Alps, using environmental DNA to obtain multi-taxon data from 418 soil samples. The spatial structure of resulting soil multitrophic networks varied significantly between and within habitats. From forests to grasslands, we observed a shift in the abundance of trophic groups from fungal to bacterial feeding channels, reflecting different ecosystem functioning. Furthermore, forest soil networks were more strongly spatially structured which could only partly be explained by abiotic conditions. Grassland soil networks were more strongly driven by plant community composition and soil characteristics. Our findings provide valuable insights into how climate and land-use changes may differentially affect soil multitrophic networks in mountains.
Ocean color remote sensing has been used for more than 2 decades to estimate primary productivity. Approaches have also been developed to disentangle phytoplankton community structure based on spectral data from space, in particular when combined with in situ measurements of photosynthetic pigments. Here, we propose a new ocean color algorithm to derive the relative cell abundance of seven phytoplankton groups, as well as their contribution to total chlorophyll a (Chl a) at the global scale. Our algorithm is based on machine learning and has been trained using remotely sensed parameters (reflectance, backscattering, and attenuation coefficients at different wavelengths, plus temperature and Chl a) combined with an omics-based biomarker developed using Tara Oceans data representing a single-copy gene encoding a component of the photosynthetic machinery that is present across all phytoplankton, including both prokaryotes and eukaryotes. It differs from previous methods which rely on diagnostic pigments to derive phytoplankton groups. Our methodology provides robust estimates of the phytoplankton community structure in terms of relative cell abundance and contribution to total Chl a concentration. The newly generated datasets yield complementary information about different aspects of phytoplankton that are valuable for assessing the contributions of different phytoplankton groups to primary productivity and inferring community assembly processes. This makes remote sensing observations excellent tools to collect essential biodiversity variables (EBVs) and provide a foundation for developing marine biodiversity forecasts.
The influential concept of the rare biosphere in microbial ecology has underscored the importance of taxa occurring at low abundances yet potentially playing key roles in communities and ecosystems. Here, we refocus the concept of rare biosphere through a functional trait-based lens and provide a framework to characterize microbial functional rarity, a combination of numerical scarcity across space or time and trait distinctiveness. We demonstrate how this novel interpretation of the rare biosphere, rooted in microbial functions, can enhance our mechanistic understanding of microbial community structure. It also sheds light on functionally distinct microbes, directing conservation efforts towards taxa harboring rare yet ecologically crucial functions.
Phenotypic plasticity can allow organisms to cope with environmental changes. Although reaction norms are commonly used to quantify plasticity along gradients of environmental conditions, they often miss the temporal dynamics of phenotypic change, especially the speed at which it occurs. Here, we argue that studying the rate of phenotypic plasticity is a crucial step to quantify and understand its adaptiveness. Iteratively measuring plastic traits allows us to describe the actual dynamics of phenotypic changes and avoid quantifying reaction norms at times that do not truly reflect the organism's capacity for plasticity. Integrating the temporal component in how we describe, quantify, and conceptualise phenotypic plasticity can change our understanding of its diversity, evolution, and consequences.
Summary paragraph Plankton are essential in marine ecosystems. However, our knowledge of overall community structure is sparse due to inconsistent sampling across their very large organismal size range. Here we use diverse imaging methods to establish complete plankton inventories of organisms spanning five orders of magnitude in size. Plankton community size and trophic structure variation validate a long-held theoretical link between organism size-spectra and ecosystem trophic structures. We found that predator/grazer biomass and biovolume unexpectedly exceed that of primary producers at most (55%) locations, likely due to our better quantification of gelatinous organisms. Bottom- heavy ecosystems (the norm on land) appear to be rare in the ocean. Collectively, gelatinous organisms represent 30% of the total biovolume (8-9% of carbon) of marine plankton communities from tropical to polar ecosystems. Communities can be split into three extreme typologies: diatom/copepod-dominated in eutrophic blooms, rhizarian/chaetognath-dominated in oligotrophic tropical oceans, and gelatinous-dominated elsewhere. While plankton taxonomic composition changes with latitude, functional and trophic structures mostly depend on the amount of prey available for each trophic level. Given future projections of oligotrophication of marine ecosystems, our findings suggest that rhizarian and gelatinous organisms will increasingly dominate the apex position of planktonic ecosystems, leading to significant changes in the ocean’s carbon cycle.
Climate warming and landscape fragmentation are both factors well known to threaten biodiversity and to generate species responses and adaptation. However, the impact of warming and fragmentation interplay on organismal responses remains largely under-explored, especially when it comes to gut symbionts, which may play a key role in essential host functions and traits by extending its functional and genetic repertoire. Here, we experimentally examined the combined effects of climate warming and habitat connectivity on the gut bacterial communities of the common lizard ( Zootoca vivipara ) over three years. While the strength of effects varied over the years, we found that a 2°C warmer climate decreases lizard gut microbiome diversity in isolated habitats. However, enabling connectivity among habitats with warmer and cooler climates offset or even reversed warming effects. The warming effects and the association between host dispersal behaviour and microbiome diversity appear to be a potential driver of this interplay. This study suggests that preserving habitat connectivity will play a key role in mitigating climate change impacts, including the diversity of the gut microbiome, and calls for more studies combining multiple anthropogenic stressors when predicting the persistence of species and communities through global changes.
Our knowledge of the factors influencing the distribution of soil organisms is limited to specific taxonomic groups. Consequently, our understanding of the drivers shaping the entire soil food web is constrained. To address this gap, we conducted an extensive soil biodiversity monitoring program in the French Alps, using environmental DNA to obtain multi-taxon data from 418 soil samples. The spatial structure of resulting soil food webs varied significantly between and within habitats. From forests to grasslands, we observed a shift in the abundance of trophic groups from fungal to bacterial feeding channels, reflecting different ecosystem functioning. Furthermore, forest food webs were more strongly spatially structured which could only partly be explained by abiotic conditions. Grassland food webs were more strongly driven by plant community composition and soil characteristics. Our findings provide valuable insights into how climate and land use changes may differentially affect soil food webs in mountains.
The assembly of phyllosphere microbial communities is under the control of stochastic and deterministic processes. In neotropical forests, the tree host identity and physiology together with strong heterogeneities of the environment within the canopy and at the leaf scale could potentially drive the assembly of phyllosphere microbial communities. We analyzed the assembly processes shaping the microbial communities living in the endophytic and epiphytic phyllosphere in tree species across vertical environmental gradients present from the top of the canopy to the ground. We used DNA metabarcoding to characterize microbial communities and described the microhabitats along the gradient by measuring morphological and chemical foliar traits of host trees. The results revealed that the assembly of both communities resulted from a balance of deterministic and stochastic effects with strong discrepancies between fungal and bacterial communities. Different effects of the host and of the vertical environmental gradient shaped epiphytic and endophytic communities. If fungal communities were mainly shaped by the host identity, different leaf morphological and chemical leaf traits drove the epi- and endophytic bacterial communities. Taken together, the phyllosphere represent a global selective pressure of the plant on microbial communities but the microhabitat at the leaf scale contribute also significantly to drive the assembly of microbial communities.
The study of microbiomes across organisms and environments has become a prominent focus in molecular ecology. This perspective article explores common challenges, methodological advancements, and future directions in the field. Key research areas include understanding the drivers of microbiome community assembly, linking microbiome composition to host genetics, exploring microbial functions, transience and spatial partitioning, and disentangling non-bacterial components of the microbiome. Methodological advancements, such as quantifying absolute abundances, sequencing complete genomes, and utilizing novel statistical approaches, are also useful tools for understanding complex microbial diversity patterns. Our aims are to encourage robust practices in microbiome studies and inspire researchers to explore the next frontier of this rapidly changing field.
The Arctic Ocean (AO) is being rapidly transformed by global warming, but its biodiversity remains understudied for many planktonic organisms, in particular for unicellular eukaryotes that play pivotal roles in marine food webs and biogeochemical cycles. The aim of this study was to characterize the biogeographic ranges of species that comprise the contemporary pool of unicellular eukaryotes in the AO as a first step toward understanding mechanisms that structure these communities and identifying potential target species for monitoring. Leveraging the Tara Oceans DNA metabarcoding data, we mapped the global distributions of operational taxonomic units (OTUs) found on Arctic shelves into five biogeographic categories, identified biogeographic indicators, and inferred the degree to which AO communities of unicellular eukaryotes share members with assemblages from lower latitudes. Arctic/Polar indicator OTUs, as well as some globally ubiquitous OTUs, dominated the detection and abundance of DNA reads in the Arctic samples. OTUs detected only in Arctic samples (Arctic-exclusives) showed restricted distribution with relatively low abundances, accounting for 10–16% of the total Arctic OTU pool. OTUs with high abundances in tropical and/or temperate latitudes (non-Polar indicators) were also found in the AO but mainly at its periphery. We observed a large change in community taxonomic composition across the Atlantic-Arctic continuum, supporting the idea that advection and environmental filtering are important processes that shape plankton assemblages in the AO. Altogether, this study highlights the connectivity between the AO and other oceans, and provides a framework for monitoring and assessing future changes in this vulnerable ecosystem.
Metazoan metabarcoding is emerging as an essential strategy for inventorying biodiversity, with diverse projects currently generating massive quantities of community-level data. The potential for integrating across such data sets offers new opportunities to better understand biodiversity and how it might respond to global change. However, large-scale syntheses may be compromised if metabarcoding workflows differ from each other. There are ongoing efforts to improve standardization for the reporting of inventory data. However, harmonization at the stage of generating metabarcode data has yet to be addressed. A modular framework for harmonized data generation offers a pathway to navigate the complex structure of terrestrial metazoan biodiversity. Here, through our collective expertise as practitioners, method developers, and researchers leading metabarcoding initiatives to inventory terrestrial biodiversity, we seek to initiate a harmonized framework for metabarcode data generation, with a terrestrial arthropod module. We develop an initial set of submodules covering the 5 main steps of metabarcode data generation: (i) sample acquisition; (ii) sample processing; (iii) DNA extraction; (iv) polymerase chain reaction amplification, library preparation, and sequencing; and (v) DNA sequence and metadata deposition, providing a backbone for a terrestrial arthropod module. To achieve this, we (i) identified key points for harmonization, (ii) reviewed the current state of the art, and (iii) distilled existing knowledge within submodules, thus promoting best practice by providing guidelines and recommendations to reduce the universe of methodological options. We advocate the adoption and further development of the terrestrial arthropod module. We further encourage the development of modules for other biodiversity fractions as an essential step toward large-scale biodiversity synthesis through harmonization.
Soil trophic networks are key to biogeochemical cycles, in particular decomposition. However, few studies have yet quantified how microbial decomposition activity along environmental gradients is jointly driven by bacteria, fungi, and their respective consumers. Here, we quantified these direct and indirect effects on decomposition and contrasted them between forests and open habitats using multiple elevational gradients in the French Alps. While environmental control on microbial decomposition activity was comparable in the two habitats, the pathways and strengths of biotic predictors strongly differed. The fungal channel composition played a moderate role in forests, while the bacterial channel composition was critical in open habitats. Importantly, we found trophic regulation by consumers to be a key modulator of the direct environmental effects on decomposition in open habitats. These results highlight the need to integrate trophic regulation when predicting future ecosystem functioning.
The development of high-throughput sequencing (HTS) technologies has greatly improved our capacity to identify fungi and unveil their ecological roles across a variety of ecosystems. Here we provide an overview of current best practices in metabarcoding analysis of fungal communities, from experimental design through molecular and computational analyses. By reanalysing published data sets, we demonstrate that operational taxonomic units (OTUs) outperform amplified sequence variants (ASVs) in recovering fungal diversity, a finding that is particularly evident for long markers. Additionally, analysis of the full-length ITS region allows more accurate taxonomic placement of fungi and other eukaryotes compared to the ITS2 subregion. Finally, we show that specific methods for compositional data analyses provide more reliable estimates of shifts in community structure. We conclude that metabarcoding analyses of fungi are especially promising for integrating fungi into the full microbiome and broader ecosystem functioning context, recovery of novel fungal lineages and ancient organisms as well as barcoding of old specimens including type material.
Land use change drives shifts in the taxonomic and functional diversity of soil organisms. Soil biota response will depend on both local scale agricultural management, and regional scale environmental conditions, with the diverse pool of soil taxa unlikely to respond in a uniform manner. To monitor the effect of land management and potential restoration efforts, we require techniques which can be deployed at various spatial scales, and which account for the high diversity of these communities. In this presentation, we describe the role of eDNA metabarcoding targeting a broad range of taxa to detect and parameterise these responses. We present the results of studies of habitat conversion of humid and dry forests in French Guiana and Colombia respectively, before detailing how the method will be used to monitor agricultural pasture in the UK undergoing conversion to “regenerative” management. In these studies, we combine measures of alpha and beta diversity to account for shifts in species abundance dependent on habitat management, and assignment of functional groups to infer shifts in soil biota functioning. Overall, we find that results track expected shifts in biota, for example a replacement of a broad diversity of plant eDNA to a community signal largely dominated by grasses. Agricultural soils are characterised by a greater proportion of bacteria and protists associated with the cycling of labile nitrogen. We conclude by pointing to the weaknesses of the method, and highlighting the importance of complimentary methods in spite of fruitful deployment across varied habitats.
Aim: Although soil biodiversity is extremely rich and spatially variable, both in terms of species and trophic groups, we still know little about its main drivers. Here, we contrast four long-standing hypotheses to explain the spatial variation of soil multitrophic diversity: energy, physiological tolerance, habitat heterogeneity and resource heterogeneity. Location: French Alps. Methods: We built on a large-scale observatory across the French Alps (Orchamp) made of seventeen elevational gradients (-90 plots) ranging from low to very high altitude (280-3,160 m), and encompassing large variations in climate, vegetation and pedological conditions. Biodiversity measurements of 36 soil trophic groups were obtained through environmental DNA metabarcoding. Using a machine learning approach, we assessed (1) the relative importance of predictors linked to different ecological hypotheses in explaining overall multi-trophic soil biodiversity and (2) the consistency of the response curves across trophic groups. Results: We showed that predictors associated with the four hypotheses had a statistically significant influence on soil multi-trophic diversity, with the strongest support for the energy and physiological tolerance hypotheses. Physiological tolerance explained spatial variation in soil diversity consistently across trophic groups, and was an especially strong predictor for bacteria, protists and microfauna. The effect of energy was more group-specific, with energy input through soil organic matter strongly affecting groups related to the detritus channel. Habitat and resource heterogeneity had overall weaker and more specific impacts on biodiversity with habitat heterogeneity affecting mostly autotrophs, and resource heterogeneity affecting bacterivores, phytophagous insects, enchytraeids and saprotrophic fungi. Main Conclusions: Despite the variability of responses to the environmental drivers found across soil trophic groups, major commonalities on the ecological processes structuring soil biodiversity emerged. We conclude that among the major ecological hypotheses traditionally applied to aboveground organisms, some are particularly relevant to predict the spatial variation in soil biodiversity across the major soil trophic groups.
In soils, plants and fungi can form complex mycorrhizal networks allowing nutrient transfers between plant individuals and species. It is less clear, however, whether such networks exist on the bark of trees where epiphytic plant communities thrive in rainforests. Previous work showed that tropical epiphytic orchids especially, harbour symbiotic fungi in their roots, but the structure and determinants of the resulting networks remain unknown at the tree scale. We tested the hypothesis that epiphytic orchids rooted in the same area on the bark share mycorrhizal fungi, regardless of their species (i.e. spatial determinant). For this purpose, we selected the trunk of six trees of two common species in a rainforest and sampled orchid roots, protocorms and surrounding bark. We identified mycorrhizal fungi including Tulasnellaceae using high‐throughput sequencing of the ITS2 marker, and reconstructed orchid–fungus bipartite networks for each tree to analyse their structure and the spatial turnover of this symbiosis. We found that epiphytic orchid communities form antinested and highly modular networks with mycorrhizal fungi spread on the bark. As expected, modules of interactions are explained by their spatial structure, with nearby roots sharing fungi, but also by the orchid species involved. These results reveal the presence of shared mycelial networks in epiphytic habitats, whose roles in the resilience and facilitation of epiphytic plant communities need to be assessed. Synthesis. Tropical tree barks are densely colonized by certain mycorrhizal fungi that can form symbioses in nearby adult and young orchids simultaneously. These mycorrhizal networks may allow water and nutrient transfers to alleviate the stressful conditions of the epiphytic habitats.