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  • Publication
    Accès libre
    Biodiversity in mountain soils above the treeline
    (2025)
    Nadine Praeg
    ;
    Michael Steinwandter
    ;
    Davnah Urbach
    ;
    Mark A. Snethlage
    ;
    Rodrigo P. Alves
    ;
    Martha E. Apple
    ;
    Peter Bilovitz
    ;
    Andrea J. Britton
    ;
    ;
    Ting‐Wen Chen
    ;
    Kenneth Dumack
    ;
    Fernando Fernandez‐Mendoza
    ;
    Michele Freppaz
    ;
    Beat Frey
    ;
    Nathalie Fromin
    ;
    Stefan Geisen
    ;
    Martin Grube
    ;
    Elia Guariento
    ;
    Antoine Guisan
    ;
    Qiao‐Qiao Ji
    ;
    Juan J. Jiménez
    ;
    Stefanie Maier
    ;
    Lucie A. Malard
    ;
    Maria A. Minor
    ;
    Cowan C. Mc Lean
    ;
    Edward A. D. Mitchell
    ;
    Thomas Peham
    ;
    Roberto Pizzolotto
    ;
    Andy F. S. Taylor
    ;
    Philippe Vernon
    ;
    Johan J. van Tol
    ;
    Donghui Wu
    ;
    Yunga Wu
    ;
    Zhijing Xie
    ;
    Bettina Weber
    ;
    Paul Illmer
    ;
    Julia Seeber
    ABSTRACT Biological diversity in mountain ecosystems has been increasingly studied over the last decade. This is also the case for mountain soils, but no study to date has provided an overall synthesis of the current state of knowledge. Here we fill this gap with a first global analysis of published research on cryptogams, microorganisms, and fauna in mountain soils above the treeline, and a structured synthesis of current knowledge. Based on a corpus of almost 1400 publications and the expertise of 37 mountain soil scientists worldwide, we summarise what is known about the diversity and distribution patterns of each of these organismal groups, specifically along elevation, and provide an overview of available knowledge on the drivers explaining these patterns and their changes. In particular, we document an elevation‐dependent decrease in faunal diversity above the treeline, while for cryptogams there is an initial increase above the treeline, followed by a decrease towards the nival belt. Thus, our data confirm the key role that elevation plays in shaping the biodiversity and distribution of these organisms in mountain soils. The response of prokaryote diversity to elevation, in turn, was more diverse, whereas fungal diversity appeared to be substantially influenced by plants. As far as available, we describe key characteristics, adaptations, and functions of mountain soil species, and despite a lack of ecological information about the uncultivated majority of prokaryotes, fungi, and protists, we illustrate the remarkable and unique diversity of life forms and life histories encountered in alpine mountain soils. By applying rule‐ as well as pattern‐based literature‐mining approaches and semi‐quantitative analyses, we identified hotspots of mountain soil research in the European Alps and Central Asia and revealed significant gaps in taxonomic coverage, particularly among biocrusts, soil protists, and soil fauna. We further report thematic priorities for research on mountain soil biodiversity above the treeline and identify unanswered research questions. Building upon the outcomes of this synthesis, we conclude with a set of research opportunities for mountain soil biodiversity research worldwide. Soils in mountain ecosystems above the treeline fulfil critical functions and make essential contributions to life on land. Accordingly, seizing these opportunities and closing knowledge gaps appears crucial to enable science‐based decision making in mountain regions and formulating laws and guidelines in support of mountain soil biodiversity conservation targets.
  • Publication
    Restriction temporaire
    Unveiling the biogeography of terrestrial protists through microscopy, metabarcoding, and species distribution modelling : from testate amoebae as model organisms to community patterns
    (Neuchâtel : Université de Neuchâtel, 2024) ; ;
    Ma thèse de doctorat porte sur la biogéographie et l'écologie des protistes terrestres libres en tant que communauté et des amibes à thèque de l’ordre des arcellinides (Amoebozoa: Arcellinida) en tant qu’organismes modèles. Mes recherches s’articulent autour de deux objectifs principaux: (1) le développement d'une stratégie d'échantillonnage pour étudier, à l’aide du métabarcoding de l’ADN environnemental, l’ensemble de la communauté des protistes du sol le long de gradients d'altitude en tenant compte de leur dynamique spatiotemporelle, et (2) le développement de modèles de distribution d’espèces d’amibes à thèque pour évaluer si les prédictions de distribution à l’échelle globale corroborent l'hypothèse selon laquelle les micro-organismes ont une distribution géographique restreinte. De plus, ces modèles prédictifs visent également à étudier la capacités et les limitations de distribution des amibes à thèque à atteindre des écosystèmes insulaires isolés, et à évaluer leurs risques d'extinction en réponse aux futurs changements climatiques. Dans la première étude, mes recherches ont porté sur la dynamique spatio-temporelle de l’ensemble de la communauté des protistes du sol le long de multiples gradients d’altitude dans les Alpes suisses et la Sierra Nevada espagnole. L’objectif était de déterminer, à l’aide du métabarcoding de l’ADN environnemental, si la dynamique temporelle des communautés de protistes du sol pourrait introduire des biais dans l’études de leur biodiversité lorsque plusieurs gradients d’altitude échantillonnés à travers différentes saisons, habitats, régions ou latitudes sont comparés. Mes analyses ont révélé que la bêta-diversité des communautés de protistes du sol est principalement influencée par l’hétérogénéité spatiale plutôt que par le turnover temporel. Ainsi, les résultats indiquent que, dans les climats tempérés, un seul échantillonnage le long d’un gradient d'altitude n'introduit pas de biais dû aux différences phénologiques entre les saisons. Par conséquent, la bêta-diversité entre plusieurs gradients et plusieurs régions peut être comparée de manière fiable, même si l'échantillonnage n'est pas simultané. Mon deuxième projet a permis d’étudier la distribution et le potentiel de dispersion à longue distance de l'amibe à thèque Apodera vas (Certes) Loeblich & Tappan à l'aide d'un modèle de distribution d’espèce à l’échelle mondiale et basé sur la niche climatique. Les résultats ont révélé de surprenantes divergences entre le potentiel de dispersion à longue distance latitudinale et longitudinale. En effet, alors que le modèle indique de nombreuses zones propices à A. vas dans l’hémisphère nord, le potentiel de distribution interhémisphérique du taxon semble limité, contrairement au potentiel de dispersion longitudinale par le vent ou par les oiseaux qui a été confirmé, notamment dans les îles péri-antarctiques. En outre, en extrapolant le modèle aux climats passés et futurs, j'ai évalué les expansions et contractions des zones propices à A. vas au fil du temps. Jusqu’à la fin du 21ème siècle, les prévisions annoncent une forte réduction des zones propices à ce taxon sur tous les continents en raison du changement climatique. Apodera vas étant un complexe d’espèces cryptiques, mes résultats mettent en évidence d’importants risques d'extinctions régionaux et souligne la nécessité de stratégies de conservation ciblées qui incluent les protistes du sol. J'ai utilisé la même approche de modélisation dans le cadre de la troisième étude pour déterminer les aires propices à l'amibe à thèque Hyalosphenia papilio Leidy à l’échelle globale et étudier les raisons de son absence dans l'archipel des Açores (Portugal) malgré la présence de vastes tourbières à sphaignes. Comme pour A. vas, le modèle de distribution de H. papilio suggère une absence de potentiel de distribution interhémisphérique, mais confirme qu'une dispersion sur de courtes distances est possible. Alors que plusieurs espèces de la même taille que H. papilio ont été trouvées dans des échantillons de sphaigne des Açores, H. papilo ainsi que d'autres espèces mixotrophes étaient absentes, et ceci malgré un climat favorable et la présence d'un habitat approprié. Ce cas de disharmonie insulaire est probablement dû davantage au développement récent des tourbières à sphaignes déclenché par des changements hydrologiques liés au déboisement qu'à une limitation de la dispersion. Pour conclure, en évaluant la robustesse des méthodes d'échantillonnage le long des gradients d'altitude, mon étude a mis en évidence que, dans les régions tempérées, un effort d'échantillonnage réduit (c'est-à-dire une fois par an au lieu d'un échantillonnage répété) ne fausserait pas la comparaison de la bêta-diversité dans le cadre d’études à large échelle. En utilisant la modélisation et les amibes à thèque comme organismes modèles, mes deux autres chapitres de thèse approfondissent les connaissances sur les potentiels mécanismes de dispersion, les filtres environnementaux et l’héritage de l’impact humain passé qui régissent la biogéographie des protistes du sol et soulignent qu'en effet, au moins certains microorganismes ont une biogéographie. De plus, la modélisation permet non seulement d'orienter les études futures, mais met également en exergue les menac es climatiques importantes qui pèsent sur la diversité microbienne. Par conséquent, mes résultats soutiennent l'idée que, à l'instar des plantes et des animaux, les protistes du sol sont fortement structurés dans l'espace à la fois à l'échelle régionale (le long des gradients d'altitude) et à l'échelle mondiale. En outre, ces motifs de distribution peuvent être observés à différents niveaux taxonomiques . En définitive, ma thèse met en lumière l’utilité de combiner différentes approches méthodologiques et différents niveaux taxonomiques pour étudier la biogéographie de protistes du sol. Elle souligne également le besoin urgent de combler les lacunes taxonomiques (‘Linnean shortfall’) et de distribution (‘Wallacean shortfall’) des protistes du sol. Finalement, mon travail illustre l'importance de la collaboration entre les chercheurs et chercheuses en protistologie, en modélisation et en conservation afin d'élaborer des mesures de conservation concrètes pour ces communautés microbiennes vitales et les écosystèmes qu'elles habitent. ABSTRACT My PhD thesis delves into the biogeography and ecology of terrestrial free-living protists, as a community, and on arcellinid testate amoebae (Amoebozoa: Arcellinida) as model organisms. My research is centred on two principal objectives:(1) the development of a metabarcodingbased sampling strategy to study spatio-temporal dynamics of soil protist communities across elevation gradients, and (2) the development of global-scale testate amoebae species distribution models to evaluate if these models corroborate the hypothesis that microorganisms possess restricted geographical distributions. These predictions further aim to investigate the dispersal capabilities and limitations of testate amoebae to reach isolated island ecosystems and to assess their extinction risks in response to future climate change. In the first study, my research investigated the spatio-temporal dynamics of the entire soil protist community along multiple elevation gradients in the Swiss Alps and Spanish Sierra Nevada using environmental DNA metabarcoding. The aim was to determine if temporal dynamics in soil protist communities could introduce biases in biodiversity studies when multiple elevation gradients sampled across different seasons, habitats, regions, or latitudes are compared. My analyses revealed that soil protist community beta-diversity is primarily influenced by spatial heterogeneity rather than temporal turnover. Thus, the results indicate that conducting a single sampling across an elevation gradient in temperate climates does not introduce biases due to phenological differences between seasons. Consequently, beta diversity patterns can be reliably compared between gradients and regions, even if the sampling is not simultaneous. My second project allowed to investigate the distribution and long-distance dispersal (LDD) potential of the testate amoeba Apodera vas (Certes) Loeblich & Tappan using a global climate niche modelling approach. The results revealed intriguing discrepancies between latitudinal and longitudinal LDD for A. vas, with no evidence of interhemispheric LDD, whereas longitudinal LDD, either by wind or by birds, was confirmed, notably in peri-Antarctic islands. Furthermore, by extrapolating the model to past and future climates, I assessed range expansions and contractions over time. Until the end of the 21st century, the predictions forecast a strong reduction in climate suitability for this taxon on all continents due to future climate change. Apodera vas being a complex of cryptic species, this underscores significant risks of regional extinctions and emphasizes the need for targeted conservation strategies that include soil protists. I employed the same modelling approach in the third project and investigated the global climate niche suitability of the testate amoeba Hyalosphenia papilio Leidy and the reasons for its absence in the Azores archipelago (Portugal), despite the presence of extensive Sphagnum-dominated peatlands. Similar to A. vas, the model suggested a lack of interhemispheric LDD for H. papilio but confirmed that short distance dispersal is likely. While several species of the same size range of H. papilio were found in Sphagnum samples from the Azores, H. papilo was absent as well as other mixotrophic species, despite favourable climatic and the presence of the appropriate habitat. This case of island disharmony may be due more to the recent development of Sphagnum peatlands triggered by hydrological changes due to forest clearance than to dispersal limitation. To conclude, by assessing the robustness of the sampling design along elevation gradients, my study highlighted that, in temperate regions, reduced sampling effort (i.e., once per year versus repeated sampling) would not bias beta diversity comparison of large-scale studies. By using species distribution modelling and testate amoebae as model organisms, my two other studies provide insights into the potential dispersal mechanisms, environmental filtering and legacy of past human impact governing the biogeography of soil protists and emphasize that at least some microorganisms do have a biogeography. Additionally, species distribution modelling not only has the potential to guide future studies but also highlights the significant climate threats to microbial diversity. Overall, my results support the notion that soil protist diversity is strongly structured spatially at both regional (along elevation gradients) and global scales, akin to plants and animals. Furthermore, these distribution patterns can be observed at different taxonomic levels (i.e., single testate amoeba taxa vs. entire soil protist community). Consequently, my thesis underscores the utility of combining different methodological approaches and focusing on different taxonomical levels to study soil protist biogeography. It also stresses the urgent need to address the Linnean (taxonomic) and Wallacean (distributional) shortfalls in soil protists. Finally, my work highlights the importance of collaboration among protist researchers, species distribution modeller and conservationists to develop concrete conservation measures for these vital microbial communities and the ecosystems they inhabit.
  • Publication
    Accès libre
    Higher spatial than seasonal beta diversity of soil protists along elevation gradients
    Biodiversity patterns along elevation gradients have long been studied for plants and animals, but only quite recently for soil microorganisms, especially protists (eukaryotes excluding plants, animals, and fungi). Microorganisms have shorter generation times than macroorganisms, and their abundance, diversity, and community structure are known to vary rapidly in response to abiotic and biotic factors. If microbial diversity varies more seasonally than spatially, a single sampling campaign along an elevation gradient, with contrasted phenologies, could introduce bias into biodiversity studies comparing multiple elevation gradients across different seasons, habitats, regions or latitudes. To address this question, we investigated the relative magnitude of spatial versus temporal diversity (alpha diversity) and community turnover (beta diversity) of soil protist communities along elevation gradients in two distant European mountain ranges. We collected soil samples in forests and grasslands below the treeline along five elevation gradients in two consecutive seasons (spring and summer) in the Spanish Sierra Nevada and the Swiss Alps, covering two distinct biogeographic regions. Using general eukaryotic primers and amplicon sequencing of soil environmental DNA, we decomposed total protist amplicon sequence variants diversity into local alpha- and beta diversity components and identified climatic and edaphic predictors of biodiversity patterns using redundancy analyses. Soil protist communities varied spatially within and among transects but temporal turnover was comparatively low. The best edaphic predictors of community variations were the same in spring and summer, but their explanatory power differed among seasons. The dominant spatial component of beta diversity suggests that patterns of soil protist communities along elevation gradients are more strongly driven by spatial heterogeneity than inter-seasonal turnover. Thus, in temperate climates, our results suggest that sampling only once between the end of spring and late summer across an elevation gradient does not introduce bias due to phenological differences when comparing beta diversity across multiple gradients. Spatio-temporal dynamics of soil protists communities were studied in forests and grasslands below the tree line along five elevation gradients in the Spanish Sierra Nevada and the Swiss Alps during two consecutive seasons (spring and summer). The total diversity of soil protist communities was predominantly shaped by beta-diversity components with spatial heterogeneity rather than temporal turnover as the main driver of soil protist community composition. Community dissimilarity of soil protists did not differ in response to temporal changes between habitats (i.e., forests versus grasslands) The significant edaphic predictors of protist community composition were highly similar in the Swiss Alps and identical in the Spanish Sierra Nevada between both seasons, but their explanatory power varied between spring and summer. Soil protist beta diversity patterns along different elevation gradients remained constant between seasons. This suggests that, in temperate climates, sampling at one time across an elevation gradient will not bias results stemming from phenological contrasts, allowing comparison of beta diversity patterns along such gradients between regions even if sampling is not simultaneous.
  • Publication
    Accès libre
    Soil filtration‐sedimentation improves shelled protist recovery in eukaryotic eDNA surveys
    (2023) ; ;
    Claudine Ah‐Peng
    ;
    Junichi Fujinuma
    ;
    Yasuhiro Kubota
    ;
    Juan Lorite
    ;
    Julio Peñas
    ;
    Shuyin Huang
    ;
    Dominique Strasberg
    ;
    Pascal Vittoz
    ;
    AbstractA large part of the soil protist diversity is missed in metabarcoding studies based on 0.25 g of soil environmental DNA (eDNA) and universal primers due to ca. 80% co‐amplification of non‐target plants, animals and fungi. To overcome this problem, enrichment of the substrate used for eDNA extraction is an easily implemented option but its effect has not yet been tested. In this study, we evaluated the effect of a 150 μm mesh size filtration and sedimentation method to improve the recovery of protist eDNA, while reducing the co‐extraction of plant, animal and fungal eDNA, using a set of contrasted forest and alpine soils from La Réunion, Japan, Spain and Switzerland. Total eukaryotic diversity was estimated by V4 18S rRNA metabarcoding and classical amplicon sequence variant calling. A 2‐ to 3‐fold enrichment in shelled protists (Euglyphida, Arcellinida and Chrysophyceae) was observed at the sample level with the proposed method, with, at the same time, a 2‐fold depletion of Fungi and a 3‐fold depletion of Embryophyceae. Protist alpha diversity was slightly lower in filtered samples due to reduced coverage in Variosea and Sarcomonadea, but significant differences were observed in only one region. Beta diversity varied mostly between regions and habitats, which explained the same proportion of variance in bulk soil and filtered samples. The increased resolution in soil protist diversity estimates provided by the filtration‐sedimentation method is a strong argument in favour of including it in the standard protocol for soil protist eDNA metabarcoding studies.
  • Publication
    Accès libre
    Global distribution modelling of a conspicuous Gondwanian soil protist reveals latitudinal dispersal limitation and range contraction in response to climate warming
    (2023) ; ;
    Olivier Broennimann
    ;
    Antoine Adde
    ;
    ;
    Valentyna Krashevska
    ;
    ;
    Eric Armynot du Châtelet
    ;
    João P. B. Alcino
    ;
    Louis Beyens
    ;
    ;
    Anatoly Bobrov
    ;
    Luciana Burdman
    ;
    ; ;
    Maria Beatriz Gomes e Souza
    ;
    Thierry J. Heger
    ;
    ;
    Daniel J. G. Lahr
    ;
    Michelle McKeown
    ;
    Ralf Meisterfeld
    ;
    ;
    Eckhard Voelcker
    ;
    Janet Wilmshurst
    ;
    Sebastien Wohlhauser
    ;
    David M. Wilkinson
    ;
    Antoine Guisan
    ;
    Edward A. D. Mitchell
    AbstractAimThe diversity and distribution of soil microorganisms and their potential for long‐distance dispersal (LDD) are poorly documented, making the threats posed by climate change difficult to assess. If microorganisms do not disperse globally, regional endemism may develop and extinction may occur due to environmental changes. Here, we addressed this question using the testate amoeba Apodera vas, a morphologically conspicuous model soil microorganism in microbial biogeography, commonly found in peatlands and forests mainly of former Gondwana. We first documented its distribution. We next assessed whether its distribution could be explained by dispersal (i.e. matching its climatic niche) or vicariance (i.e. palaeogeography), based on the magnitude of potential range expansions or contractions in response to past and on‐going climatic changes. Last, we wanted to assess the likelihood of cryptic diversity and its potential threat from climate and land‐use changes (e.g. due to limited LDD).LocationDocumented records: Southern Hemisphere and intertropical zone; modelling: Global.MethodsWe first built an updated global distribution map of A. vas using 401 validated georeferenced records. We next used these data to develop a climatic niche model to predict its past (LGM, i.e. 21 ± 3 ka BP; PMIP3 IPSL‐CM5A‐LR), present and future (IPSL‐CMP6A‐LR predictions for 2071–2100, SSP3 and 5) potential distributions in responses to climate, by relating the species occurrences to climatic and topographic predictors. We then used these predictions to test our hypotheses (dispersal/vicariance, cryptic diversity, future threat from LDD limitation).ResultsOur models show that favourable climatic conditions for A. vas currently exist in the British Isles, an especially well‐studied region for testate amoebae where this species has never been found. This demonstrates a lack of interhemispheric LDD, congruent with the palaeogeography (vicariance) hypothesis. Longitudinal LDD is, however, confirmed by the presence of A. vas in isolated and geologically young peri‐Antarctic islands. Potential distribution maps for past, current and future climates show favourable climatic conditions existing on parts of all southern continents, with shifts to higher land from LGM to current in the tropics and a strong range contraction from current to future (global warming IPSL‐CM6A‐LR scenario for 2071–2100, SSP3.70 and SSP5.85) with favourable conditions developing on the Antarctic Peninsula.Main ConclusionsThis study illustrates the value of climate niche models for research on microbial diversity and biogeography, along with exploring the role played by historical factors and dispersal limitation in shaping microbial biogeography. We assess the discrepancy between latitudinal and longitudinal LDD for A. vas, which is possibly due to contrast in wind patterns and/or likelihood of transport by birds. Our models also suggest that climate change may lead to regional extinction of terrestrial microscopic organisms, thus illustrating the pertinence of including microorganisms in biodiversity conservation research and actions.