Biogeographic history of a large clade of ectomycorrhizal fungi, the Russulaceae, in the Neotropics and adjacent regions.

The biogeography of neotropical fungi remains poorly understood. Here, we reconstruct the origins and diversification of neotropical lineages in one of the largest clades of ectomycorrhizal fungi in the globally widespread family Russulaceae. We inferred a supertree of 3285 operational taxonomic units, representing worldwide internal transcribed spacer sequences. We reconstructed biogeographic history and diversification and identified lineages in the Neotropics and adjacent Patagonia. The ectomycorrhizal Russulaceae have a tropical African origin. The oldest lineages in tropical South America, most with African sister groups, date to the mid-Eocene, possibly coinciding with a boreotropical migration corridor. There were several transatlantic dispersal events from Africa more recently. Andean and Central American lineages mostly have north-temperate origins and are associated with North Andean uplift and the general north-south biotic interchange across the Panama isthmus, respectively. Patagonian lineages have Australasian affinities. Diversification rates in tropical South America and other tropical areas are lower than in temperate areas. Neotropical Russulaceae have multiple biogeographic origins since the mid-Eocene involving dispersal and co-migration. Discontinuous distributions of host plants may explain low diversification rates of tropical lowland ectomycorrhizal fungi. Deeply diverging neotropical fungal lineages need to be better documented.

Cascading effects of moth outbreaks on subarctic soil food webs.

The increasing severity and frequency of natural disturbances requires a better understanding of their effects on all compartments of biodiversity. In Northern Fennoscandia, recent large-scale moth outbreaks have led to an abrupt change in plant communities from birch forests dominated by dwarf shrubs to grass-dominated systems. However, the indirect effects on the belowground compartment remained unclear. Here, we combined eDNA surveys of multiple trophic groups with network analyses to demonstrate that moth defoliation has far-reaching consequences on soil food webs. Following this disturbance, diversity and relative abundance of certain trophic groups declined (e.g., ectomycorrhizal fungi), while many others expanded (e.g., bacterivores and omnivores) making soil food webs more diverse and structurally different. Overall, the direct and indirect consequences of moth outbreaks increased belowground diversity at different trophic levels. Our results highlight that a holistic view of ecosystems improves our understanding of cascading effects of major disturbances on soil food webs.

Root anatomy helps to reconcile observed root trait syndromes in tropical tree species.

PREMISE: Studying the organization of functional traits in plant leaves and stems has revealed notable patterns linking function and form; however, evidence of similarly robust organization in root tissues remains controversial. We posit that anatomical traits in roots can provide insight on the overall organization of the root system. We hypothesized that size variation in the tissue outside the stele is related in a nonlinear fashion with functional traits associated with direct resource uptake, including a negative relationship with root architectural traits, and that similar relationships detected in tropical areas also hold true in other biomes. METHODS: We addressed our hypotheses using empirical data from 24 tropical tree species in French Guiana, including anatomical measurements in first order roots and functional trait description for the entire fine root system. In addition, we compiled a global meta-analysis of root traits for 500+ forest species across tropical, subtropical, and temperate forests. RESULTS: Our results supported the expected nonlinear relationships between cortical size and morphological traits and a negative linear trend with architectural traits. We confirmed a global negative relationship among specific root length (SRL), diameter, and tissue density, suggesting similar anatomical constraints in root systems across woody plants. However, the importance of factors varies across biomes, possibly related to the unequal phylogenetic representation across latitudes. CONCLUSIONS: Our findings imply that the rhizocentric hypothesis can be a valuable approach to understand fine root trait syndromes and the evolution of absorptive roots in vascular plants.

Taxonomic, phylogenetic and functional diversity of root-associated fungi in bromeliads: effects of host identity, life forms and nutritional modes.

Bromeliads represent a major component of neotropical forests and encompass a considerable diversity of life forms and nutritional modes. Bromeliads explore highly stressful habitats and root-associated fungi may play a crucial role in this, but the driving factors and variations in root-associated fungi remain largely unknown. We explored root-associated fungal communities in 17 bromeliad species and their variations linked to host identity, life forms and nutritional modes by using ITS1 gene-based high-throughput sequencing and by characterizing fungal functional guilds. We found a dual association of mycorrhizal and nonmycorrhizal fungi. The different species, life forms and nutritional modes among bromeliad hosts had fungal communities that differ in their taxonomic and functional composition. Specifically, roots of epiphytic bromeliads had more endophytic fungi and dark septate endophytes and fewer mycorrhizal fungi than terrestrial bromeliads and lithophytes. Our results contribute to a fundamental knowledge base on different fungal groups in previously undescribed Bromeliaceae. The diverse root-associated fungal communities in bromeliads may enhance plant fitness in both stressful and nutrient-poor environments and may give more flexibility to the plants to adapt to changing environmental conditions.

Surprising low diversity of the plant pathogen Phytophthora in Amazonian forests.

The genus Phytophthora represents a group of plant pathogens with broad global distribution. The majority of them cause the collar and root-rot of diverse plant species. Little is known about Phytophthora communities in forest ecosystems, especially in the Neotropical forests where natural enemies could maintain the huge plant diversity via negative density dependence. We characterized the diversity of soil-borne Phytophthora communities in the North French Guiana rainforest and investigated how they are structured by host identity and environmental factors. In this little-explored habitat, 250 soil cores were sampled from 10 plots hosting 10 different plant families across three forest environments (Terra Firme, Seasonally Flooded and White Sand). Phytophthora diversity was studied using a baiting approach and metabarcoding (High-Throughput Sequencing) on environmental DNA extracted from both soil samples and baiting-leaves. These three approaches revealed very similar communities, characterized by an unexpected low diversity of Phytophthora species, with the dominance of two cryptic species close to Phytophthora heveae. As expected, the Phytophthora community composition of the French Guiana rainforest was significantly impacted by the host plant family and environment. However, these plant pathogen communities are very small and are dominated by generalist species, questioning their potential roles as drivers of plant diversity in these Amazonian forests.

Latent Dirichlet Allocation reveals spatial and taxonomic structure in a DNA-based census of soil biodiversity from a tropical forest.

High-throughput sequencing of amplicons from environmental DNA samples permits rapid, standardized and comprehensive biodiversity assessments. However, retrieving and interpreting the structure of such data sets requires efficient methods for dimensionality reduction. Latent Dirichlet Allocation (LDA) can be used to decompose environmental DNA samples into overlapping assemblages of co-occurring taxa. It is a flexible model-based method adapted to uneven sample sizes and to large and sparse data sets. Here, we compare LDA performance on abundance and occurrence data, and we quantify the robustness of the LDA decomposition by measuring its stability with respect to the algorithm's initialization. We then apply LDA to a survey of 1,131 soil DNA samples that were collected in a 12-ha plot of primary tropical forest and amplified using standard primers for bacteria, protists, fungi and metazoans. The analysis reveals that bacteria, protists and fungi exhibit a strong spatial structure, which matches the topographical features of the plot, while metazoans do not, confirming that microbial diversity is primarily controlled by environmental variation at the studied scale. We conclude that LDA is a sensitive, robust and computationally efficient method to detect and interpret the structure of large DNA-based biodiversity data sets. We finally discuss the possible future applications of this approach for the study of biodiversity.

Fungi of French Guiana gathered in a taxonomic, environmental and molecular dataset.

In Amazonia, the knowledge about Fungi remains patchy and biased towards accessible sites. This is particularly the case in French Guiana where the existing collections have been confined to few coastal localities. Here, we aimed at filling the gaps of knowledge in undersampled areas of this region, particularly focusing on the Basidiomycota. From 2011, we comprehensively collected fruiting-bodies with a stratified and reproducible sampling scheme in 126 plots. Sites of sampling reflected the main forest habitats of French Guiana in terms of soil fertility and topography. The dataset of 5219 specimens gathers 245 genera belonging to 75 families, 642 specimens are barcoded. The dataset is not a checklist as only 27% of the specimens are identified at the species level but 96% are identified at the genus level. We found an extraordinary diversity distributed across forest habitats. The dataset is an unprecedented and original collection of Basidiomycota for the region, making specimens available for taxonomists and ecologists. The database is publicly available in the GBIF repository ( https://doi.org/10.15468/ymvlrp ).

Coordinated community structure among trees, fungi and invertebrate groups in Amazonian rainforests.

Little is known regarding how trophic interactions shape community assembly in tropical forests. Here we assess multi-taxonomic community assembly rules using a rare standardized coordinated inventory comprising exhaustive surveys of five highly-diverse taxonomic groups exerting key ecological functions: trees, fungi, earthworms, ants and spiders. We sampled 36 1.9-ha plots from four remote locations in French Guiana including precise soil measurements, and we tested whether species turnover was coordinated among groups across geographic and edaphic gradients. All species group pairs exhibited significant compositional associations that were independent from soil conditions. For some of the pairs, associations were also partly explained by soil properties, especially soil phosphorus availability. Our study provides evidence for coordinated turnover among taxonomic groups beyond simple relationships with environmental factors, thereby refining our understanding regarding the nature of interactions occurring among these ecologically important groups.

Body size determines soil community assembly in a tropical forest.

Tropical forests shelter an unparalleled biological diversity. The relative influence of environmental selection (i.e., abiotic conditions, biotic interactions) and stochastic-distance-dependent neutral processes (i.e., demography, dispersal) in shaping communities has been extensively studied for various organisms, but has rarely been explored across a large range of body sizes, in particular in soil environments. We built a detailed census of the whole soil biota in a 12-ha tropical forest plot using soil DNA metabarcoding. We show that the distribution of 19 taxonomic groups (ranging from microbes to mesofauna) is primarily stochastic, suggesting that neutral processes are prominent drivers of the assembly of these communities at this scale. We also identify aluminium, topography and plant species identity as weak, yet significant drivers of soil richness and community composition of bacteria, protists and to a lesser extent fungi. Finally, we show that body size, which determines the scale at which an organism perceives its environment, predicted the community assembly across taxonomic groups, with soil mesofauna assemblages being more stochastic than microbial ones. These results suggest that the relative contribution of neutral processes and environmental selection to community assembly directly depends on body size. Body size is hence an important determinant of community assembly rules at the scale of the ecological community in tropical soils and should be accounted for in spatial models of tropical soil food webs.

Diversity and Structure of Fungal Communities in Neotropical Rainforest Soils: The Effect of Host Recurrence.

The patterns of the distribution of fungal species and their potential interactions with trees remain understudied in Neotropical rainforests, which harbor more than 16,000 tree species, mostly dominated by endomycorrhizal trees. Our hypothesis was that tree species shape the non-mycorrhizal fungal assemblages in soil and litter and that the diversity of fungal communities in these two compartments is partly dependent on the coverage of trees in the Neotropical rainforest. In French Guiana, a long-term plantation and a natural forest were selected to test this hypothesis. Fungal ITS1 regions were sequenced from soil and litter samples from within the vicinity of tree species. A broad range of fungal taxa was found, with 42 orders and 14 classes. Significant spatial heterogeneity in the fungal communities was found without strong variation in the species richness and evenness among the tree plots. However, tree species shaped the fungal assemblages in the soil and litter, explaining up to 18 % of the variation among the communities in the natural forest. These results demonstrate that vegetation cover has an important effect on the structure of fungal assemblages inhabiting the soil and litter in Amazonian forests, illustrating the relative impact of deterministic processes on fungal community structures in these highly diverse ecosystems.

C, N and P fertilization in an Amazonian rainforest supports stoichiometric dissimilarity as a driver of litter diversity effects on decomposition.

Plant leaf litter generally decomposes faster as a group of different species than when individual species decompose alone, but underlying mechanisms of these diversity effects remain poorly understood. Because resource C : N : P stoichiometry (i.e. the ratios of these key elements) exhibits strong control on consumers, we supposed that stoichiometric dissimilarity of litter mixtures (i.e. the divergence in C : N : P ratios among species) improves resource complementarity to decomposers leading to faster mixture decomposition. We tested this hypothesis with: (i) a wide range of leaf litter mixtures of neotropical tree species varying in C : N : P dissimilarity, and (ii) a nutrient addition experiment (C, N and P) to create stoichiometric similarity. Litter mixtures decomposed in the field using two different types of litterbags allowing or preventing access to soil fauna. Litter mixture mass loss was higher than expected from species decomposing singly, especially in presence of soil fauna. With fauna, synergistic litter mixture effects increased with increasing stoichiometric dissimilarity of litter mixtures and this positive relationship disappeared with fertilizer addition. Our results indicate that litter stoichiometric dissimilarity drives mixture effects via the nutritional requirements of soil fauna. Incorporating ecological stoichiometry in biodiversity research allows refinement of the underlying mechanisms of how changing biodiversity affects ecosystem functioning.

Cantharellaceae of Guyana II: new species of Craterellus, new South American distribution records for Cantharellus guyanensis and Craterellus excelsus, and a key to the Neotropical taxa.

Craterellus olivaceoluteus sp. nov. and Craterellus cinereofimbriatus sp. nov. are described as new to science. These fungi were collected from Guyana in association with ectomycorrhizal host trees in the genera Dicymbe (Fabaceae subfam. Caesalpinioideae) and Pakaraimaea (Dipterocarpaceae). Cantharellus guyanensis Mont., originally described from French Guiana, is redescribed from recent collections from Guyana, with additional range extensions for the species provided based on material examined from French Guiana, Venezuela, and north central, northeastern and southern Brazil, circumscribing nearly the entire Guiana Shield region and beyond. A new distribution record from French Guiana is provided for Craterellus excelsus T.W. Henkel & Aime. Macromorphological, micromorphological and habitat data are provided for the new species and C. guyanensis as well as DNA sequence data from the nuclear ribosomal regions of the internal transcribed spacer (ITS) and 28S large subunit (LSU); additional sequence data is provided for C. guyanensis and C. excelsus specimens collected outside Guyana. The relationships of these taxa within the Cantharellaceae were evaluated with phylogenetic analyses of ITS and LSU sequence data. This work brings the total number of Cantharellaceae species known from Guyana to eight. A key to the Cantharellus and Craterellus species known from the lowland Neotropics and extralimital montane Central and South America is provided.

Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi.

We aimed to enhance understanding of the molecular diversity of arbuscular mycorrhizal fungi (AMF) by building a new global dataset targeting previously unstudied geographical areas. In total, we sampled 96 plant species from 25 sites that encompassed all continents except Antarctica. AMF in plant roots were detected by sequencing the nuclear SSU rRNA gene fragment using either cloning followed by Sanger sequencing or 454-sequencing. A total of 204 AMF phylogroups (virtual taxa, VT) were recorded, increasing the described number of Glomeromycota VT from 308 to 341 globally. Novel VT were detected from 21 sites; three novel but nevertheless widespread VT (Glomus spp. MO-G52, MO-G53, MO-G57) were recorded from six continents. The largest increases in regional VT number were recorded in previously little-studied Oceania and in the boreal and polar climatic zones - this study providing the first molecular data from the latter. Ordination revealed differences in AM fungal communities between different continents and climatic zones, suggesting that both biogeographic history and environmental conditions underlie the global variation of those communities. Our results show that a considerable proportion of Glomeromycota diversity has been recorded in many regions, though further large increases in richness can be expected in remaining unstudied areas.

Distinct microbial limitations in litter and underlying soil revealed by carbon and nutrient fertilization in a tropical rainforest.

Human-caused alterations of the carbon and nutrient cycles are expected to impact tropical ecosystems in the near future. Here we evaluated how a combined change in carbon (C), nitrogen (N) and phosphorus (P) availability affects soil and litter microbial respiration and litter decomposition in an undisturbed Amazonian rainforest in French Guiana. In a fully factorial C (as cellulose), N (as urea), and P (as phosphate) fertilization experiment we analyzed a total of 540 litterbag-soil pairs after a 158-day exposure in the field. Rates of substrate-induced respiration (SIR) measured in litter and litter mass loss were similarly affected by fertilization showing the strongest stimulation when N and P were added simultaneously. The stimulating NP effect on litter SIR increased considerably with increasing initial dissolved organic carbon (DOC) concentrations in litter, suggesting that the combined availability of N, P, and a labile C source has a particularly strong effect on microbial activity. Cellulose fertilization, however, did not further stimulate the NP effect. In contrast to litter SIR and litter mass loss, soil SIR was reduced with N fertilization and showed only a positive effect in response to P fertilization that was further enhanced with additional C fertilization. Our data suggest that increased nutrient enrichment in the studied Amazonian rainforest can considerably change microbial activity and litter decomposition, and that these effects differ between the litter layer and the underlying soil. Any resulting change in relative C and nutrient fluxes between the litter layer and the soil can have important consequences for biogeochemical cycles in tropical forest ecosystems.

A cost-benefit analysis of acclimation to low irradiance in tropical rainforest tree seedlings: leaf life span and payback time for leaf deployment.

The maintenance in the long run of a positive carbon balance under very low irradiance is a prerequisite for survival of tree seedlings below the canopy or in small gaps in a tropical rainforest. To provide a quantitative basis for this assumption, experiments were carried out to determine whether construction cost (CC) and payback time for leaves and support structures, as well as leaf life span (i) differ among species and (ii) display an irradiance-elicited plasticity. Experiments were also conducted to determine whether leaf life span correlates to CC and payback time and is close to the optimal longevity derived from an optimization model. Saplings from 13 tropical tree species were grown under three levels of irradiance. Specific-CC was computed, as well as CC scaled to leaf area at the metamer level. Photosynthesis was recorded over the leaf life span. Payback time was derived from CC and a simple photosynthesis model. Specific-CC displayed only little interspecific variability and irradiance-elicited plasticity, in contrast to CC scaled to leaf area. Leaf life span ranged from 4 months to >26 months among species, and was longest in seedlings grown under lowest irradiance. It was always much longer than payback time, even under the lowest irradiance. Leaves were shed when their photosynthesis had reached very low values, in contrast to what was predicted by an optimality model. The species ranking for the different traits was stable across irradiance treatments. The two pioneer species always displayed the smallest CC, leaf life span, and payback time. All species displayed a similar large irradiance-elicited plasticity.

Long-term presence of tree species but not chemical diversity affect litter mixture effects on decomposition in a neotropical rainforest.

Plant litter diversity effects on decomposition rates are frequently reported, but with a strong bias towards temperate ecosystems. Altered decomposition and nutrient recycling with changing litter diversity may be particularly important in tree species-rich tropical rainforests on nutrient-poor soils. Using 28 different mixtures of leaf litter from 16 Amazonian rainforest tree species, we tested the hypothesis that litter mixture effects on decomposition increase with increasing functional litter diversity. Litter mixtures and all single litter species were exposed in the field for 9 months using custom-made microcosms with soil fauna access. In order to test the hypothesis that the long-term presence of tree species contributing to the litter mixtures increases mixture effects on decomposition, microcosms were installed in a plantation at sites including the respective tree species composition and in a nearby natural forest where these tree species are absent. We found that mixture decomposition deviated from predictions based on single species, with predominantly synergistic effects. Functional litter diversity, defined as either richness, evenness, or divergence based on a wide range of chemical traits, did not explain the observed litter mixture effects. However, synergistic effects in litter mixtures increased with the long-term presence of tree species contributing to these mixtures as the home field advantage hypothesis assumes. Our data suggest that complementarity effects on mixed litter decomposition may emerge through long-term interactions between aboveground and belowground biota.