Elevation alters ecosystem properties across temperate treelines globally.

Temperature is a primary driver of the distribution of biodiversity as well as of ecosystem boundaries. Declining temperature with increasing elevation in montane systems has long been recognized as a major factor shaping plant community biodiversity, metabolic processes, and ecosystem dynamics. Elevational gradients, as thermoclines, also enable prediction of long-term ecological responses to climate warming. One of the most striking manifestations of increasing elevation is the abrupt transitions from forest to treeless alpine tundra. However, whether there are globally consistent above- and belowground responses to these transitions remains an open question. To disentangle the direct and indirect effects of temperature on ecosystem properties, here we evaluate replicate treeline ecotones in seven temperate regions of the world. We find that declining temperatures with increasing elevation did not affect tree leaf nutrient concentrations, but did reduce ground-layer community-weighted plant nitrogen, leading to the strong stoichiometric convergence of ground-layer plant community nitrogen to phosphorus ratios across all regions. Further, elevation-driven changes in plant nutrients were associated with changes in soil organic matter content and quality (carbon to nitrogen ratios) and microbial properties. Combined, our identification of direct and indirect temperature controls over plant communities and soil properties in seven contrasting regions suggests that future warming may disrupt the functional properties of montane ecosystems, particularly where plant community reorganization outpaces treeline advance.

Plant responses to fertilization experiments in lowland, species-rich, tropical forests.

We present a meta-analysis of plant responses to fertilization experiments conducted in lowland, species-rich, tropical forests. We also update a key result and present the first species-level analyses of tree growth rates for a 15-yr factorial nitrogen (N), phosphorus (P), and potassium (K) experiment conducted in central Panama. The update concerns community-level tree growth rates, which responded significantly to the addition of N and K together after 10 yr of fertilization but not after 15 yr. Our experimental soils are infertile for the region, and species whose regional distributions are strongly associated with low soil P availability dominate the local tree flora. Under these circumstances, we expect muted responses to fertilization, and we predicted species associated with low-P soils would respond most slowly. The data did not support this prediction, species-level tree growth responses to P addition were unrelated to species-level soil P associations. The meta-analysis demonstrated that nutrient limitation is widespread in lowland tropical forests and evaluated two directional hypotheses concerning plant responses to N addition and to P addition. The meta-analysis supported the hypothesis that tree (or biomass) growth rate responses to fertilization are weaker in old growth forests and stronger in secondary forests, where rapid biomass accumulation provides a nutrient sink. The meta-analysis found no support for the long-standing hypothesis that plant responses are stronger for P addition and weaker for N addition. We do not advocate discarding the latter hypothesis. There are only 14 fertilization experiments from lowland, species-rich, tropical forests, 13 of the 14 experiments added nutrients for five or fewer years, and responses vary widely among experiments. Potential fertilization responses should be muted when the species present are well adapted to nutrient-poor soils, as is the case in our experiment, and when pest pressure increases with fertilization, as it does in our experiment. The statistical power and especially the duration of fertilization experiments conducted in old growth, tropical forests might be insufficient to detect the slow, modest growth responses that are to be expected.

Plasticity in nitrogen uptake among plant species with contrasting nutrient acquisition strategies in a tropical forest.

Nitrogen (N) availability influences the productivity and distribution of plants in tropical montane forests. Strategies to acquire soil N, such as direct uptake of organic compounds or associations with root symbionts to enhance N acquisition in exchange for carbon (C), may facilitate plant species coexistence and ecosystem N retention. Alternatively, rapid microbial turnover of soil N forms in tropical soils might promote flexible plant N-uptake strategies and mediate species coexistence. We tested whether sympatric plant species with different root symbiont associations, and therefore potentially different nutrient acquisition strategies, partition chemical forms of N or show plasticity in N uptake in a tropical pre-montane forest in Panama. We traced the movement of three 15 N forms into soil pools, microbes, and seedlings of eleven species differing in root traits. Seedlings were grown in a split-plot field transplant experiment, with plots receiving equimolar mixtures of ammonium, nitrate, and glycine, with one form isotopically labeled in each block. After 48 h, more 15 N was recovered in microbes than in plants, while all pools (extractable organic and inorganic N, microbial biomass, and leaves) contained greater amounts of 15 N from nitrate than from ammonium or glycine. Furthermore, 13 C from dual-labeled glycine was not recovered in the leaves of any seedling, suggesting the studied species do not directly take up organic N or transform organic N prior to translocation to leaves. Nitrogen uptake differed by root symbiont group only for nitrate, with greater 15 N recovery in plants with arbuscular mycorrhizal (AM) associations or proteoid roots compared to orchids. Some root trait groups differed in 15 N recovery among N forms, with greater nitrate uptake than ammonium or glycine by AM-associated and N2 -fixing plants. However, only five of eleven species showed differences in uptake among N forms. These results indicate flexibility in uptake of N forms in tropical plants across root trait groups, with only a few species displaying weak preferences for a specific N form.

Ectomycorrhizal impacts on plant nitrogen nutrition: emerging isotopic patterns, latitudinal variation and hidden mechanisms.

Ectomycorrhizal (EcM)-mediated nitrogen (N) acquisition is one main strategy used by terrestrial plants to facilitate growth. Measurements of natural abundance nitrogen isotope ratios (denoted as δ(15)N relative to a standard) increasingly serve as integrative proxies for mycorrhiza-mediated N acquisition due to biological fractionation processes that alter (15)N:(14)N ratios. Current understanding of these processes is based on studies from high-latitude ecosystems where plant productivity is largely limited by N availability. Much less is known about the cause and utility of ecosystem δ(15)N patterns in the tropics. Using structural equation models, model selection and isotope mass balance we assessed relationships among co-occurring soil, mycorrhizal plants and fungal N pools measured from 40 high- and 9 low-latitude ecosystems. At low latitudes (15)N-enrichment caused ecosystem components to significantly deviate from those in higher latitudes. Collectively, δ(15)N patterns suggested reduced N-dependency and unique sources of EcM (15)N-enrichment under conditions of high N availability typical of the tropics. Understanding the role of mycorrhizae in global N cycles will require reevaluation of high-latitude perspectives on fractionation sources that structure ecosystem δ(15)N patterns, as well as better integration of EcM function with biogeochemical theories pertaining to climate-nutrient cycling relationships.

Comparing High-throughput Platforms for Sequencing the V4 Region of SSU-rDNA in Environmental Microbial Eukaryotic Diversity Surveys.

High-throughput sequencing platforms are continuing to increase resulting read lengths, which is allowing for a deeper and more accurate depiction of environmental microbial diversity. With the nascent Reagent Kit v3, Illumina MiSeq now has the ability to sequence the eukaryotic hyper-variable V4 region of the SSU-rDNA locus with paired-end reads. Using DNA collected from soils with analyses of strictly- and nearly identical amplicons, here we ask how the new Illumina MiSeq data compares with what we can obtain with Roche/454 GS FLX with regard to quantity and quality, presence and absence, and abundance perspectives. We show that there is an easy qualitative transition from the Roche/454 to the Illumina MiSeq platforms. The ease of this transition is more nuanced quantitatively for low-abundant amplicons, although estimates of abundances are known to also vary within platforms.

A systematic, morphological and ecological overview of the Clavariaceae (Agaricales).

The Clavariaceae is a diverse family of mushroom-forming fungi composed of species that produce simple clubs, coralloid, lamellate-stipitate, hydnoid and resupinate sporocarps. Here we present a systematic and ecological overview of the Clavariaceae based on phylogenetic analysis of sequences of the nuclear large subunit ribosomal RNA (nLSU), including nine from type collections. Forty-seven sequences from sporocarps of diverse taxa across the Clavariaceae were merged with 243 environmental sequences from GenBank and analyzed phylogenetically to determine major clades within the family. Four major clades or lineages were recovered: (i) Mucronella, (ii) Ramariopsis-Clavulinopsis, (iii) Hyphodontiella and (iv) Clavaria-Camarophyllopsis-Clavicorona. Clavaria is paraphyletic, within which the lamellate and pileate-stipitate genus Camarophyllopsis is derived and composed of two independent lineages. The monotypic genus Clavicorona also appears nested within Clavaria. The monophyly of Clavaria and Camarophyllopsis, however, cannot be statistically rejected. We compared differing classification schemes for the genera Ramariopsis and Clavulinopsis, most of which are inconsistent with the molecular phylogeny and are statistically rejected. Scytinopogon, a genus classified in the Clavariaceae by several authors, shares phylogenetic affinities with the Trechisporales. Overall 126 molecular operational taxonomic units can be recognized in the Clavariaceae, roughly half of which are known only from environmental sequences, an estimate that exceeds the known number of species in the family. Stable isotope ratios of carbon and nitrogen were measured from specimens representing most major phylogenetic lineages to predict trophic strategies. These results suggest that most non-lignicolous species feature a biotrophic mode of nutrition. Ancestral state reconstruction analysis highlights the taxonomic significance of at least nine morphological traits at various depths in the family tree.

Elucidating the nutritional dynamics of fungi using stable isotopes.

Mycorrhizal and saprotrophic (SAP) fungi are essential to terrestrial element cycling due to their uptake of mineral nutrients and decomposition of detritus. Linking these ecological roles to specific fungi is necessary to improve our understanding of global nutrient cycling, fungal ecophysiology, and forest ecology. Using discriminant analyses of nitrogen (delta(15)N) and carbon (delta(13)C) isotope values from 813 fungi across 23 sites, we verified collector-based categorizations as either ectomycorrhizal (ECM) or SAP in > 91% of the fungi, and provided probabilistic assignments for an additional 27 fungi of unknown ecological role. As sites ranged from boreal tundra to tropical rainforest, we were able to show that fungal delta(13)C (26 sites) and delta(15)N (32 sites) values could be predicted by climate or latitude as previously shown in plant and soil analyses. Fungal delta(13)C values are likely reflecting differences in C-source between ECM and SAP fungi, whereas (15)N enrichment of ECM fungi relative to SAP fungi suggests that ECM fungi are consistently delivering (15)N depleted N to host trees across a range of ecosystem types.

New species of Boletellus from Guyana.

Boletellus exiguus sp. nov. and Boletellus dicymbophilus sp. nov. (Boletaceae, Boletales, Basidiomycota) are described as new to science. These boletes were collected from tropical forests dominated by ectomycorrhizal Dicymbe corymbosa (Caesalpiniaceae) in the Pakaraima Mountains of western Guyana.

Patchy field sampling biases understanding of climate change impacts across the Arctic.

Effective societal responses to rapid climate change in the Arctic rely on an accurate representation of region-specific ecosystem properties and processes. However, this is limited by the scarcity and patchy distribution of field measurements. Here, we use a comprehensive, geo-referenced database of primary field measurements in 1,840 published studies across the Arctic to identify statistically significant spatial biases in field sampling and study citation across this globally important region. We find that 31% of all study citations are derived from sites located within 50 km of just two research sites: Toolik Lake in the USA and Abisko in Sweden. Furthermore, relatively colder, more rapidly warming and sparsely vegetated sites are under-sampled and under-recognized in terms of citations, particularly among microbiology-related studies. The poorly sampled and cited areas, mainly in the Canadian high-Arctic archipelago and the Arctic coastline of Russia, constitute a large fraction of the Arctic ice-free land area. Our results suggest that the current pattern of sampling and citation may bias the scientific consensuses that underpin attempts to accurately predict and effectively mitigate climate change in the region. Further work is required to increase both the quality and quantity of sampling, and incorporate existing literature from poorly cited areas to generate a more representative picture of Arctic climate change and its environmental impacts.

Yeasts dominate soil fungal communities in three lowland Neotropical rainforests.

Forest soils typically harbour a vast diversity of fungi, but are usually dominated by filamentous (hyphae-forming) taxa. Compared to temperate and boreal forests, though, we have limited knowledge about the fungal diversity in tropical rainforest soils. Here we show, by environmental metabarcoding of soil samples collected in three Neotropical rainforests, that Yeasts dominate the fungal communities in terms of the number of sequencing reads and OTUs. These unicellular forms are commonly found in aquatic environments, and their hyperdiversity may be the result of frequent inundation combined with numerous aquatic microenvironments in these rainforests. Other fungi that are frequent in aquatic environments, such as the abundant Chytridiomycotina, were also detected. While there was low similarity in OTU composition within and between the three rainforests, the fungal communities in Central America were more similar to each other than the communities in South America, reflecting a general biogeographic pattern also seen in animals, plants and protists.

Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests.

High animal and plant richness in tropical rainforest communities has long intrigued naturalists. It is unknown if similar hyperdiversity patterns are reflected at the microbial scale with unicellular eukaryotes (protists). Here we show, using environmental metabarcoding of soil samples and a phylogeny-aware cleaning step, that protist communities in Neotropical rainforests are hyperdiverse and dominated by the parasitic Apicomplexa, which infect arthropods and other animals. These host-specific parasites potentially contribute to the high animal diversity in the forests by reducing population growth in a density-dependent manner. By contrast, too few operational taxonomic units (OTUs) of Oomycota were found to broadly drive high tropical tree diversity in a host-specific manner under the Janzen-Connell model. Extremely high OTU diversity and high heterogeneity between samples within the same forests suggest that protists, not arthropods, are the most diverse eukaryotes in tropical rainforests. Our data show that protists play a large role in tropical terrestrial ecosystems long viewed as being dominated by macroorganisms.

Convergence of soil nitrogen isotopes across global climate gradients.

Quantifying global patterns of terrestrial nitrogen (N) cycling is central to predicting future patterns of primary productivity, carbon sequestration, nutrient fluxes to aquatic systems, and climate forcing. With limited direct measures of soil N cycling at the global scale, syntheses of the (15)N:(14)N ratio of soil organic matter across climate gradients provide key insights into understanding global patterns of N cycling. In synthesizing data from over 6000 soil samples, we show strong global relationships among soil N isotopes, mean annual temperature (MAT), mean annual precipitation (MAP), and the concentrations of organic carbon and clay in soil. In both hot ecosystems and dry ecosystems, soil organic matter was more enriched in (15)N than in corresponding cold ecosystems or wet ecosystems. Below a MAT of 9.8°C, soil δ(15)N was invariant with MAT. At the global scale, soil organic C concentrations also declined with increasing MAT and decreasing MAP. After standardizing for variation among mineral soils in soil C and clay concentrations, soil δ(15)N showed no consistent trends across global climate and latitudinal gradients. Our analyses could place new constraints on interpretations of patterns of ecosystem N cycling and global budgets of gaseous N loss.

Fungal biogeography. Global diversity and geography of soil fungi.

Fungi play major roles in ecosystem processes, but the determinants of fungal diversity and biogeographic patterns remain poorly understood. Using DNA metabarcoding data from hundreds of globally distributed soil samples, we demonstrate that fungal richness is decoupled from plant diversity. The plant-to-fungus richness ratio declines exponentially toward the poles. Climatic factors, followed by edaphic and spatial variables, constitute the best predictors of fungal richness and community composition at the global scale. Fungi show similar latitudinal diversity gradients to other organisms, with several notable exceptions. These findings advance our understanding of global fungal diversity patterns and permit integration of fungi into a general macroecological framework.

Do ectomycorrhizas alter leaf-litter decomposition in monodominant tropical forests of Guyana?

This work tested the hypothesis that ectomycorrhizas (EM) of Dicymbe corymbosa alter leaf-litter decomposition and residual litter quality in tropical forests of Guyana. Mass loss of leaf litter in litter bags was determined on three occasions, in two experiments, during a 12-month period. Paired root-exclusion plots were located randomly within a D. corymbosa forest. Both D. corymbosa and mixed-species leaf litters were reciprocally transplanted into their respective forest types. Elemental analysis was performed on the residual D. corymbosa leaf litter after 1 yr. Leaf litter mass loss in the D. corymbosa forest was not influenced by EM, despite high EM colonization. Elemental analysis of D. corymbosa leaf litter residues demonstrated reduced calcium levels in the presence of EM, which were negatively correlated with EM rootlet-colonizing mass. The lack of EM effect on the litter decomposition rate, coupled with high EM colonization, suggests an important but indirect role in mineral nutrient acquisition. Lowered Ca concentration in leaf litter exposed to EM may suggest a high Ca demand by the ectotroph system.

Mast fruiting and seedling survival of the ectomycorrhizal, monodominant Dicymbe corymbosa (Caesalpiniaceae) in Guyana.

In Guyana, we investigated seed output, and resulting seedling establishment and survival, during a 'mast' year, by the ectomycorrhizal, monodominant rainforest canopy tree Dicymbe corymbosa (Caesalpiniaceae), a species with high, synchronous seed production at intermittent years. By utilizing seed traps, the mast seed output, predation, carbon and mineral investment, and masting synchrony were quantified in 2003 in primary D. corymbosa forests. Establishment of seedling cohorts was monitored, and climatic conditions associated with masting were assessed. During 2003, D. corymbosa in the Pakaraima Mountains exhibited high, synchronous seed production with low dispersal and predation. Investment in reproductive biomass was large relative to that in other tropical forests. Recent D. corymbosa reproductive events followed El Nino-induced droughts, with little intervening seed production. Over 12 months, 40% of the 2003 seedling cohort survived. Our results suggest that D. corymbosa has a strongly bimodal fruiting pattern that allows the establishment of a large seedling bank, facilitating persistent monodominance. Resource investment in large seed crops may depend on mineral recycling via ectomycorrhizas, coupled with the reallocation of carbon from vegetative maintenance.