Acrogenospora terricola sp. nov., a fungal species associated with seeds of pioneer trees in the soil seed bank of a lowland forest in Panama.

As currently circumscribed, Acrogenospora (Acrogenosporaceae, Minutisphaerales, Dothideomycetes) is a genus of saprobic hyphomycetes with distinctive conidia. Although considered common and cosmopolitan, the genus is poorly represented by sequence data, and no neotropical representatives are present in public sequence databases. Consequently, Acrogenospora has been largely invisible to ecological studies that rely on sequence-based identification. As part of an effort to identify fungi collected during ecological studies, we identified strains of Acrogenospora isolated in culture from seeds in the soil seed bank of a lowland tropical forest in Panama. Here we describe Acrogenospora terricola sp. nov. based on morphological and phylogenetic analyses. We confirm that the genus has a pantropical distribution. The observation of Acrogenospora infecting seeds in a terrestrial environment contrasts with previously described species in the genus, most of which occur on decaying wood in freshwater environments. This work highlights the often hidden taxonomic value of collections derived from ecological studies of fungal communities and the ways in which rich sequence databases can shed light on the identity, distributions and diversity of cryptic microfungi.

Local canopy disturbance as an explanation for long-term increases in liana abundance.

Canopy disturbance explains liana abundance and distribution within tropical forests and thus may also explain the widespread pattern of increasing liana abundance; however, this hypothesis remains untested. We used a 10-year study (2007-2017) of 117,100 rooted lianas in an old-growth Panamanian forest to test whether local canopy disturbance explains increasing liana abundance. We found that liana density increased 29.2% and basal area 12.5%. The vast majority of these increases were associated with clonal stem proliferation following canopy disturbance, particularly in liana-dense, low-canopy gaps, which had far greater liana increases than did undisturbed forest. Lianas may be ecological niche constructors, arresting tree regeneration in gaps and thus creating a high-light environment that favours sustained liana proliferation. Our findings demonstrate that liana abundance is increasing rapidly and their ability to proliferate via copious clonal stem production in canopy gaps explains much of their increase in this and possibly other tropical forests.

Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest.

The Janzen-Connell (JC) hypothesis provides a conceptual framework for explaining the maintenance of tree diversity in tropical forests. Its central tenet-that recruits experience high mortality near conspecifics and at high densities-assumes a degree of host specialization in interactions between plants and natural enemies. Studies confirming JC effects have focused primarily on spatial distributions of seedlings and saplings, leaving major knowledge gaps regarding the fate of seeds in soil and the specificity of the soilborne fungi that are their most important antagonists. Here we use a common garden experiment in a lowland tropical forest in Panama to show that communities of seed-infecting fungi are structured predominantly by plant species, with only minor influences of factors such as local soil type, forest characteristics, or time in soil (1-12 months). Inoculation experiments confirmed that fungi affected seed viability and germination in a host-specific manner and that effects on seed viability preceded seedling emergence. Seeds are critical components of reproduction for tropical trees, and the factors influencing their persistence, survival, and germination shape the populations of seedlings and saplings on which current perspectives regarding forest dynamics are based. Together these findings bring seed dynamics to light in the context of the JC hypothesis, implicating them directly in the processes that have emerged as critical for diversity maintenance in species-rich tropical forests.

Dormancy-defense syndromes and tradeoffs between physical and chemical defenses in seeds of pioneer species.

Seeds of tropical pioneer trees have chemical and physical characteristics that determine their capacity to persist in the soil seed bank. These traits allow seeds to survive in the soil despite diverse predators and pathogens, and to germinate and recruit even decades after dispersal. Defenses in seedlings and adult plants often are described in terms of tradeoffs between chemical and physical defense, but the interplay of defensive strategies has been evaluated only rarely for seeds. Here we evaluated whether classes of seed defenses were negatively correlated across species (consistent with tradeoffs in defense strategies), or whether groups of traits formed associations across species (consistent with seed defense syndromes). Using 16 of the most common pioneer tree species in a neotropical lowland forest in Panama we investigated relationships among four physical traits (seed fracture resistance, seed coat thickness, seed permeability, and seed mass) and two chemical traits (number of phenolic compounds and phenolic peak area), and their association with seed persistence. In addition, seed toxicity was assessed with bioassays in which we evaluated the activity of seed extracts against representative fungal pathogens and a model invertebrate. We did not find univariate tradeoffs between chemical and physical defenses. Instead, we found that seed permeability - a trait that distinguishes physical dormancy from other dormancy types - was positively associated with chemical defense traits and negatively associated with physical defense traits. Using a linear discriminant analysis and a hierarchical cluster analysis we found evidence to distinguish three distinct seed defense syndromes that correspond directly with seed dormancy classes (i.e., quiescent, physical, and physiological). Our data suggest that short and long-term persistence of seeds can be achieved via two strategies: having permeable seeds that are well defended chemically, corresponding to the physiologically dormant defense syndrome; or having impermeable seeds that are well defended physically, corresponding to the physically dormant defense syndrome. In turn, transient seeds appear to have a lower degree of chemical and physical defenses, corresponding to the quiescent defense syndrome. Overall, we find that seed defense and seed dormancy are linked, suggesting that environmental pressures on seed persistence and for delayed germination can select for trait combinations defining distinct dormancy-defense syndromes.

No evidence that boron influences tree species distributions in lowland tropical forests of Panama.

It was recently proposed that boron might be the most important nutrient structuring tree species distributions in tropical forests. Here we combine observational and experimental studies to test this hypothesis for lowland tropical forests of Panama. Plant-available boron is uniformly low in tropical forest soils of Panama and is not significantly associated with any of the > 500 species in a regional network of forest dynamics plots. Experimental manipulation of boron supply to seedlings of three tropical tree species revealed no evidence of boron deficiency or toxicity at concentrations likely to occur in tropical forest soils. Foliar boron did not correlate with soil boron along a local scale gradient of boron availability. Fifteen years of boron addition to a tropical forest increased plant-available boron by 70% but did not significantly change tree productivity or boron concentrations in live leaves, wood or leaf litter. The annual input of boron in rainfall accounts for a considerable proportion of the boron in annual litterfall and is similar to the pool of plant-available boron in the soil, and is therefore sufficient to preclude boron deficiency. We conclude that boron does not influence tree species distributions in Panama and presumably elsewhere in the lowland tropics.

An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest.

Tropical forests are renowned for their high diversity, yet in many sites a single tree species accounts for the majority of the individuals in a stand. An explanation for these monodominant forests remains elusive, but may be linked to mycorrhizal symbioses. We tested three hypotheses by which ectomycorrhizas might facilitate the dominance of the tree, Oreomunnea mexicana, in montane tropical forest in Panama. We tested whether access to ectomycorrhizal networks improved growth and survival of seedlings, evaluated whether ectomycorrhizal fungi promote seedling growth via positive plant-soil feedback, and measured whether Oreomunnea reduced inorganic nitrogen availability. We found no evidence that Oreomunnea benefits from ectomycorrhizal networks or plant-soil feedback. However, we found three-fold higher soil nitrate and ammonium concentrations outside than inside Oreomunnea-dominated forest and a correlation between soil nitrate and Oreomunnea abundance in plots. Ectomycorrhizal effects on nitrogen cycling might therefore provide an explanation for the monodominance of ectomycorrhizal tree species worldwide.

Variation in wood nutrients along a tropical soil fertility gradient.

Wood contains the majority of the nutrients in tropical trees, yet controls over wood nutrient concentrations and their function are poorly understood. We measured wood nutrient concentrations in 106 tree species in 10 forest plots spanning a regional fertility gradient in Panama. For a subset of species, we quantified foliar nutrients and wood density to test whether wood nutrients scale with foliar nutrients at the species level, or wood nutrient storage increases with wood density as predicted by the wood economics spectrum. Wood nutrient concentrations varied enormously among species from fourfold in nitrogen (N) to > 30-fold in calcium (Ca), potassium (K), magnesium (Mg) and phosphorus (P). Community-weighted mean wood nutrient concentrations correlated positively with soil Ca, K, Mg and P concentrations. Wood nutrients scaled positively with leaf nutrients, supporting the hypothesis that nutrient allocation is conserved across plant organs. Wood P was most sensitive to variation in soil nutrient availability, and significant radial declines in wood P indicated that tropical trees retranslocate P as sapwood transitions to heartwood. Wood P decreased with increasing wood density, suggesting that low wood P and dense wood are traits associated with tree species persistence on low fertility soils. Substantial variation among species and communities in wood nutrient concentrations suggests that allocation of nutrients to wood, especially P, influences species distributions and nutrient dynamics in tropical forests.

Seedling growth responses to phosphorus reflect adult distribution patterns of tropical trees.

Soils influence tropical forest composition at regional scales. In Panama, data on tree communities and underlying soils indicate that species frequently show distributional associations to soil phosphorus. To understand how these associations arise, we combined a pot experiment to measure seedling responses of 15 pioneer species to phosphorus addition with an analysis of the phylogenetic structure of phosphorus associations of the entire tree community. Growth responses of pioneers to phosphorus addition revealed a clear tradeoff: species from high-phosphorus sites grew fastest in the phosphorus-addition treatment, while species from low-phosphorus sites grew fastest in the low-phosphorus treatment. Traits associated with growth performance remain unclear: biomass allocation, phosphatase activity and phosphorus-use efficiency did not correlate with phosphorus associations; however, phosphatase activity was most strongly down-regulated in response to phosphorus addition in species from high-phosphorus sites. Phylogenetic analysis indicated that pioneers occur more frequently in clades where phosphorus associations are overdispersed as compared with the overall tree community, suggesting that selection on phosphorus acquisition and use may be strongest for pioneer species with high phosphorus demand. Our results show that phosphorus-dependent growth rates provide an additional explanation for the regional distribution of tree species in Panama, and possibly elsewhere.

Two tropical conifers show strong growth and water-use efficiency responses to altered CO2 concentration.

BACKGROUND AND AIMS: Conifers dominated wet lowland tropical forests 100 million years ago (MYA). With a few exceptions in the Podocarpaceae and Araucariaceae, conifers are now absent from this biome. This shift to angiosperm dominance also coincided with a large decline in atmospheric CO2 concentration (ca). We compared growth and physiological performance of two lowland tropical angiosperms and conifers at ca levels representing pre-industrial (280 ppm), ambient (400 ppm) and Eocene (800 ppm) conditions to explore how differences in ca affect the growth and water-use efficiency (WUE) of seedlings from these groups. METHODS: Two conifers (Araucaria heterophylla and Podocarpus guatemalensis) and two angiosperm trees (Tabebuia rosea and Chrysophyllum cainito) were grown in climate-controlled glasshouses in Panama. Growth, photosynthetic rates, nutrient uptake, and nutrient use and water-use efficiencies were measured. KEY RESULTS: Podocarpus seedlings showed a stronger (66 %) increase in relative growth rate with increasing ca relative to Araucaria (19 %) and the angiosperms (no growth enhancement). The response of Podocarpus is consistent with expectations for species with conservative growth traits and low mesophyll diffusion conductance. While previous work has shown limited stomatal response of conifers to ca, we found that the two conifers had significantly greater increases in leaf and whole-plant WUE than the angiosperms, reflecting increased photosynthetic rate and reduced stomatal conductance. Foliar nitrogen isotope ratios (δ15N) and soil nitrate concentrations indicated a preference in Podocarpus for ammonium over nitrate, which may impact nitrogen uptake relative to nitrate assimilators under high ca SIGNIFICANCE: Podocarps colonized tropical forests after angiosperms achieved dominance and are now restricted to infertile soils. Although limited to a single species, our data suggest that higher ca may have been favourable for podocarp colonization of tropical South America 60 MYA, while plasticity in photosynthetic capacity and WUE may help account for their continued persistence under large changes in ca since the Eocene.

Variation in ectomycorrhizal fungal communities associated with Oreomunnea mexicana (Juglandaceae) in a Neotropical montane forest.

Neotropical montane forests are often dominated by ectomycorrhizal (EM) tree species, yet the diversity of their EM fungal communities remains poorly explored. In lower montane forests in western Panama, the EM tree species Oreomunnea mexicana (Juglandaceae) forms locally dense populations in forest otherwise characterized by trees that form arbuscular mycorrhizal (AM) associations. The objective of this study was to compare the composition of EM fungal communities associated with Oreomunnea adults, saplings, and seedlings across sites differing in soil fertility and the amount and seasonality of rainfall. Analysis of fungal nrITS DNA (nuclear ribosomal internal transcribed spacers) revealed 115 EM fungi taxa from 234 EM root tips collected from adults, saplings, and seedlings in four sites. EM fungal communities were equally species-rich and diverse across Oreomunnea developmental stages and sites, regardless of soil conditions or rainfall patterns. However, ordination analysis revealed high compositional turnover between low and high fertility/rainfall sites located ca. 6 km apart. The EM fungal community was dominated by Russula (ca. 36 taxa). Cortinarius, represented by 14 species and previously reported to extract nitrogen from organic sources under low nitrogen availability, was found only in low fertility/high rainfall sites. Phylogenetic diversity analyses of Russula revealed greater evolutionary distance among taxa found on sites with contrasting fertility and rainfall than was expected by chance, suggesting that environmental differences among sites may be important in structuring EM fungal communities. More research is needed to evaluate whether EM fungal taxa associated with Oreomunnea form mycorrhizal networks that might account for local dominance of this tree species in otherwise diverse forest communities.