Tank formation transforms nitrogen metabolism of an epiphytic bromeliad and its phyllosphere bacteria.

PREMISE: Up to half of tropical forest plant species grow on other plants. Lacking access to soils, vascular epiphytes have unique adaptations for mineral nutrition. Among the most distinctive is the tank growth form of certain large bromeliads, which absorb nutrients that are cycled by complex microbial communities in water trapped among their overlapping leaf bases. However, tanks form only after years of growth by juvenile plants, which must acquire nutrients differently. Understanding how nutrient dynamics change during tank bromeliad development can provide key insights into the role of microorganisms in the maintenance of tropical forest biodiversity. METHODS: We evaluated variations in plant morphology, growth, foliar nitrogen physiology, and phyllosphere bacterial communities along a size gradient spanning the transition to tank formation in the threatened species Tillandsia utriculata. RESULTS: Sequential morphological and growth phases coincided with the transition to tank formation when the longest leaf on plants was between 14 and 19 cm. Before this point, foliar ammonium concentrations were very high, but after, leaf segments absorbed significantly more nitrate. Leaf-surface bacterial communities tracked ontogenetic changes in plant morphology and nitrogen metabolism, with less-diverse communities in tankless plants distinguished by a high proportion of taxa implicated in ureolysis, nitrogen fixation, and methanotrophy, whereas nitrate reduction characterized communities on individuals that could form a tank. CONCLUSIONS: Coupled changes in plant morphology, physiology, and microbiome function facilitate the transition between alternative nutritional modes in tank bromeliads. Comparing bromeliads across life stages and habitats may illuminate how nitrogen-use varies across scales.

A trait-based understanding of wood decomposition by fungi.

As the primary decomposers of organic material in terrestrial ecosystems, fungi are critical agents of the global carbon cycle. Yet our ability to link fungal community composition to ecosystem functioning is constrained by a limited understanding of the factors accounting for different wood decomposition rates among fungi. Here we examine which traits best explain fungal decomposition ability by combining detailed trait-based assays on 34 saprotrophic fungi from across North America in the laboratory with a 5-y field study comprising 1,582 fungi isolated from 74 decomposing logs. Fungal growth rate (hyphal extension rate) was the strongest single predictor of fungal-mediated wood decomposition rate under laboratory conditions, and accounted for up to 27% of the in situ variation in decomposition in the field. At the individual level, decomposition rate was negatively correlated with moisture niche width (an indicator of drought stress tolerance) and with the production of nutrient-mineralizing extracellular enzymes. Together, these results suggest that decomposition rates strongly align with a dominance-tolerance life-history trade-off that was previously identified in these isolates, forming a spectrum from slow-growing, stress-tolerant fungi that are poor decomposers to fast-growing, highly competitive fungi with fast decomposition rates. Our study illustrates how an understanding of fungal trait variation could improve our predictive ability of the early and midstages of wood decay, to which our findings are most applicable. By mapping our results onto the biogeographic distribution of the dominance-tolerance trade-off across North America, we approximate broad-scale patterns in intrinsic fungal-mediated wood decomposition rates.

Wood construction more strongly shapes deadwood microbial communities than spatial location over 5 years of decay.

Diverse communities of fungi and bacteria in deadwood mediate wood decay. While rates of decomposition vary greatly among woody species and spatially distinct habitats, the relative importance of these factors in structuring microbial communities and whether these shift over time remains largely unknown. We characterized fungal and bacterial diversity within pieces of deadwood that experienced 6.3-98.8% mass loss while decaying in common garden 'rotplots' in a temperate oak-hickory forest in the Ozark Highlands, MO, USA. Communities were isolated from 21 woody species that had been decomposing for 1-5 years in spatially distinct habitats at the landscape scale (top and bottom of watersheds) and within stems (top and bottom of stems). Microbial community structure varied more strongly with wood traits than with spatial locations, mirroring the relative role of these factors on decay rates on the same pieces of wood even after 5 years. Co-occurring fungal and bacterial communities persistently influenced one another independently from their shared environmental conditions. However, the relative influence of wood construction versus spatial locations differed between fungi and bacteria, suggesting that life history characteristics of these clades structure diversity differently across space and time in decomposing wood.

Accurate forest projections require long-term wood decay experiments because plant trait effects change through time.

Whether global change will drive changing forests from net carbon (C) sinks to sources relates to how quickly deadwood decomposes. Because complete wood mineralization takes years, most experiments focus on how traits, environments and decomposer communities interact as wood decay begins. Few experiments last long enough to test whether drivers change with decay rates through time, with unknown consequences for scaling short-term results up to long-term forest ecosystem projections. Using a 7 year experiment that captured complete mineralization among 21 temperate tree species, we demonstrate that trait effects fade with advancing decay. However, wood density and vessel diameter, which may influence permeability, control how decay rates change through time. Denser wood loses mass more slowly at first but more quickly with advancing decay, which resolves ambiguity about the after-life consequences of this key plant functional trait by demonstrating that its effect on decay depends on experiment duration and sampling frequency. Only long-term data and a time-varying model yielded accurate predictions of both mass loss in a concurrent experiment and naturally recruited deadwood structure in a 32-year-old forest plot. Given the importance of forests in the carbon cycle, and the pivotal role for wood decay, accurate ecosystem projections are critical and they require experiments that go beyond enumerating potential mechanisms by identifying the temporal scale for their effects.

Mutualism Persistence and Abandonment during the Evolution of the Mycorrhizal Symbiosis.

Mutualistic symbioses with mycorrhizal fungi are widespread in plants. The majority of plant species associate with arbuscular mycorrhizal (AM) fungi. By contrast, the minority associate with ectomycorrhizal (EM) fungi, have abandoned the symbiosis and are nonmycorrhizal (NM), or engage in an intermediate, weakly AM symbiosis (AMNM). To understand the processes that maintain the mycorrhizal symbiosis or cause its loss, we reconstructed its evolution using a ∼3,000-species seed plant phylogeny integrated with mycorrhizal state information. Reconstruction indicated that the common ancestor of seed plants most likely associated with AM fungi and that the EM, NM, and AMNM states descended from the AM state. Direct transitions from the AM state to the EM and NM states were infrequent and generally irreversible, implying that natural selection or genetic constraint could promote stasis once a particular state evolved. However, the evolution of the NM state was more frequent via an indirect pathway through the AMNM state, suggesting that weakening of the AM symbiosis is a necessary precursor to mutualism abandonment. Nevertheless, reversions from the AMNM state back to the AM state were an order of magnitude more likely than transitions to the NM state, suggesting that natural selection favors the AM symbiosis over mutualism abandonment.

Selective logging: do rates of forest turnover in stems, species composition and functional traits decrease with time since disturbance? - A 45 year perspective.

Selective logging, the targeted harvesting of timber trees in a single cutting cycle, is globally rising in extent and intensity. Short-term impacts of selective logging on tropical forests have been widely investigated, but long-term effects on temporal dynamics of forest structure and composition are largely unknown. Understanding these long-term dynamics will help determine whether tropical forests are resilient to selective logging and inform choices between competing demands of anthropogenic use versus conservation of tropical forests. Forest dynamics can be studied within the framework of succession theory, which predicts that temporal turnover rates should decline with time since disturbance. Here, we investigated the temporal dynamics of a tropical forest in Kibale National Park, Uganda over 45 years following selective logging. We estimated turnover rates in stems, species composition, and functional traits (wood density and diameter at breast height), using observations from four censuses in 1989, 1999, 2006, and 2013, of stems ≥ 10 cm diameter within 17 unlogged and 9 logged 200 × 10 m vegetation plots. We used null models to account for interdependencies among turnover rates in stems, species composition, and functional traits. We tested predictions that turnover rates should be higher and decrease with increasing time since the selective logging event in logged forest, but should be less temporally variable in unlogged forest. Overall, we found higher turnover rates in logged forest for all three attributes, but turnover rates did not decline through time in logged forest and was not less temporally variable in unlogged forest. These results indicate that successional models that assume recovery to pre-disturbance conditions are inadequate for predicting the effects of selective logging on the dynamics of the tropical forest in Kibale. Selective logging resulted in persistently higher turnover rates, which may compromise the carbon storage capacity of Kibale's forest. Selective logging effects may also interact with effects from other global trends, potentially causing major long-term shifts in the dynamics of tropical forests. Similar studies in tropical forests elsewhere will help determine the generality of these conclusions. Ultimately, the view that selective logging is a benign approach to the management of tropical forests should be reconsidered in the light of studies of the effects of this practice on long-term forest dynamics.

Responses to historical climate change identify contemporary threats to diversity in Dodecatheon.

Anthropogenic climate change may threaten many species with extinction. However, species at risk today survived global climate change in recent geological history. Describing how habitat tracking and adaptation allowed species to survive warming since the end of the Pleistocene can indicate the relative importance of dispersal and natural selection during climate change. By taking this historical perspective, we can identify how contemporary climate change could interfere with these mechanisms and threaten the most vulnerable species. We focused on a group of closely related plant species in the genus Dodecatheon (Primulaceae) in eastern North America. Two rare species (Dodecatheon amethystinum and Dodecatheon frenchii) that are endemic to patchy cool cliffs may be glacial relicts whose ranges constricted following the last glacial maximum. Alternatively, these species may be extreme ecotypes of a single widespread species (Dodecatheon meadia) that quickly adapted to microclimatic differences among habitats. We test support for these alternative scenarios by combining ecophysiological and population genetic data at a regional scale. An important ecophysiological trait distinguishes rare species from D. meadia, but only a few northern populations of D. amethystinum are genetically distinctive. These relict populations indicate that habitat tracking did occur with historical climate change. However, relatively stronger evidence for isolation by distance and admixture suggests that local adaptation and genetic introgression have been at least as important. The complex response of Dodecatheon to historical climate change suggests that contemporary conservation efforts should accommodate evolutionary processes, in some cases by restoring genetic connectivity between ecologically differentiated populations.

Understanding how an amphicarpic species with a mixed mating system responds to fire: a population genetic approach.

Amphicarpic plants produce both above-ground and below-ground seeds. Because below-ground seeds are protected in the soil and may maintain viability when above-ground conditions are stressful, they were proposed as an adaptation to recolonize a site after disturbance. However, whether below-ground seeds are the main colonizers after a disturbance remains unknown. Our goal was to understand whether recolonization by an amphicarpic species after fire was accomplished primarily through germination of seeds produced above-ground or below-ground. We investigated Polygala lewtonii, an amphicarpic, perennial species endemic to fire-prone Florida sandhill and scrub, where fire kills plants but subsequently increases recruitment and population sizes. Polygala lewtonii produces three flower types: above-ground chasmogamous flowers and above-ground and below-ground cleistogamous flowers, with previous research demonstrating chasmogamous flowers produce a much greater proportion of seeds than cleistogamous flowers. We quantified outcrossing in seeds produced by chasmogamous flowers to determine whether it differed from the 100 % self-fertilized below-ground seeds. Approximately 25 % of seeds from chasmogamous flowers showed evidence of cross-pollination. Assuming that chasmogamous flowers produce the majority of the above-ground seeds, as was shown previously, this indicates it is possible to differentiate between germination by above-ground versus below-ground seeds in post-fire colonization. We next compared genetic diversity, admixture, inbreeding and population genetic structure pre- and post-fire. If fire promoted germination of chasmogamous seeds, heterozygosity and admixture would increase, and genetic structure and inbreeding would decrease. Instead, inbreeding and genetic structure increased and admixture decreased, suggesting that the below-ground selfed seeds (with limited dispersal ability) increased their contribution to the population after fire, possibly because fire reduced above-ground seed viability. Additionally, new alleles not found previously in range-wide analyses emerged from the seed bank post-fire. These results suggest that amphicarpy is a powerful adaptation to preserve genetic variation, maintain adaptive potential and promote rapid post-fire colonization.

Extraction and Purification of DNA from Wood at Various Stages of Decay for Metabarcoding of Wood-Associated Fungi.

Assessment of endophytic and saprotrophic microbial communities from wood-extracted DNA presents challenges due to the presence of surface microbes that contaminate samples and plant compounds that act as inhibiting agents. Here, we describe a method for decontaminating, sampling, and processing wood at various stages of decay for high-throughput extraction and purification of DNA.

Good neighbors aplenty: fungal endophytes rarely exhibit competitive exclusion patterns across a span of woody habitats.

Environmental forces and biotic interactions, both positive and negative, structure ecological communities, but their relative roles remain obscure despite strong theory. For instance, ecologically similar species, based on the principle of limiting similarity, are expected to be most competitive and show negative interactions. Specious communities that assemble along broad environmental gradients afford the most power to test theory, but the communities often are difficult to quantify. Microbes, specifically fungal endophytes of wood, are especially suited for testing community assembly theory because they are relatively easy to sample across a comprehensive range of environmental space with clear axes of variation. Moreover, endophytes mediate key forest carbon cycle processes, and although saprophytic fungi from dead wood typically compete, endophytic fungi in living wood may enhance success through cooperative symbioses. To classify interactions within endophyte communities, we analyzed fungal DNA barcode variation across 22 woody plant species growing in woodlands near Richmond, New South Wales, Australia. We estimated the response of endophytes to the measured wood environment (i.e., 11 anatomical and chemical wood traits) and each other using latent-variable models and identified recurrent communities across wood environments using model-based classification. We used this information to evaluate whether (1) co-occurrence patterns are consistent with strong competitive exclusion, and (2) a priori classifications by trophic mode and phylum distinguish taxa that are more likely to have positive vs. negative associations under the principle of limiting similarity. Fungal endophytes were diverse (mean = 140 taxa/sample), with differences in community composition structured by wood traits. Variation in wood water content and carbon concentration were associated with especially large community shifts. Surprisingly, after accounting for wood traits, fungal species were still more than three times more likely to have positive than negative co-occurrence patterns. That is, patterns consistent with strong competitive exclusion were rare, and positive interactions among fungal endophytes were more common than expected. Confirming the frequency of positive vs. negative interactions among fungal taxa requires experimental tests, and our findings establish clear paths for further study. Evidence to date intriguingly suggests that, across a wide range of wood traits, cooperation may outweigh combat for these fungi.

When a tree falls: Controls on wood decay predict standing dead tree fall and new risks in changing forests.

When standing dead trees (snags) fall, they have major impacts on forest ecosystems. Snag fall can redistribute wildlife habitat and impact public safety, while governing important carbon (C) cycle consequences of tree mortality because ground contact accelerates C emissions during deadwood decay. Managing the consequences of altered snag dynamics in changing forests requires predicting when snags fall as wood decay erodes mechanical resistance to breaking forces. Previous studies have pointed to common predictors, such as stem size, degree of decay and species identity, but few have assessed the relative strength of underlying mechanisms driving snag fall across biomes. Here, we analyze nearly 100,000 repeated snag observations from boreal to subtropical forests across the eastern United States to show that wood decay controls snag fall in ways that could generate previously unrecognized forest-climate feedback. Warmer locations where wood decays quickly had much faster rates of snag fall. The effect of temperature on snag fall was so strong that in a simple forest C model, anticipated warming by mid-century reduced snag C by 22%. Furthermore, species-level differences in wood decay resistance (durability) accurately predicted the timing of snag fall. Differences in half-life for standing dead trees were similar to expected differences in the service lifetimes of wooden structures built from their timber. Strong effects of temperature and wood durability imply future forests where dying trees fall and decay faster than at present, reducing terrestrial C storage and snag-dependent wildlife habitat. These results can improve the representation of forest C cycling and assist forest managers by helping predict when a dead tree may fall.

Ecological correlates of risk and incidence of West Nile virus in the United States.

West Nile virus, which was recently introduced to North America, is a mosquito-borne pathogen that infects a wide range of vertebrate hosts, including humans. Several species of birds appear to be the primary reservoir hosts, whereas other bird species, as well as other vertebrate species, can be infected but are less competent reservoirs. One hypothesis regarding the transmission dynamics of West Nile virus suggests that high bird diversity reduces West Nile virus transmission because mosquito blood-meals are distributed across a wide range of bird species, many of which have low reservoir competence. One mechanism by which this hypothesis can operate is that high-diversity bird communities might have lower community-competence, defined as the sum of the product of each species' abundance and its reservoir competence index value. Additional hypotheses posit that West Nile virus transmission will be reduced when either: (1) abundance of mosquito vectors is low; or (2) human population density is low. We assessed these hypotheses at two spatial scales: a regional scale near Saint Louis, MO, and a national scale (continental USA). We found that prevalence of West Nile virus infection in mosquito vectors and in humans increased with decreasing bird diversity and with increasing reservoir competence of the bird community. Our results suggest that conservation of avian diversity might help ameliorate the current West Nile virus epidemic in the USA.