Shifts in internal stem damage along a tropical precipitation gradient and implications for forest biomass estimation.

Woody biomass is a large carbon store in terrestrial ecosystems. In calculating biomass, tree stems are assumed to be solid structures. However, decomposer agents such as microbes and insects target stem heartwood, causing internal wood decay which is poorly quantified. We investigated internal stem damage across five sites in tropical Australia along a precipitation gradient. We estimated the amount of internal aboveground biomass damaged in living trees and measured four potential stem damage predictors: wood density, stem diameter, annual precipitation, and termite pressure (measured as termite damage in downed deadwood). Stem damage increased with increasing diameter, wood density, and termite pressure and decreased with increasing precipitation. High wood density stems sustained less damage in wet sites and more damage in dry sites, likely a result of shifting decomposer communities and their differing responses to changes in tree species and wood traits across sites. Incorporating stem damage reduced aboveground biomass estimates by > 30% in Australian savannas, compared to only 3% in rainforests. Accurate estimates of carbon storage across woody plant communities are critical for understanding the global carbon budget. Future biomass estimates should consider stem damage in concert with the effects of changes in decomposer communities and abiotic conditions.

The challenge of estimating global termite methane emissions.

Methane is a powerful greenhouse gas, more potent than carbon dioxide, and emitted from a variety of natural sources including wetlands, permafrost, mammalian guts and termites. As increases in global temperatures continue to break records, quantifying the magnitudes of key methane sources has never been more pertinent. Over the last 40 years, the contribution of termites to the global methane budget has been subject to much debate. The most recent estimates of termite emissions range between 9 and 15 Tg CH4 year-1, approximately 4% of emissions from natural sources (excluding wetlands). However, we argue that the current approach for estimating termite contributions to the global methane budget is flawed. Key parameters, namely termite methane emissions from soil, deadwood, living tree stems, epigeal mounds and arboreal nests, are largely ignored in global estimates. This omission occurs because data are lacking and research objectives, crucially, neglect variation in termite ecology. Furthermore, inconsistencies in data collection methods prohibit the pooling of data required to compute global estimates. Here, we summarise the advances made over the last 40 years and illustrate how different aspects of termite ecology can influence the termite contribution to global methane emissions. Additionally, we highlight technological advances that may help researchers investigate termite methane emissions on a larger scale. Finally, we consider dynamic feedback mechanisms of climate warming and land-use change on termite methane emissions. We conclude that ultimately the global contribution of termites to atmospheric methane remains unknown and thus present an alternative framework for estimating their emissions. To significantly improve estimates, we outline outstanding questions to guide future research efforts.

Symbiotic status alters fungal eco-evolutionary offspring trajectories.

Despite host-fungal symbiotic interactions being ubiquitous in all ecosystems, understanding how symbiosis has shaped the ecology and evolution of fungal spores that are involved in dispersal and colonization of their hosts has been ignored in life-history studies. We assembled a spore morphology database covering over 26,000 species of free-living to symbiotic fungi of plants, insects and humans and found more than eight orders of variation in spore size. Evolutionary transitions in symbiotic status correlated with shifts in spore size, but the strength of this effect varied widely among phyla. Symbiotic status explained more variation than climatic variables in the current distribution of spore sizes of plant-associated fungi at a global scale while the dispersal potential of their spores is more restricted compared to free-living fungi. Our work advances life-history theory by highlighting how the interaction between symbiosis and offspring morphology shapes the reproductive and dispersal strategies among living forms.

Beyond the usual climate? Factors determining flowering and fruiting phenology across a genus over 117 years.

PREMISE: Although changes in plant phenology are largely attributed to changes in climate, the roles of other factors such as genetic constraints, competition, and self-compatibility are underexplored. METHODS: We compiled >900 herbarium records spanning 117 years for all eight nominal species of the winter-annual genus Leavenworthia (Brassicaceae). We used linear regression to determine the rate of phenological change across years and phenological sensitivity to climate. Using a variance partitioning analysis, we assessed the relative influence of climatic and nonclimatic factors (self-compatibility, range overlap, latitude, and year) on Leavenworthia reproductive phenology. RESULTS: Flowering advanced by ~2.0 days and fruiting by ~1.3 days per decade. For every 1°C increase in spring temperature, flowering advanced ~2.3 days and fruiting ~3.3 days. For every 100 mm decrease in spring precipitation, each advanced ~6-7 days. The best models explained 35.4% of flowering variance and 33.9% of fruiting. Spring precipitation accounted for 51.3% of explained variance in flowering date and 44.6% in fruiting. Mean spring temperature accounted for 10.6% and 19.3%, respectively. Year accounted for 16.6% of flowering variance and 5.4% of fruiting, and latitude for 2.3% and 15.1%, respectively. Nonclimatic variables combined accounted for <11% of the variance across phenophases. CONCLUSIONS: Spring precipitation and other climate-related factors were dominant predictors of phenological variance. Our results emphasize the strong effect of precipitation on phenology, especially in the moisture-limited habitats preferred by Leavenworthia. Among the many factors that determine phenology, climate is the dominant influence, indicating that the effects of climate change on phenology are expected to increase.

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.

The global spectrum of plant form and function.

Earth is home to a remarkable diversity of plant forms and life histories, yet comparatively few essential trait combinations have proved evolutionarily viable in today's terrestrial biosphere. By analysing worldwide variation in six major traits critical to growth, survival and reproduction within the largest sample of vascular plant species ever compiled, we found that occupancy of six-dimensional trait space is strongly concentrated, indicating coordination and trade-offs. Three-quarters of trait variation is captured in a two-dimensional global spectrum of plant form and function. One major dimension within this plane reflects the size of whole plants and their parts; the other represents the leaf economics spectrum, which balances leaf construction costs against growth potential. The global plant trait spectrum provides a backdrop for elucidating constraints on evolution, for functionally qualifying species and ecosystems, and for improving models that predict future vegetation based on continuous variation in plant form and function.

Maternal effects shape the seed mycobiome in Quercus petraea.

The tree seed mycobiome has received little attention despite its potential role in forest regeneration and health. The aim of the present study was to analyze the processes shaping the composition of seed fungal communities in natural forests as seeds transition from the mother plant to the ground for establishment. We used metabarcoding approaches and confocal microscopy to analyze the fungal communities of seeds collected in the canopy and on the ground in four natural populations of sessile oak (Quercus petraea). Ecological processes shaping the seed mycobiome were inferred using joint species distribution models. Fungi were present in seed internal tissues, including the embryo. The seed mycobiome differed among oak populations and trees within the same population. Its composition was largely influenced by the mother, with weak significant environmental influences. The models also revealed several probable interactions among fungal pathogens and mycoparasites. Our results demonstrate that maternal effects, environmental filtering and biotic interactions all shape the seed mycobiome of sessile oak. They provide a starting point for future research aimed at understanding how maternal genes and environments interact to control the vertical transmission of fungal species that could then influence seed dispersal and germination, and seedling recruitment.

The evolutionary assembly of forest communities along environmental gradients: recent diversification or sorting of pre-adapted clades?

Recent studies have demonstrated that ecological processes that shape community structure and dynamics change along environmental gradients. However, much less is known about how the emergence of the gradients themselves shape the evolution of species that underlie community assembly. In this study, we address how the creation of novel environments leads to community assembly via two nonmutually exclusive processes: immigration and ecological sorting of pre-adapted clades (ISPC), and recent adaptive diversification (RAD). We study these processes in the context of the elevational gradient created by the uplift of the Central Andes. We develop a novel approach and method based on the decomposition of species turnover into within- and among-clade components, where clades correspond to lineages that originated before mountain uplift. Effects of ISPC and RAD can be inferred from how components of turnover change with elevation. We test our approach using data from over 500 Andean forest plots. We found that species turnover between communities at different elevations is dominated by the replacement of clades that originated before the uplift of the Central Andes. Our results suggest that immigration and sorting of clades pre-adapted to montane habitats is the primary mechanism shaping tree communities across elevations.

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.

Three keys to the radiation of angiosperms into freezing environments.

Early flowering plants are thought to have been woody species restricted to warm habitats. This lineage has since radiated into almost every climate, with manifold growth forms. As angiosperms spread and climate changed, they evolved mechanisms to cope with episodic freezing. To explore the evolution of traits underpinning the ability to persist in freezing conditions, we assembled a large species-level database of growth habit (woody or herbaceous; 49,064 species), as well as leaf phenology (evergreen or deciduous), diameter of hydraulic conduits (that is, xylem vessels and tracheids) and climate occupancies (exposure to freezing). To model the evolution of species' traits and climate occupancies, we combined these data with an unparalleled dated molecular phylogeny (32,223 species) for land plants. Here we show that woody clades successfully moved into freezing-prone environments by either possessing transport networks of small safe conduits and/or shutting down hydraulic function by dropping leaves during freezing. Herbaceous species largely avoided freezing periods by senescing cheaply constructed aboveground tissue. Growth habit has long been considered labile, but we find that growth habit was less labile than climate occupancy. Additionally, freezing environments were largely filled by lineages that had already become herbs or, when remaining woody, already had small conduits (that is, the trait evolved before the climate occupancy). By contrast, most deciduous woody lineages had an evolutionary shift to seasonally shedding their leaves only after exposure to freezing (that is, the climate occupancy evolved before the trait). For angiosperms to inhabit novel cold environments they had to gain new structural and functional trait solutions; our results suggest that many of these solutions were probably acquired before their foray into the cold.

Functional biogeography of angiosperms: life at the extremes.

Nonlinear relationships between species and their environments are believed common in ecology and evolution, including during angiosperms' rise to dominance. Early angiosperms are thought of as woody evergreens restricted to warm, wet habitats. They have since expanded into numerous cold and dry places. This expansion may have included transitions across important environmental thresholds. To understand linear and nonlinear relationships between angiosperm structure and biogeographic distributions, we integrated large datasets of growth habits, conduit sizes, leaf phenologies, evolutionary histories, and environmental limits. We consider current-day patterns and develop a new evolutionary model to investigate processes that created them. The macroecological pattern was clear: herbs had lower minimum temperature and precipitation limits. In woody species, conduit sizes were smaller in evergreens and related to species' minimum temperatures. Across evolutionary timescales, our new modeling approach found conduit sizes in deciduous species decreased linearly with minimum temperature limits. By contrast, evergreen species had a sigmoidal relationship with minimum temperature limits and an inflection overlapping freezing. These results suggest freezing represented an important threshold for evergreen but not deciduous woody angiosperms. Global success of angiosperms appears tied to a small set of alternative solutions when faced with a novel environmental threshold.

Global convergence in the vulnerability of forests to drought.

Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (<1 megapascal) hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk.

Linking wood traits to vital rates in tropical rainforest trees: Insights from comparing sapling and adult wood.

PREMISE OF THE STUDY: Wood density is the top predictor of growth and mortality rates (vital rates) but with modest explanatory power at best. Stronger links to vital rates are expected if wood density is decomposed into its anatomical properties at sapling and adult stages, since saplings and adults differ in wood traits and vital rates. We examined whether anatomical determinants of wood density and strength of the relationship between wood traits and vital rates shift between saplings and adults. METHODS: Using wood segments from near pith (sapling) and near bark (adult) for 20 tree species (three adults each) from Barro Colorado Island, Panama, we quantified wood traits. Vital rates for saplings and adults were obtained from an earlier study. KEY RESULTS: Anatomical predictors of wood density were similar for sapling and adult wood, with wood density variation largely explained by fiber lumen area and fiber wall fraction. In sapling wood only, growth rates decreased with fiber wall fraction and increased with fiber lumen area, while mortality rates increased with vessel area but decreased with fiber wall fraction and vessel density. CONCLUSIONS: Wood traits of sapling trees provide functional insight into the growth-mortality tradeoff. Sapling wood with relatively large fiber lumen area and wide vessels, enabling faster hydraulic transport but less mechanical strength, is associated with fast growth and high mortality. Sapling wood with relatively more fiber wall and many narrow vessels, enabling greater mechanical strength but slower hydraulic transport, is associated with slow growth and low mortality.

Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species.

The evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem conduits, thus impeding sap transport to the leaves. A well-known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water). We tested this safety-efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12%, 50% and 88% of maximal conductivity are lost. Although correlations between safety and efficiency were weak (r(2)  < 0.086), no species had high efficiency and high safety, supporting the idea for a safety-efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r(2)  < 0.02 in most cases) with higher wood density, lower leaf- to sapwood-area and shorter stature. There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.

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.

Radial variation in wood specific gravity of tropical tree species differing in growth-mortality strategies.

UNLABELLED: • PREMISE OF THE STUDY: Wood specific gravity (WSG) mediates an interspecific trade-off between growth and mortality and is a key measure for estimating carbon stocks. Most studies use species mean values to represent WSG, despite variation at different levels of biological organization. We examined sources of variation in WSG across four nested scales (segments within cores, cores within trees, trees within species, and species), compared the pattern of radial variation in WSG among species differing in growth strategies, and investigated the effect of WSG radial variation on aboveground biomass estimates.• METHODS: We took two perpendicular cores from six individuals each of 20 tropical tree species representing a broad range of mean WSGs and growth-mortality strategies in a lowland tropical moist forest in Panama. Cores were divided into 1-cm segments, and WSG was determined for each segment.• KEY RESULTS: The bulk of the total variance in WSG was dominated by interspecies variation (88%), whereas variation due to measurement error, segments within cores, and cores within trees (8%) was minimal. Radial variation in WSG, defined as change in WSG with increasing distance from the pith, was significant in 17 of the 20 species and included significant monotonic increases in 6 species and nonmonotonic patterns in 11 species. Radial variation in WSG resulted in a small but significant bias in aboveground biomass estimates.• CONCLUSIONS: Radial variation in WSG is related to a species' growth strategy and, though minimal compared with interspecific variation in WSG, can cause a downward bias when not incorporated into aboveground biomass estimates.

Coevolutionary legacies for plant decomposition.

Coevolution has driven speciation and evolutionary novelty in functional traits across the Tree of Life. Classic coevolutionary syndromes such as plant-pollinator, plant-herbivore, and host-parasite have focused strongly on the fitness consequences during the lifetime of the interacting partners. Less is known about the consequences of coevolved traits for ecosystem-level processes, in particular their 'afterlife' legacies for litter decomposition, nutrient cycling, and the functional ecology of decomposers. We review the mechanisms by which traits resulting from coevolution between plants and their consumers, microbial symbionts, or humans, and between microbial decomposers and invertebrates, drive plant litter decomposition pathways and rates. This supports the idea that much of current global variation in the decomposition of plant material is a legacy of coevolution.