Coupling of plant and mycorrhizal fungal diversity: its occurrence, relevance, and possible implications under global change.

First principles predict that diversity at one trophic level often begets diversity at other levels, suggesting plant and mycorrhizal fungal diversity should be coupled. Local-scale studies have shown positive coupling between the two, but the association is less consistent when extended to larger spatial and temporal scales. These inconsistencies are likely due to divergent relationships of different mycorrhizal fungal guilds to plant diversity, scale dependency, and a lack of coordinated sampling efforts. Given that mycorrhizal fungi play a central role in plant productivity and nutrient cycling, as well as ecosystem responses to global change, an improved understanding of the coupling between plant and mycorrhizal fungal diversity across scales will reduce uncertainties in predicting the ecosystem consequences of species gains and losses.

Tree diversity regulates forest pest invasion.

Nonnative pests often cause cascading ecological impacts, leading to detrimental socioeconomic consequences; however, how plant diversity may influence insect and disease invasions remains unclear. High species diversity in host communities may promote pest invasions by providing more niches (i.e., facilitation), but it can also diminish invasion success because low host dominance may make it more difficult for pests to establish (i.e., dilution). Most studies to date have focused on small-scale, experimental, or individual pest/disease species, while large-scale empirical studies, especially in natural ecosystems, are extremely rare. Using subcontinental-level data, we examined the role of tree diversity on pest invasion across the conterminous United States and found that the tree-pest diversity relationships are hump-shaped. Pest diversity increases with tree diversity at low tree diversity (because of facilitation or amplification) and is reduced at higher tree diversity (as a result of dilution). Thus, tree diversity likely regulates forest pest invasion through both facilitation and dilution that operate simultaneously, but their relative strengths vary with overall diversity. Our findings suggest the role of native species diversity in regulating nonnative pest invasions.

Biomass losses resulting from insect and disease invasions in US forests.

Worldwide, forests are increasingly affected by nonnative insects and diseases, some of which cause substantial tree mortality. Forests in the United States have been invaded by a particularly large number (>450) of tree-feeding pest species. While information exists about the ecological impacts of certain pests, region-wide assessments of the composite ecosystem impacts of all species are limited. Here we analyze 92,978 forest plots distributed across the conterminous United States to estimate biomass loss associated with elevated mortality rates caused by the 15 most damaging nonnative forest pests. We find that these species combined caused an additional (i.e., above background levels) tree mortality rate of 5.53 TgC per year. Compensation, in the form of increased growth and recruitment of nonhost species, was not detectable when measured across entire invaded ranges but does occur several decades following pest invasions. In addition, 41.1% of the total live forest biomass in the conterminous United States is at risk of future loss from these 15 pests. These results indicate that forest pest invasions, driven primarily by globalization, represent a huge risk to US forests and have significant impacts on carbon dynamics.

Microbial mechanisms and ecosystem flux estimation for aerobic NOy emissions from deciduous forest soils.

Reactive nitrogen oxides (NOy; NOy = NO + NO2 + HONO) decrease air quality and impact radiative forcing, yet the factors responsible for their emission from nonpoint sources (i.e., soils) remain poorly understood. We investigated the factors that control the production of aerobic NOy in forest soils using molecular techniques, process-based assays, and inhibitor experiments. We subsequently used these data to identify hotspots for gas emissions across forests of the eastern United States. Here, we show that nitrogen oxide soil emissions are mediated by microbial community structure (e.g., ammonium oxidizer abundances), soil chemical characteristics (pH and C:N), and nitrogen (N) transformation rates (net nitrification). We find that, while nitrification rates are controlled primarily by chemoautotrophic ammonia-oxidizing archaea (AOA), the production of NOy is mediated in large part by chemoautotrophic ammonia-oxidizing bacteria (AOB). Variation in nitrification rates and nitrogen oxide emissions tracked variation in forest communities, as stands dominated by arbuscular mycorrhizal (AM) trees had greater N transformation rates and NOy fluxes than stands dominated by ectomycorrhizal (ECM) trees. Given mapped distributions of AM and ECM trees from 78,000 forest inventory plots, we estimate that broadleaf forests of the Midwest and the eastern United States as well as the Mississippi River corridor may be considered hotspots of biogenic NOy emissions. Together, our results greatly improve our understanding of NOy fluxes from forests, which should lead to improved predictions about the atmospheric consequences of tree species shifts owing to land management and climate change.

Dominant forest tree mycorrhizal type mediates understory plant invasions.

Forest mycorrhizal type mediates nutrient dynamics, which in turn can influence forest community structure and processes. Using forest inventory data, we explored how dominant forest tree mycorrhizal type affects understory plant invasions with consideration of forest structure and soil properties. We found that arbuscular mycorrhizal (AM) dominant forests, which are characterised by thin forest floors and low soil C : N ratio, were invaded to a greater extent by non-native invasive species than ectomycorrhizal (ECM) dominant forests. Understory native species cover and richness had no strong associations with AM tree dominance. We also found no difference in the mycorrhizal type composition of understory invaders between AM and ECM dominant forests. Our results indicate that dominant forest tree mycorrhizal type is closely linked with understory invasions. The increased invader abundance in AM dominant forests can further facilitate nutrient cycling, leading to the alteration of ecosystem structure and functions.

A unified approach for quantifying invasibility and degree of invasion.

Habitat invasibility is a central focus of invasion biology, with implications for basic ecological patterns and processes and for effective invasion management. "Invasibility" is, however, one of the most elusive metrics and misused terms in ecology. Empirical studies and meta-analyses of invasibility have produced inconsistent and even conflicting results. This lack of consistency, and subsequent difficulty in making broad cross-habitat comparisons, stem in part from (1) the indiscriminant use of a closely related, but fundamentally different concept, that of degree of invasion (DI) or level of invasion; and (2) the lack of common invasibility metrics, as illustrated by our review of all invasibility-related papers published in 2013. To facilitate both cross-habitat comparison and more robust ecological generalizations, we clarify the definitions of invasibility and DI, and for the first time propose a common metric for quantifying invasibility based on a habitat's resource availability as inferred from relative resident species richness and biomass. We demonstrate the feasibility of our metric using empirical data collected from 2475 plots from three forest ecosystems in the eastern United States. We also propose a similar metric for DI. Our unified, resource-based metrics are scaled from 0 to 1, facilitating cross-habitat comparisons. Our proposed metrics clearly distinguish invasibility and DI from each other, which will help to (1) advance invasion ecology by allowing more robust testing of generalizations and (2) facilitate more effective invasive species control and management.

Spatial prediction of plant invasion using a hybrid of machine learning and geostatistical method.

Modeling ecological patterns and processes often involve large-scale and complex high-dimensional spatial data. Due to the nonlinearity and multicollinearity of ecological data, traditional geostatistical methods have faced great challenges in model accuracy. As machine learning has increased our ability to construct models on big data, the main focus of the study is to propose the use of statistical models that hybridize machine learning and spatial interpolation methods to cope with increasingly large-scale and complex ecological data. Here, two machine learning algorithms, boosted regression tree (BRT) and least absolute shrinkage and selection operator (LASSO), were combined with ordinary kriging (OK) to model plant invasions across the eastern United States. The accuracies of the hybrid models and conventional models were evaluated by 10-fold cross-validation. Based on an invasive plants dataset of 15 ecoregions across the eastern United States, the results showed that the hybrid algorithms were significantly better at predicting plant invasion when compared to commonly used algorithms in terms of RMSE and paired-samples t-test (with the p-value < .0001). Besides, the additional aspect of the combined algorithms is to have the ability to select influential variables associated with the establishment of invasive cover, which cannot be achieved by conventional geostatistics. Higher accuracy in the prediction of large-scale biological invasions improves our understanding of the ecological conditions that lead to the establishment and spread of plants into novel habitats across spatial scales. The results demonstrate the effectiveness and robustness of the hybrid BRTOK and LASOK that can be used to analyze large-scale and high-dimensional spatial datasets, and it has offered an optional source of models for spatial interpolation of ecology properties. It will also provide a better basis for management decisions in early-detection modeling of invasive species.

Identifying the generalizable controls on insect associations of native and non-native trees.

Trees growing outside their native geographic ranges often exhibit exceptional growth and survival due in part to the lack of co-evolved natural enemies that may limit their spread and suppress population growth. While most non-native trees tend to accumulate natural enemies over time, it remains uncertain which host and insect characteristics affect these novel associations and whether novel associations follow patterns of assembly similar to those of native hosts. Here, we used a dataset of insect-host tree associations in Europe to model which native insect species are paired with which native tree species, and then tested the model on its ability to predict which native insects are paired with which non-native trees. We show that native and non-native tree species closely related to known hosts are more likely to be hosts themselves, but that native host geographic range size, insect feeding guild, and sampling effort similarly affect insect associations. Our model had a strong ability to predict which insect species utilize non-native trees as hosts, but evolutionarily isolated tree species posed the greatest challenge to the model. These results demonstrate that insect-host associations can be reliably predicted, regardless of whether insect and host trees have co-evolved, and provide a framework for predicting future pest threats using a select number of easily attainable tree and insect characteristics.

DeepTree: Modeling Trees with Situated Latents.

In this paper, we propose DeepTree, a novel method for modeling trees based on learning developmental rules for branching structures instead of manually defining them. We call our deep neural model "situated latent" because its behavior is determined by the intrinsic state -encoded as a latent space of a deep neural model- and by the extrinsic (environmental) data that is "situated" as the location in the 3D space and on the tree structure. We use a neural network pipeline to train a situated latent space that allows us to locally predict branch growth only based on a single node in the branch graph of a tree model. We use this representation to progressively develop new branch nodes, thereby mimicking the growth process of trees. Starting from a root node, a tree is generated by iteratively querying the neural network on the newly added nodes resulting in the branching structure of the whole tree. Our method enables generating a wide variety of tree shapes without the need to define intricate parameters that control their growth and behavior. Furthermore, we show that the situated latents can also be used to encode the environmental response of tree models, e.g., when trees grow next to obstacles. We validate the effectiveness of our method by measuring the similarity of our tree models and by procedurally generated ones based on a number of established metrics for tree form.

Phenological response to climate variation in a northern red oak plantation: Links to survival and productivity.

In a changing climate, the future survival and productivity of species rely on individual populations to respond to shifting environmental conditions. Many tree species, including northern red oak (Quercus rubra), exhibit phenotypic plasticity, the ability to respond to changes in environmental conditions at within-generation time scales, through varying traits such as leaf phenology. Phenotypic plasticity of phenology may vary among populations within a species' range, and it is unclear if the range of plasticity is adequate to promote fitness. Here, we used a 58-year-old common garden to test whether northern red oak populations differed in phenological sensitivity to changes in temperature and whether differences in phenological sensitivity were associated with differences in productivity and survival (proxies of fitness). We recorded 8 years of spring leaf emergence and autumn leaf coloration and loss in 28 distinct populations from across the species' full range. Across the 28 populations, spring leaf out consistently advanced in warmer years, but fall phenology was less responsive to changes in temperature. Southern, warm-adapted populations had larger shifts in phenology in response to springtime warming but had lower long-term survival. Moreover, higher phenological sensitivity to spring warming was not strongly linked to increased productivity. Instead, fitness was more closely linked to latitudinal gradients. Although springtime phenological sensitivity to climate change is common across northern red oak populations, responses of productivity and survival, which could determine longer-term trajectories of species abundance, are more variable across the species' range.

Higher productivity in forests with mixed mycorrhizal strategies.

Decades of theory and empirical studies have demonstrated links between biodiversity and ecosystem functioning, yet the putative processes that underlie these patterns remain elusive. This is especially true for forest ecosystems, where the functional traits of plant species are challenging to quantify. We analyzed 74,563 forest inventory plots that span 35 ecoregions in the contiguous USA and found that in ~77% of the ecoregions mixed mycorrhizal plots were more productive than plots where either arbuscular or ectomycorrhizal fungal-associated tree species were dominant. Moreover, the positive effects of mixing mycorrhizal strategies on forest productivity were more pronounced at low than high tree species richness. We conclude that at low richness different mycorrhizal strategies may allow tree species to partition nutrient uptake and thus can increase community productivity, whereas at high richness other dimensions of functional diversity can enhance resource partitioning and community productivity. Our findings highlight the importance of mixed mycorrhizal strategies, in addition to that of taxonomic diversity in general, for maintaining ecosystem functioning in forests.

Integrating gradient with scale in ecological and evolutionary studies.

Gradient and scale are two key concepts in ecology and evolution that are closely related but inherently distinct. While scale commonly refers to the dimensional space of a specific ecological/evolutionary (eco-evo) issue, gradient measures the range of a given variable. Gradient and scale can jointly and interactively influence eco-evo patterns. Extensive previous research investigated how changing scales may affect the observation and interpretation of eco-evo patterns; however, relatively little attention has been paid to the role of changing gradients. Here, synthesizing recent research progress, we suggest that the role of scale in the emergence of ecological patterns should be evaluated in conjunction with considering the underlying environmental gradients. This is important because, in most studies, the range of the gradient is often part of its full potential range. The difference between sampled (partial) versus potential (full) environmental gradients may profoundly impact observed eco-evo patterns and alter scale-gradient relationships. Based on observations from both field and experimental studies, we illustrate the underlying features of gradients and how they may affect observed patterns, along with the linkages of these features to scales. Since sampled gradients often do not cover their full potential ranges, we discuss how the breadth and the starting and ending positions of key gradients may affect research design and data interpretation. We then outline potential approaches and related perspectives to better integrate gradient with scale in future studies.

Photographic assessment of temperate forest understory phenology in relation to springtime meteorological drivers.

Phenology shows sensitive responses to seasonal changes in atmospheric conditions. Forest understory phenology, in particular, is a crucial component of the forest ecosystem that interacts with meteorological factors, and ecosystem functions such as carbon exchange and nutrient cycling. Quantifying understory phenology is challenging due to the multiplicity of species and heterogeneous spatial distribution. The use of digital photography for assessing forest understory phenology was systematically tested in this study within a temperate forest during spring 2007. Five phenology metrics (phenometrics) were extracted from digital photos using three band algebra and two greenness percentage (image binarization) methods. Phenometrics were compared with a comprehensive suite of concurrent meteorological variables. Results show that greenness percentage cover approaches were relatively robust in capturing forest understory green-up. Derived spring phenology of understory plants responded to accumulated air temperature as anticipated, and with day-to-day changes strongly affected by estimated moisture availability. This study suggests that visible-light photographic assessment is useful for efficient forest understory phenology monitoring and allows more comprehensive data collection in support of ecosystem/land surface models.

Multispecies forest plantations outyield monocultures across a broad range of conditions.

Multispecies tree planting has long been applied in forestry and landscape restoration in the hope of providing better timber production and ecosystem services; however, a systematic assessment of its effectiveness is lacking. We compiled a global dataset of matched single-species and multispecies plantations to evaluate the impact of multispecies planting on stand growth. Average tree height, diameter at breast height, and aboveground biomass were 5.4, 6.8, and 25.5% higher, respectively, in multispecies stands compared with single-species stands. These positive effects were mainly the result of interspecific complementarity and were modulated by differences in leaf morphology and leaf life span, stand age, planting density, and temperature. Our results have implications for designing afforestation and reforestation strategies and bridging experimental studies of biodiversity-ecosystem functioning relationships with real-world practices.

Warm temperatures increase population growth of a nonnative defoliator and inhibit demographic responses by parasitoids.

Changes in thermal regimes that disparately affect hosts and parasitoids could release hosts from biological control. When multiple natural enemy species share a host, shifts in host-parasitoid dynamics could depend on whether natural enemies interact antagonistically vs. synergistically. We investigated how biotic and abiotic factors influence the population ecology of larch casebearer (Coleophora laricella), a nonnative pest, and two imported parasitoids, Agathis pumila and Chrysocharis laricinellae, by analyzing (1) temporal dynamics in defoliation from 1962 to 2018, and (2) historical, branch-level data on densities of larch casebearer and parasitism rates by the two imported natural enemies from 1972 to 1995. Analyses of defoliation indicated that, prior to the widespread establishment of parasitoids (1962 to ~1980), larch casebearer outbreaks occurred in 2-6 yr cycles. This pattern was followed by a >15-yr period during which populations were at low, apparently stable densities undetectable via aerial surveys, presumably under control from parasitoids. However, since the late 1990s and despite the persistence of both parasitoids, outbreaks exhibiting unstable dynamics have occurred. Analyses of branch-level data indicated that growth of casebearer populations, A. pumila populations, and within-casebearer densities of C. laricinellae-a generalist whose population dynamics are likely also influenced by use of alternative hosts-were inhibited by density dependence, with high intraspecific densities in one year slowing growth into the next. Casebearer population growth was also inhibited by parasitism from A. pumila, but not C. laricinellae, and increased with warmer autumnal temperatures. Growth of A. pumila populations and within-casebearer densities of C. laricinellae increased with casebearer densities but decreased with warmer annual maximum temperatures. Moreover, parasitism by A. pumila was associated with increased growth of within-casebearer densities of C. laricinellae without adverse effects on its own demographics, indicating a synergistic interaction between these parasitoids. Our results indicate that warming can be associated with opposing effects between trophic levels, with deleterious effects of warming on one natural enemy species potentially being exacerbated by similar impacts on another. Coupling of such parasitoid responses with positive responses of hosts to warming might have contributed to the return of casebearer outbreaks to North America.

Shifts in dominant tree mycorrhizal associations in response to anthropogenic impacts.

Plant-fungal symbioses play critical roles in vegetation dynamics and nutrient cycling, modulating the impacts of global changes on ecosystem functioning. Here, we used forest inventory data consisting of more than 3 million trees to develop a spatially resolved "mycorrhizal tree map" of the contiguous United States. We show that abundances of the two dominant mycorrhizal tree groups-arbuscular mycorrhizal (AM) and ectomycorrhizal trees-are associated primarily with climate. Further, we show that anthropogenic influences, primarily nitrogen (N) deposition and fire suppression, in concert with climate change, have increased AM tree dominance during the past three decades in the eastern United States. Given that most AM-dominated forests in this region are underlain by soils with high N availability, our results suggest that the increasing abundance of AM trees has the potential to induce nutrient acceleration, with critical consequences for forest productivity, ecosystem carbon and nutrient retention, and feedbacks to climate change.

Predicting invasiveness of exotic woody species using a traits-based framework.

Identifying potentially invasive species and preventing their introduction and establishment are of critical importance in invasion ecology and land management. Although an extensive body of research has been dedicated to identifying traits that confer invasiveness, our current knowledge is still often inconclusive due to limitations in geographic extent and/or scope of traits analyzed. Here, using a comprehensive set of 45 traits, we performed a case study of invasive traits displayed by exotic woody plants in the United States (U.S.) by comparing 63 invasive and 794 non-invasive exotic woody plant species naturalized across the country. We found that invasive woody species often bear the following two key traits: vegetative reproduction and long-distance seed dispersal (via water, birds or mammals). Boosted classification tree models based on these traits accurately predicted species invasiveness (86% accuracy on average). Presented findings provide a generalized understanding of the relative importance of functional traits in identifying potentially invasive woody species in the U.S. The knowledge generated in this study can be used to improve current classification systems of non-native woody plants used by various U.S. governmental agencies and land managers.

Relationships between advance oak regeneration and biotic and abiotic factors.

Relationships between advance regeneration of four tree species (red maple (Acer rubrum L.), white oak (Quercus alba L.), chestnut oak (Q. montana Willd.) and northern red oak (Q. rubra L.)) and biotic (non-tree vegetation and canopy composition) and abiotic (soil series and topographic variables) factors were investigated in 52, mature mixed-oak stands in the central Appalachians. Aggregate height was used as a composite measure of regeneration abundance. Analyses were carried out separately for two physiographic provinces. Associations with tree regeneration were found for all biotic and abiotic factors both in partial models and full models. Red maple was abundant on most of the sites, but high red maple abundance was commonly associated with wet north-facing slopes with little or no cover of mountain-laurel (Kalmia latifolia L.) and hay-scented fern (Dennstaedtia punctilobula (Michx.) Moore). Regeneration of the three oak species was greatly favored by the abundance of overstory trees of their own kind. White oak regeneration was most abundant on south-facing, gentle, lower slopes with soils in the Buchanan series. Chestnut oak regeneration was more common on south-facing, steep upper slopes with stony soils. There was a positive association between chestnut oak and huckleberry (Gaylussacia baccata (Wangh.) Koch) cover classes. Northern red oak was more abundant on north-facing wet sites with Hazleton soil, and was associated with low occurrence of mountain-laurel and hay-scented fern.

Impacts of climate on the biodiversity-productivity relationship in natural forests.

Understanding biodiversity-productivity relationships (BPRs) is of theoretical importance, and has important management implications. Most work on BPRs has focused on simple and/or experimentally assembled communities, and it is unclear how these observed BPRs can be extended to complex natural forest ecosystems. Using data from over 115,000 forest plots across the contiguous United States, we show that the bivariate BPRs are positive in dry climates and hump-shaped in mesic climates. When considering other site characteristics, BPRs change to neutral in dry climates and remain hump-shaped in humid sites. Our results indicate that climatic variation is an underlying determinant of contrasting BPRs observed across a large spatial extent, while both biotic factors (e.g., stand age and density) and abiotic factors (e.g., soil properties) can impact BPRs within a given climate unit. These findings suggest that tradeoffs need be made when considering whether to maximize productivity vs. conserve biodiversity, especially in mesic climates.

Divergence of species responses to climate change.

Climate change can have profound impacts on biodiversity and the sustainability of many ecosystems. Various studies have investigated the impacts of climate change, but large-scale, trait-specific impacts are less understood. We analyze abundance data over time for 86 tree species/groups across the eastern United States spanning the last three decades. We show that more tree species have experienced a westward shift (73%) than a poleward shift (62%) in their abundance, a trend that is stronger for saplings than adult trees. The observed shifts are primarily due to the changes of subpopulation abundances in the leading edges and are significantly associated with changes in moisture availability and successional processes. These spatial shifts are associated with species that have similar traits (drought tolerance, wood density, and seed weight) and evolutionary histories (most angiosperms shifted westward and most gymnosperms shifted poleward). Our results indicate that changes in moisture availability have stronger near-term impacts on vegetation dynamics than changes in temperature. The divergent responses to climate change by trait- and phylogenetic-specific groups could lead to changes in composition of forest ecosystems, putting the resilience and sustainability of various forest ecosystems in question.