Latitudinal patterns in stabilizing density dependence of forest communities.

Numerous studies have shown reduced performance in plants that are surrounded by neighbours of the same species1,2, a phenomenon known as conspecific negative density dependence (CNDD)3. A long-held ecological hypothesis posits that CNDD is more pronounced in tropical than in temperate forests4,5, which increases community stabilization, species coexistence and the diversity of local tree species6,7. Previous analyses supporting such a latitudinal gradient in CNDD8,9 have suffered from methodological limitations related to the use of static data10-12. Here we present a comprehensive assessment of latitudinal CNDD patterns using dynamic mortality data to estimate species-site-specific CNDD across 23 sites. Averaged across species, we found that stabilizing CNDD was present at all except one site, but that average stabilizing CNDD was not stronger toward the tropics. However, in tropical tree communities, rare and intermediate abundant species experienced stronger stabilizing CNDD than did common species. This pattern was absent in temperate forests, which suggests that CNDD influences species abundances more strongly in tropical forests than it does in temperate ones13. We also found that interspecific variation in CNDD, which might attenuate its stabilizing effect on species diversity14,15, was high but not significantly different across latitudes. Although the consequences of these patterns for latitudinal diversity gradients are difficult to evaluate, we speculate that a more effective regulation of population abundances could translate into greater stabilization of tropical tree communities and thus contribute to the high local diversity of tropical forests.

Distribution of biomass dynamics in relation to tree size in forests across the world.

Tree size shapes forest carbon dynamics and determines how trees interact with their environment, including a changing climate. Here, we conduct the first global analysis of among-site differences in how aboveground biomass stocks and fluxes are distributed with tree size. We analyzed repeat tree censuses from 25 large-scale (4-52 ha) forest plots spanning a broad climatic range over five continents to characterize how aboveground biomass, woody productivity, and woody mortality vary with tree diameter. We examined how the median, dispersion, and skewness of these size-related distributions vary with mean annual temperature and precipitation. In warmer forests, aboveground biomass, woody productivity, and woody mortality were more broadly distributed with respect to tree size. In warmer and wetter forests, aboveground biomass and woody productivity were more right skewed, with a long tail towards large trees. Small trees (1-10 cm diameter) contributed more to productivity and mortality than to biomass, highlighting the importance of including these trees in analyses of forest dynamics. Our findings provide an improved characterization of climate-driven forest differences in the size structure of aboveground biomass and dynamics of that biomass, as well as refined benchmarks for capturing climate influences in vegetation demographic models.

Demographic composition, not demographic diversity, predicts biomass and turnover across temperate and tropical forests.

The growth and survival of individual trees determine the physical structure of a forest with important consequences for forest function. However, given the diversity of tree species and forest biomes, quantifying the multitude of demographic strategies within and across forests and the way that they translate into forest structure and function remains a significant challenge. Here, we quantify the demographic rates of 1961 tree species from temperate and tropical forests and evaluate how demographic diversity (DD) and demographic composition (DC) differ across forests, and how these differences in demography relate to species richness, aboveground biomass (AGB), and carbon residence time. We find wide variation in DD and DC across forest plots, patterns that are not explained by species richness or climate variables alone. There is no evidence that DD has an effect on either AGB or carbon residence time. Rather, the DC of forests, specifically the relative abundance of large statured species, predicted both biomass and carbon residence time. Our results demonstrate the distinct DCs of globally distributed forests, reflecting biogeography, recent history, and current plot conditions. Linking the DC of forests to resilience or vulnerability to climate change, will improve the precision and accuracy of predictions of future forest composition, structure, and function.

Tree height and leaf drought tolerance traits shape growth responses across droughts in a temperate broadleaf forest.

As climate change drives increased drought in many forested regions, mechanistic understanding of the factors conferring drought tolerance in trees is increasingly important. The dendrochronological record provides a window through which we can understand how tree size and traits shape growth responses to droughts. We analyzed tree-ring records for 12 species in a broadleaf deciduous forest in Virginia (USA) to test hypotheses for how tree height, microenvironment characteristics, and species' traits shaped drought responses across the three strongest regional droughts over a 60-yr period. Drought tolerance (resistance, recovery, and resilience) decreased with tree height, which was strongly correlated with exposure to higher solar radiation and evaporative demand. The potentially greater rooting volume of larger trees did not confer a resistance advantage, but marginally increased recovery and resilience, in sites with low topographic wetness index. Drought tolerance was greater among species whose leaves lost turgor (wilted) at more negative water potentials and experienced less shrinkage upon desiccation. The tree-ring record reveals that tree height and leaf drought tolerance traits influenced growth responses during and after significant droughts in the meteorological record. As climate change-induced droughts intensify, tall trees with drought-sensitive leaves will be most vulnerable to immediate and longer-term growth reductions.

Tree-mycorrhizal associations detected remotely from canopy spectral properties.

A central challenge in global ecology is the identification of key functional processes in ecosystems that scale, but do not require, data for individual species across landscapes. Given that nearly all tree species form symbiotic relationships with one of two types of mycorrhizal fungi - arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) fungi - and that AM- and ECM-dominated forests often have distinct nutrient economies, the detection and mapping of mycorrhizae over large areas could provide valuable insights about fundamental ecosystem processes such as nutrient cycling, species interactions, and overall forest productivity. We explored remotely sensed tree canopy spectral properties to detect underlying mycorrhizal association across a gradient of AM- and ECM-dominated forest plots. Statistical mining of reflectance and reflectance derivatives across moderate/high-resolution Landsat data revealed distinctly unique phenological signals that differentiated AM and ECM associations. This approach was trained and validated against measurements of tree species and mycorrhizal association across ~130 000 trees throughout the temperate United States. We were able to predict 77% of the variation in mycorrhizal association distribution within the forest plots (P < 0.001). The implications for this work move us toward mapping mycorrhizal association globally and advancing our understanding of biogeochemical cycling and other ecosystem processes.

CTFS-ForestGEO: a worldwide network monitoring forests in an era of global change.

Global change is impacting forests worldwide, threatening biodiversity and ecosystem services including climate regulation. Understanding how forests respond is critical to forest conservation and climate protection. This review describes an international network of 59 long-term forest dynamics research sites (CTFS-ForestGEO) useful for characterizing forest responses to global change. Within very large plots (median size 25 ha), all stems ≥ 1 cm diameter are identified to species, mapped, and regularly recensused according to standardized protocols. CTFS-ForestGEO spans 25 °S-61 °N latitude, is generally representative of the range of bioclimatic, edaphic, and topographic conditions experienced by forests worldwide, and is the only forest monitoring network that applies a standardized protocol to each of the world's major forest biomes. Supplementary standardized measurements at subsets of the sites provide additional information on plants, animals, and ecosystem and environmental variables. CTFS-ForestGEO sites are experiencing multifaceted anthropogenic global change pressures including warming (average 0.61 °C), changes in precipitation (up to ± 30% change), atmospheric deposition of nitrogen and sulfur compounds (up to 3.8 g N m(-2) yr(-1) and 3.1 g S m(-2) yr(-1)), and forest fragmentation in the surrounding landscape (up to 88% reduced tree cover within 5 km). The broad suite of measurements made at CTFS-ForestGEO sites makes it possible to investigate the complex ways in which global change is impacting forest dynamics. Ongoing research across the CTFS-ForestGEO network is yielding insights into how and why the forests are changing, and continued monitoring will provide vital contributions to understanding worldwide forest diversity and dynamics in an era of global change.

Mycorrhizal feedbacks influence global forest structure and diversity.

One mechanism proposed to explain high species diversity in tropical systems is strong negative conspecific density dependence (CDD), which reduces recruitment of juveniles in proximity to conspecific adult plants. Although evidence shows that plant-specific soil pathogens can drive negative CDD, trees also form key mutualisms with mycorrhizal fungi, which may counteract these effects. Across 43 large-scale forest plots worldwide, we tested whether ectomycorrhizal tree species exhibit weaker negative CDD than arbuscular mycorrhizal tree species. We further tested for conmycorrhizal density dependence (CMDD) to test for benefit from shared mutualists. We found that the strength of CDD varies systematically with mycorrhizal type, with ectomycorrhizal tree species exhibiting higher sapling densities with increasing adult densities than arbuscular mycorrhizal tree species. Moreover, we found evidence of positive CMDD for tree species of both mycorrhizal types. Collectively, these findings indicate that mycorrhizal interactions likely play a foundational role in global forest diversity patterns and structure.

Consequences of spatial patterns for coexistence in species-rich plant communities.

Ecology cannot yet fully explain why so many tree species coexist in natural communities such as tropical forests. A major difficulty is linking individual-level processes to community dynamics. We propose a combination of tree spatial data, spatial statistics and dynamical theory to reveal the relationship between spatial patterns and population-level interaction coefficients and their consequences for multispecies dynamics and coexistence. Here we show that the emerging population-level interaction coefficients have, for a broad range of circumstances, a simpler structure than their individual-level counterparts, which allows for an analytical treatment of equilibrium and stability conditions. Mechanisms such as animal seed dispersal, which result in clustering of recruits that is decoupled from parent locations, lead to a rare-species advantage and coexistence of otherwise neutral competitors. Linking spatial statistics with theories of community dynamics offers new avenues for explaining species coexistence and calls for rethinking community ecology through a spatial lens.

Nonconsumptive effects of a generalist ungulate herbivore drive decline of unpalatable forest herbs.

High herbivore pressure is expected to benefit unpalatable species that co-occur with palatable browsed species. However, for five unpalatable understory species we found no evidence of benefit from deer browse. Detailed studies of one species in natural populations, Arisaema triphyllum, revealed surprising changes in its population structure and demography: deer browse level on a palatable species significantly correlates with reduced plant size and seed rain and male-biased sex ratios of co-occurring Arisaema populations. Analyses of individual size in five unpalatable forest plant species in long-term experimental paired deer exclosure/deer access plots corroborate the natural site results; all five species were smaller in deer access plots. Analyses of abiotic variables in natural and experimental sites suggest one potential mechanism for indirect effects of deer. Deer-mediated soil quality declines included increased soil penetration resistance and decreased leaf litter depth, which are known to hinder plant growth. Our results are likely applicable to other unpalatable forest species and have clear consequences for understory biodiversity. Unpalatable plant species in forests experiencing high deer numbers may be in decline along with their palatable neighbors. Our study implicates deer overabundance in the cascade of forest species decline and the urgency of this conservation issue in North America.

A regional assessment of white-tailed deer effects on plant invasion.

Herbivores can profoundly influence plant species assembly, including plant invasion, and resulting community composition. Population increases of native herbivores, e.g. white-tailed deer (Odocoileus virginianus), combined with burgeoning plant invasions raise concerns for native plant diversity and forest regeneration. While individual researchers typically test for the impact of deer on plant invasion at a few sites, the overarching influence of deer on plant invasion across regional scales is unclear. We tested the effects of deer on the abundance and diversity of introduced and native herbaceous and woody plants across 23 white-tailed deer research sites distributed across the east-central and north-eastern USA and representing a wide range of deer densities and invasive plant abundance and identity. Deer access/exclusion or deer population density did not affect introduced plant richness or community-level abundance. Native and total plant species richness, abundance (cover and stem density) and Shannon diversity were lower in deer-access vs. deer-exclusion plots. Among deer-access plots, native species richness, native and total cover, and Shannon diversity (cover) declined as deer density increased. Deer access increased the proportion of introduced species cover (but not of species richness or stem density). As deer density increased, the proportion of introduced species richness, cover and stem density all increased. Because absolute abundance of introduced plants was unaffected by deer, the increase in proportion of introduced plant abundance is likely an indirect effect of deer reducing native cover. Indicator species analysis revealed that deer access favoured three introduced plant species, including Alliaria petiolata and Microstegium vimineum, as well as four native plant species. In contrast, deer exclusion favoured three introduced plant species, including Lonicera japonica and Rosa multiflora, and 15 native plant species. Overall, native deer reduced community diversity, lowering native plant richness and abundance, and benefited certain invasive plants, suggesting pervasive impacts of this keystone herbivore on plant community composition and ecosystem services in native forests across broad swathes of the eastern USA.

Response to Comment on "Plant diversity increases with the strength of negative density dependence at the global scale".

Hülsmann and Hartig suggest that ecological mechanisms other than specialized natural enemies or intraspecific competition contribute to our estimates of conspecific negative density dependence (CNDD). To address their concern, we show that our results are not the result of a methodological artifact and present a null-model analysis that demonstrates that our original findings-(i) stronger CNDD at tropical relative to temperate latitudes and (ii) a latitudinal shift in the relationship between CNDD and species abundance-persist even after controlling for other processes that might influence spatial relationships between adults and recruits.

Response to Comment on "Plant diversity increases with the strength of negative density dependence at the global scale".

Chisholm and Fung claim that our method of estimating conspecific negative density dependence (CNDD) in recruitment is systematically biased, and present an alternative method that shows no latitudinal pattern in CNDD. We demonstrate that their approach produces strongly biased estimates of CNDD, explaining why they do not detect a latitudinal pattern. We also address their methodological concerns using an alternative distance-weighted approach, which supports our original findings of a latitudinal gradient in CNDD and a latitudinal shift in the relationship between CNDD and species abundance.

Reconstructing a herbivore's diet using a novel rbcL DNA mini-barcode for plants.

Next Generation Sequencing and the application of metagenomic analyses can be used to answer questions about animal diet choice and study the consequences of selective foraging by herbivores. The quantification of herbivore diet choice with respect to native versus exotic plant species is particularly relevant given concerns of invasive species establishment and their effects on ecosystems. While increased abundance of white-tailed deer (Odocoileus virginianus) appears to correlate with increased incidence of invasive plant species, data supporting a causal link is scarce. We used a metabarcoding approach (PCR amplicons of the plant rbcL gene) to survey the diet of white-tailed deer (fecal samples), from a forested site in Warren County, Virginia with a comprehensive plant species inventory and corresponding reference collection of plant barcode and chloroplast sequences. We sampled fecal pellet piles and extracted DNA from 12 individual deer in October 2014. These samples were compared to a reference DNA library of plant species collected within the study area. For 72 % of the amplicons, we were able to assign taxonomy at the species level, which provides for the first time-sufficient taxonomic resolution to quantify the relative frequency at which native and exotic plant species are being consumed by white-tailed deer. For each of the 12 individual deer we collected three subsamples from the same fecal sample, resulting in sequencing 36 total samples. Using Qiime, we quantified the plant DNA found in all 36 samples, and found that variance within samples was less than variance between samples (F = 1.73, P = 0.004), indicating additional subsamples may not be necessary. Species level diversity ranged from 60 to 93 OTUs per individual and nearly 70 % of all plant sequences recovered were from native plant species. The number of species detected did reduce significantly (range 4-12) when we excluded species whose OTU composed <1 % of each sample's total. When compared to the abundance of native and non-natives plants inventoried in the local community, our results support the observation that white-tailed deer have strong foraging preferences, but these preferences were not consistent for species in either class. Deer forage behaviour may favour some exotic species, but not all.

Sapling growth rates reveal conspecific negative density dependence in a temperate forest.

Local tree species diversity is maintained in part by conspecific negative density dependence (CNDD). This pervasive mechanism occurs in a variety of forms and ecosystems, but research to date has been heavily skewed toward tree seedling survival in tropical forests. To evaluate CNDD more broadly, we investigated how sapling growth rates were affected by conspecific adult neighbors in a fully mapped 25.6 ha temperate deciduous forest. We examined growth rates as a function of the local adult tree neighborhood (via spatial autoregressive modeling) and compared the spatial positioning of faster-growing and slower-growing saplings with respect to adult conspecific and heterospecific trees (via bivariate point pattern analysis). In addition, to determine whether CNDD-driven variation in growth rates leaves a corresponding spatial signal, we extended our point pattern analysis to a static, growth-independent comparison of saplings and the next larger size class. We found that negative conspecific effects on sapling growth were most prevalent. Five of the nine species that were sufficiently abundant for analysis exhibited CNDD, while only one species showed evidence of a positive conspecific effect, and one or two species, depending on the analysis, displayed heterospecific effects. There was general agreement between the autoregressive models and the point pattern analyses based on sapling growth rates, but point pattern analyses based on single-point-in-time size classes yielded results that differed markedly from the other two approaches. Our work adds to the growing body of evidence that CNDD is an important force in temperate forests, and demonstrates that this process extends to sapling growth rates. Further, our findings indicate that point pattern analyses based solely on size classes may fail to detect the process of interest (e.g., neighborhood-driven variation in growth rates), in part due to the confounding of tree size and age.

Plant diversity increases with the strength of negative density dependence at the global scale.

Theory predicts that higher biodiversity in the tropics is maintained by specialized interactions among plants and their natural enemies that result in conspecific negative density dependence (CNDD). By using more than 3000 species and nearly 2.4 million trees across 24 forest plots worldwide, we show that global patterns in tree species diversity reflect not only stronger CNDD at tropical versus temperate latitudes but also a latitudinal shift in the relationship between CNDD and species abundance. CNDD was stronger for rare species at tropical versus temperate latitudes, potentially causing the persistence of greater numbers of rare species in the tropics. Our study reveals fundamental differences in the nature of local-scale biotic interactions that contribute to the maintenance of species diversity across temperate and tropical communities.

Long-Term Effects of White-Tailed Deer Exclusion on the Invasion of Exotic Plants: A Case Study in a Mid-Atlantic Temperate Forest.

Exotic plant invasions and chronic high levels of herbivory are two of the major biotic stressors impacting temperate forest ecosystems in eastern North America, and the two problems are often linked. We used a 4-ha deer exclosure maintained since 1991 to examine the influence of a generalist herbivore, white-tailed deer (Odocoileus virginianus), on the abundance of four exotic invasive (Rosa multiflora, Berberis thunbergii, Rubus phoenicolasius and Microstegium vimineum) and one native (Cynoglossum virginianum) plant species, within a 25.6-ha mature temperate forest dynamics plot in Virginia, USA. We identified significant predictors of the abundance of each focal species using generalized linear models incorporating 10 environmental and landscape variables. After controlling for those predictors, we applied our models to a 4-ha deer exclusion site and a 4-ha reference site, both embedded within the larger plot, to test the role of deer on the abundance of the focal species. Slope, edge effects and soil pH were the most frequent predictors of the abundance of the focal species on the larger plot. The abundance of C. virginianum, known to be deer-dispersed, was significantly lower in the exclosure. Similar patterns were detected for B. thunbergii, R. phoenicolasius and M. vimineum, whereas R. multiflora was more abundant within the exclosure. Our results indicate that chronic high deer density facilitates increased abundances of several exotic invasive plant species, with the notable exception of R. multiflora. We infer that the invasion of many exotic plant species that are browse-tolerant to white-tailed deer could be limited by reducing deer populations.

Closely-related taxa influence woody species discrimination via DNA barcoding: evidence from global forest dynamics plots.

To determine how well DNA barcodes from the chloroplast region perform in forest dynamics plots (FDPs) from global CTFS-ForestGEO network, we analyzed DNA barcoding sequences of 1277 plant species from a wide phylogenetic range (3 FDPs in tropics, 5 in subtropics and 5 in temperate zone) and compared the rates of species discrimination (RSD). We quantified RSD by two DNA barcode combinations (rbcL + matK and rbcL + matK + trnH-psbA) using a monophyly-based method (GARLI). We defined two indexes of closely-related taxa (Gm/Gt and S/G ratios) and correlated these ratios with RSD. The combination of rbcL + matK averagely discriminated 88.65%, 83.84% and 72.51% at the local, regional and global scales, respectively. An additional locus trnH-psbA increased RSD by 2.87%, 1.49% and 3.58% correspondingly. RSD varied along a latitudinal gradient and were negatively correlated with ratios of closely-related taxa. Successes of species discrimination generally depend on scales in global FDPs. We suggested that the combination of rbcL + matK + trnH-psbA is currently applicable for DNA barcoding-based phylogenetic studies on forest communities.

Comparative evolutionary diversity and phylogenetic structure across multiple forest dynamics plots: a mega-phylogeny approach.

Forest dynamics plots, which now span longitudes, latitudes, and habitat types across the globe, offer unparalleled insights into the ecological and evolutionary processes that determine how species are assembled into communities. Understanding phylogenetic relationships among species in a community has become an important component of assessing assembly processes. However, the application of evolutionary information to questions in community ecology has been limited in large part by the lack of accurate estimates of phylogenetic relationships among individual species found within communities, and is particularly limiting in comparisons between communities. Therefore, streamlining and maximizing the information content of these community phylogenies is a priority. To test the viability and advantage of a multi-community phylogeny, we constructed a multi-plot mega-phylogeny of 1347 species of trees across 15 forest dynamics plots in the ForestGEO network using DNA barcode sequence data (rbcL, matK, and psbA-trnH) and compared community phylogenies for each individual plot with respect to support for topology and branch lengths, which affect evolutionary inference of community processes. The levels of taxonomic differentiation across the phylogeny were examined by quantifying the frequency of resolved nodes throughout. In addition, three phylogenetic distance (PD) metrics that are commonly used to infer assembly processes were estimated for each plot [PD, Mean Phylogenetic Distance (MPD), and Mean Nearest Taxon Distance (MNTD)]. Lastly, we examine the partitioning of phylogenetic diversity among community plots through quantification of inter-community MPD and MNTD. Overall, evolutionary relationships were highly resolved across the DNA barcode-based mega-phylogeny, and phylogenetic resolution for each community plot was improved when estimated within the context of the mega-phylogeny. Likewise, when compared with phylogenies for individual plots, estimates of phylogenetic diversity in the mega-phylogeny were more consistent, thereby removing a potential source of bias at the plot-level, and demonstrating the value of assessing phylogenetic relationships simultaneously within a mega-phylogeny. An unexpected result of the comparisons among plots based on the mega-phylogeny was that the communities in the ForestGEO plots in general appear to be assemblages of more closely related species than expected by chance, and that differentiation among communities is very low, suggesting deep floristic connections among communities and new avenues for future analyses in community ecology.