Overabundant deer and invasive plants drive widespread regeneration debt in eastern United States national parks.

Advanced regeneration, in the form of tree seedlings and saplings, is critical for ensuring the long-term viability and resilience of forest ecosystems in the eastern United States. Lack of regeneration and/or compositional mismatch between regeneration and canopy layers, called regeneration debt, can lead to shifts in forest composition, structure, and, in extreme cases, forest loss. In this study, we examined status and trends in regeneration across 39 national parks from Virginia to Maine, spanning 12 years to apply the regeneration debt concept. We further refined the concept by adding new metrics and classifying results into easily interpreted categories adapted from the literature: imminent failure, probable failure, insecure, and secure. We then used model selection to determine the potential drivers most influencing patterns of regeneration debt. Status and trends indicated widespread regeneration debt in eastern national parks, with 27 of 39 parks classified as imminent or probable failure. Deer browse impact was consistently the strongest predictor of regeneration abundance. The most pervasive component of regeneration debt observed across parks was a sapling bottleneck, characterized by critically low sapling density of native canopy species and significant declines in native canopy sapling basal area or density for most parks. Regeneration mismatches also threaten forest resilience in many parks, where native canopy seedlings and saplings were outnumbered by native subcanopy species, particularly species that are less palatable deer browse. The devastating impact of emerald ash borer eliminating ash as a native canopy tree also drove regeneration mismatches in many parks that contain abundant ash regeneration, demonstrating the vulnerability of forests that lack diverse understories to invasive pests and pathogens. These findings underscore the critical importance of an integrated forest management approach that promotes an abundant and diverse regeneration layer. In most cases, this can only be achieved through long-term (i.e., multidecadal) management of white-tailed deer and invasive plants. Small-scale disturbances that increase structural complexity may also promote regeneration where stress from deer and invasive plants is minimal. Without immediate and sustained management intervention, the forest loss we are already observing may become a widespread pattern in eastern national parks and the broader region.

High aboveground carbon stock of African tropical montane forests.

Tropical forests store 40-50 per cent of terrestrial vegetation carbon1. However, spatial variations in aboveground live tree biomass carbon (AGC) stocks remain poorly understood, in particular in tropical montane forests2. Owing to climatic and soil changes with increasing elevation3, AGC stocks are lower in tropical montane forests compared with lowland forests2. Here we assemble and analyse a dataset of structurally intact old-growth forests (AfriMont) spanning 44 montane sites in 12 African countries. We find that montane sites in the AfriMont plot network have a mean AGC stock of 149.4 megagrams of carbon per hectare (95% confidence interval 137.1-164.2), which is comparable to lowland forests in the African Tropical Rainforest Observation Network4 and about 70 per cent and 32 per cent higher than averages from plot networks in montane2,5,6 and lowland7 forests in the Neotropics, respectively. Notably, our results are two-thirds higher than the Intergovernmental Panel on Climate Change default values for these forests in Africa8. We find that the low stem density and high abundance of large trees of African lowland forests4 is mirrored in the montane forests sampled. This carbon store is endangered: we estimate that 0.8 million hectares of old-growth African montane forest have been lost since 2000. We provide country-specific montane forest AGC stock estimates modelled from our plot network to help to guide forest conservation and reforestation interventions. Our findings highlight the need for conserving these biodiverse9,10 and carbon-rich ecosystems.

Long-term trends indicate that invasive plants are pervasive and increasing in eastern national parks.

While invasive plant distributions are relatively well known in the eastern United States, temporal changes in species distributions and interactions among species have received little attention. Managers are therefore left to make management decisions without knowing which species pose the greatest threats based on their ability to spread, persist and outcompete other invasive species. To fill this gap, we used the U.S. National Park Service's Inventory and Monitoring Program data collected from over 1,400 permanent forest plots spanning 12 yr and covering 39 eastern national parks to analyze invasive plant trends. We analyzed trends in abundance at multiple scales, including plot frequency, quadrat frequency, and average quadrat cover. We examined trends overall, by functional group, and by species. We detected considerably more increasing than decreasing trends in invasive plant abundance. In fact, 80% of the parks in our study had at least one significant increasing trend in invasive abundance over time. Where detected, significant negative trends tended to be herbaceous or graminoid species. However, these declines were often countered by roughly equivalent increases in invasive shrubs over the same time period, and we only detected overall declines in invasive abundance in two parks in our study. Present in over 30% of plots and responsible for the steepest and greatest number of significant increases, Japanese stiltgrass (Microstegium vimineum) was the most aggressive invader in our study and is a high management priority. Invasive shrubs, especially Japanese barberry (Berberis thunbergii), Japanese honeysuckle (Lonicera japonica), multiflora rose (Rosa multiflora), and wineberry (Rubus phoenicolasius), also increased across multiple parks, and sometimes at the expense of Japanese stiltgrass. Given the added risks to human health from tick-borne diseases, invasive shrubs are a high management priority. While these findings provide critical information to managers for species prioritization, they also demonstrate the incredible management challenge that invasive plants pose in protected areas, particularly since we documented few overall declines in invasive abundance. As parks work to overcome deferred maintenance of infrastructure, our findings suggest that deferred management of natural resources, particularly invasive species, requires similar attention and long-term commitment to reverse these widespread increasing invasive trends.

Tree mode of death and mortality risk factors across Amazon forests.

The carbon sink capacity of tropical forests is substantially affected by tree mortality. However, the main drivers of tropical tree death remain largely unknown. Here we present a pan-Amazonian assessment of how and why trees die, analysing over 120,000 trees representing > 3800 species from 189 long-term RAINFOR forest plots. While tree mortality rates vary greatly Amazon-wide, on average trees are as likely to die standing as they are broken or uprooted-modes of death with different ecological consequences. Species-level growth rate is the single most important predictor of tree death in Amazonia, with faster-growing species being at higher risk. Within species, however, the slowest-growing trees are at greatest risk while the effect of tree size varies across the basin. In the driest Amazonian region species-level bioclimatic distributional patterns also predict the risk of death, suggesting that these forests are experiencing climatic conditions beyond their adaptative limits. These results provide not only a holistic pan-Amazonian picture of tree death but large-scale evidence for the overarching importance of the growth-survival trade-off in driving tropical tree mortality.

Competition influences tree growth, but not mortality, across environmental gradients in Amazonia and tropical Africa.

Competition among trees is an important driver of community structure and dynamics in tropical forests. Neighboring trees may impact an individual tree's growth rate and probability of mortality, but large-scale geographic and environmental variation in these competitive effects has yet to be evaluated across the tropical forest biome. We quantified effects of competition on tree-level basal area growth and mortality for trees ≥10-cm diameter across 151 ~1-ha plots in mature tropical forests in Amazonia and tropical Africa by developing nonlinear models that accounted for wood density, tree size, and neighborhood crowding. Using these models, we assessed how water availability (i.e., climatic water deficit) and soil fertility influenced the predicted plot-level strength of competition (i.e., the extent to which growth is reduced, or mortality is increased, by competition across all individual trees). On both continents, tree basal area growth decreased with wood density and increased with tree size. Growth decreased with neighborhood crowding, which suggests that competition is important. Tree mortality decreased with wood density and generally increased with tree size, but was apparently unaffected by neighborhood crowding. Across plots, variation in the plot-level strength of competition was most strongly related to plot basal area (i.e., the sum of the basal area of all trees in a plot), with greater reductions in growth occurring in forests with high basal area, but in Amazonia, the strength of competition also varied with plot-level wood density. In Amazonia, the strength of competition increased with water availability because of the greater basal area of wetter forests, but was only weakly related to soil fertility. In Africa, competition was weakly related to soil fertility and invariant across the shorter water availability gradient. Overall, our results suggest that competition influences the structure and dynamics of tropical forests primarily through effects on individual tree growth rather than mortality and that the strength of competition largely depends on environment-mediated variation in basal area.

Asynchronous carbon sink saturation in African and Amazonian tropical forests.

Structurally intact tropical forests sequestered about half of the global terrestrial carbon uptake over the 1990s and early 2000s, removing about 15 per cent of anthropogenic carbon dioxide emissions1-3. Climate-driven vegetation models typically predict that this tropical forest 'carbon sink' will continue for decades4,5. Here we assess trends in the carbon sink using 244 structurally intact African tropical forests spanning 11 countries, compare them with 321 published plots from Amazonia and investigate the underlying drivers of the trends. The carbon sink in live aboveground biomass in intact African tropical forests has been stable for the three decades to 2015, at 0.66 tonnes of carbon per hectare per year (95 per cent confidence interval 0.53-0.79), in contrast to the long-term decline in Amazonian forests6. Therefore the carbon sink responses of Earth's two largest expanses of tropical forest have diverged. The difference is largely driven by carbon losses from tree mortality, with no detectable multi-decadal trend in Africa and a long-term increase in Amazonia. Both continents show increasing tree growth, consistent with the expected net effect of rising atmospheric carbon dioxide and air temperature7-9. Despite the past stability of the African carbon sink, our most intensively monitored plots suggest a post-2010 increase in carbon losses, delayed compared to Amazonia, indicating asynchronous carbon sink saturation on the two continents. A statistical model including carbon dioxide, temperature, drought and forest dynamics accounts for the observed trends and indicates a long-term future decline in the African sink, whereas the Amazonian sink continues to weaken rapidly. Overall, the uptake of carbon into Earth's intact tropical forests peaked in the 1990s. Given that the global terrestrial carbon sink is increasing in size, independent observations indicating greater recent carbon uptake into the Northern Hemisphere landmass10 reinforce our conclusion that the intact tropical forest carbon sink has already peaked. This saturation and ongoing decline of the tropical forest carbon sink has consequences for policies intended to stabilize Earth's climate.

Evolutionary diversity is associated with wood productivity in Amazonian forests.

Higher levels of taxonomic and evolutionary diversity are expected to maximize ecosystem function, yet their relative importance in driving variation in ecosystem function at large scales in diverse forests is unknown. Using 90 inventory plots across intact, lowland, terra firme, Amazonian forests and a new phylogeny including 526 angiosperm genera, we investigated the association between taxonomic and evolutionary metrics of diversity and two key measures of ecosystem function: aboveground wood productivity and biomass storage. While taxonomic and phylogenetic diversity were not important predictors of variation in biomass, both emerged as independent predictors of wood productivity. Amazon forests that contain greater evolutionary diversity and a higher proportion of rare species have higher productivity. While climatic and edaphic variables are together the strongest predictors of productivity, our results show that the evolutionary diversity of tree species in diverse forest stands also influences productivity. As our models accounted for wood density and tree size, they also suggest that additional, unstudied, evolutionarily correlated traits have significant effects on ecosystem function in tropical forests. Overall, our pan-Amazonian analysis shows that greater phylogenetic diversity translates into higher levels of ecosystem function: tropical forest communities with more distantly related taxa have greater wood productivity.

The persistence of carbon in the African forest understory.

Quantifying carbon dynamics in forests is critical for understanding their role in long-term climate regulation1-4. Yet little is known about tree longevity in tropical forests3,5-8, a factor that is vital for estimating carbon persistence3,4. Here we calculate mean carbon age (the period that carbon is fixed in trees7) in different strata of African tropical forests using (1) growth-ring records with a unique timestamp accurately demarcating 66 years of growth in one site and (2) measurements of diameter increments from the African Tropical Rainforest Observation Network (23 sites). We find that in spite of their much smaller size, in understory trees mean carbon age (74 years) is greater than in sub-canopy (54 years) and canopy (57 years) trees and similar to carbon age in emergent trees (66 years). The remarkable carbon longevity in the understory results from slow and aperiodic growth as an adaptation to limited resource availability9-11. Our analysis also reveals that while the understory represents a small share (11%) of the carbon stock12,13, it contributes disproportionally to the forest carbon sink (20%). We conclude that accounting for the diversity of carbon age and carbon sequestration among different forest strata is critical for effective conservation management14-16 and for accurate modelling of carbon cycling4.

Compositional response of Amazon forests to climate change.

Most of the planet's diversity is concentrated in the tropics, which includes many regions undergoing rapid climate change. Yet, while climate-induced biodiversity changes are widely documented elsewhere, few studies have addressed this issue for lowland tropical ecosystems. Here we investigate whether the floristic and functional composition of intact lowland Amazonian forests have been changing by evaluating records from 106 long-term inventory plots spanning 30 years. We analyse three traits that have been hypothesized to respond to different environmental drivers (increase in moisture stress and atmospheric CO2 concentrations): maximum tree size, biogeographic water-deficit affiliation and wood density. Tree communities have become increasingly dominated by large-statured taxa, but to date there has been no detectable change in mean wood density or water deficit affiliation at the community level, despite most forest plots having experienced an intensification of the dry season. However, among newly recruited trees, dry-affiliated genera have become more abundant, while the mortality of wet-affiliated genera has increased in those plots where the dry season has intensified most. Thus, a slow shift to a more dry-affiliated Amazonia is underway, with changes in compositional dynamics (recruits and mortality) consistent with climate-change drivers, but yet to significantly impact whole-community composition. The Amazon observational record suggests that the increase in atmospheric CO2 is driving a shift within tree communities to large-statured species and that climate changes to date will impact forest composition, but long generation times of tropical trees mean that biodiversity change is lagging behind climate change.

Diversity and carbon storage across the tropical forest biome.

Tropical forests are global centres of biodiversity and carbon storage. Many tropical countries aspire to protect forest to fulfil biodiversity and climate mitigation policy targets, but the conservation strategies needed to achieve these two functions depend critically on the tropical forest tree diversity-carbon storage relationship. Assessing this relationship is challenging due to the scarcity of inventories where carbon stocks in aboveground biomass and species identifications have been simultaneously and robustly quantified. Here, we compile a unique pan-tropical dataset of 360 plots located in structurally intact old-growth closed-canopy forest, surveyed using standardised methods, allowing a multi-scale evaluation of diversity-carbon relationships in tropical forests. Diversity-carbon relationships among all plots at 1 ha scale across the tropics are absent, and within continents are either weak (Asia) or absent (Amazonia, Africa). A weak positive relationship is detectable within 1 ha plots, indicating that diversity effects in tropical forests may be scale dependent. The absence of clear diversity-carbon relationships at scales relevant to conservation planning means that carbon-centred conservation strategies will inevitably miss many high diversity ecosystems. As tropical forests can have any combination of tree diversity and carbon stocks both require explicit consideration when optimising policies to manage tropical carbon and biodiversity.

Evolutionary heritage influences Amazon tree ecology.

Lineages tend to retain ecological characteristics of their ancestors through time. However, for some traits, selection during evolutionary history may have also played a role in determining trait values. To address the relative importance of these processes requires large-scale quantification of traits and evolutionary relationships among species. The Amazonian tree flora comprises a high diversity of angiosperm lineages and species with widely differing life-history characteristics, providing an excellent system to investigate the combined influences of evolutionary heritage and selection in determining trait variation. We used trait data related to the major axes of life-history variation among tropical trees (e.g. growth and mortality rates) from 577 inventory plots in closed-canopy forest, mapped onto a phylogenetic hypothesis spanning more than 300 genera including all major angiosperm clades to test for evolutionary constraints on traits. We found significant phylogenetic signal (PS) for all traits, consistent with evolutionarily related genera having more similar characteristics than expected by chance. Although there is also evidence for repeated evolution of pioneer and shade tolerant life-history strategies within independent lineages, the existence of significant PS allows clearer predictions of the links between evolutionary diversity, ecosystem function and the response of tropical forests to global change.

Hyperdominance in Amazonian forest carbon cycling.

While Amazonian forests are extraordinarily diverse, the abundance of trees is skewed strongly towards relatively few 'hyperdominant' species. In addition to their diversity, Amazonian trees are a key component of the global carbon cycle, assimilating and storing more carbon than any other ecosystem on Earth. Here we ask, using a unique data set of 530 forest plots, if the functions of storing and producing woody carbon are concentrated in a small number of tree species, whether the most abundant species also dominate carbon cycling, and whether dominant species are characterized by specific functional traits. We find that dominance of forest function is even more concentrated in a few species than is dominance of tree abundance, with only ≈1% of Amazon tree species responsible for 50% of carbon storage and productivity. Although those species that contribute most to biomass and productivity are often abundant, species maximum size is also influential, while the identity and ranking of dominant species varies by function and by region.

Markedly divergent estimates of Amazon forest carbon density from ground plots and satellites.

AIM: The accurate mapping of forest carbon stocks is essential for understanding the global carbon cycle, for assessing emissions from deforestation, and for rational land-use planning. Remote sensing (RS) is currently the key tool for this purpose, but RS does not estimate vegetation biomass directly, and thus may miss significant spatial variations in forest structure. We test the stated accuracy of pantropical carbon maps using a large independent field dataset. LOCATION: Tropical forests of the Amazon basin. The permanent archive of the field plot data can be accessed at: http://dx.doi.org/10.5521/FORESTPLOTS.NET/2014_1. METHODS: Two recent pantropical RS maps of vegetation carbon are compared to a unique ground-plot dataset, involving tree measurements in 413 large inventory plots located in nine countries. The RS maps were compared directly to field plots, and kriging of the field data was used to allow area-based comparisons. RESULTS: The two RS carbon maps fail to capture the main gradient in Amazon forest carbon detected using 413 ground plots, from the densely wooded tall forests of the north-east, to the light-wooded, shorter forests of the south-west. The differences between plots and RS maps far exceed the uncertainties given in these studies, with whole regions over- or under-estimated by > 25%, whereas regional uncertainties for the maps were reported to be < 5%. MAIN CONCLUSIONS: Pantropical biomass maps are widely used by governments and by projects aiming to reduce deforestation using carbon offsets, but may have significant regional biases. Carbon-mapping techniques must be revised to account for the known ecological variation in tree wood density and allometry to create maps suitable for carbon accounting. The use of single relationships between tree canopy height and above-ground biomass inevitably yields large, spatially correlated errors. This presents a significant challenge to both the forest conservation and remote sensing communities, because neither wood density nor species assemblages can be reliably mapped from space.

Increasing carbon storage in intact African tropical forests.

The response of terrestrial vegetation to a globally changing environment is central to predictions of future levels of atmospheric carbon dioxide. The role of tropical forests is critical because they are carbon-dense and highly productive. Inventory plots across Amazonia show that old-growth forests have increased in carbon storage over recent decades, but the response of one-third of the world's tropical forests in Africa is largely unknown owing to an absence of spatially extensive observation networks. Here we report data from a ten-country network of long-term monitoring plots in African tropical forests. We find that across 79 plots (163 ha) above-ground carbon storage in live trees increased by 0.63 Mg C ha(-1) yr(-1) between 1968 and 2007 (95% confidence interval (CI), 0.22-0.94; mean interval, 1987-96). Extrapolation to unmeasured forest components (live roots, small trees, necromass) and scaling to the continent implies a total increase in carbon storage in African tropical forest trees of 0.34 Pg C yr(-1) (CI, 0.15-0.43). These reported changes in carbon storage are similar to those reported for Amazonian forests per unit area, providing evidence that increasing carbon storage in old-growth forests is a pan-tropical phenomenon. Indeed, combining all standardized inventory data from this study and from tropical America and Asia together yields a comparable figure of 0.49 Mg C ha(-1) yr(-1) (n = 156; 562 ha; CI, 0.29-0.66; mean interval, 1987-97). This indicates a carbon sink of 1.3 Pg C yr(-1) (CI, 0.8-1.6) across all tropical forests during recent decades. Taxon-specific analyses of African inventory and other data suggest that widespread changes in resource availability, such as increasing atmospheric carbon dioxide concentrations, may be the cause of the increase in carbon stocks, as some theory and models predict.

Modified Whittaker plots as an assessment and monitoring tool for vegetation in a lowland tropical rainforest.

Resource exploitation in lowland tropical forests is increasing and causing loss of biodiversity. Effective evaluation and management of the impacts of development on tropical forests requires appropriate assessment and monitoring tools. We propose the use of 0.1-ha multi-scale, modified Whittaker plots (MWPs) to assess and monitor vegetation in lowland tropical rainforests. We established MWPs at 4 sites to: (1) describe and compare composition and structure of the sites using MWPs, (2) compare these results to those of 1-ha permanent vegetation plots (BDPs), and (3) evaluate the ability of MWPs to detect changes in populations (statistical power). We recorded more than 400 species at each site. Species composition among the sites was distinctive, while mean abundance and basal area was similar. Comparisons between MWPs and BDPs show that they record similar species composition and abundance and that both perform equally well at detecting rare species. However, MWPs tend to record more species, and power analysis studies show that MWPs were more effective at detecting changes in the mean number of species of trees > or = 10 cm in diameter at breast height (dbh) and in herbaceous plants. Ten MWPs were sufficient to detect a change of 11% in the mean number of herb species, and they were able to detect a 14% change in the mean number of species of trees > or =10 cm dbh. The value of MWPs for assessment and monitoring is discussed, along with recommendations for improving the sampling design to increase power.