Global dominance of lianas over trees is driven by forest disturbance, climate and topography.

Growing evidence suggests that liana competition with trees is threatening the global carbon sink by slowing the recovery of forests following disturbance. A recent theory based on local and regional evidence further proposes that the competitive success of lianas over trees is driven by interactions between forest disturbance and climate. We present the first global assessment of liana-tree relative performance in response to forest disturbance and climate drivers. Using an unprecedented dataset, we analysed 651 vegetation samples representing 26,538 lianas and 82,802 trees from 556 unique locations worldwide, derived from 83 publications. Results show that lianas perform better relative to trees (increasing liana-to-tree ratio) when forests are disturbed, under warmer temperatures and lower precipitation and towards the tropical lowlands. We also found that lianas can be a critical factor hindering forest recovery in disturbed forests experiencing liana-favourable climates, as chronosequence data show that high competitive success of lianas over trees can persist for decades following disturbances, especially when the annual mean temperature exceeds 27.8°C, precipitation is less than 1614 mm and climatic water deficit is more than 829 mm. These findings reveal that degraded tropical forests with environmental conditions favouring lianas are disproportionately more vulnerable to liana dominance and thus can potentially stall succession, with important implications for the global carbon sink, and hence should be the highest priority to consider for restoration management.

Des preuves de plus en plus nombreuses suggèrent que la competition entre lianes et les arbres menace le puits de carbone mondial en ralentissant la récupération des forêts après une perturbation. Une théorie récente, fondée sur des observations locales et régionales, propose en outre que le succès compétitif des lianes sur les arbres est dû aux interactions entre la perturbation forestière et le climat. Nous présentons la première évaluation mondiale de la performance relative des lianes par rapport aux arbres en réponse aux perturbations forestières et aux facteurs climatiques. En utilisant un ensemble de données sans précédent, nous avons analysé 651 échantillons de végétation représentant 26,538 lianes et 82,802 arbres, issus de 556 emplacements uniques dans le monde entier, tirés de 83 publications. Les résultats montrent que les lianes ont de meilleure performances par rapport aux arbres (augmentation du ratio liane-arbre) lorsque les forêts sont perturbées, sous des zones chaudes aves précipitations faibles, et vers les basses altitudes tropicales. Nous avons également constaté que les lianes peuvent être un facteur critique entravant la récupération des forêts dans les forêts perturbées connaissant des climats favorables aux lianes, car les données de chronoséquence montrent que le succès compétitif élevé des lianes sur les arbres peut persister pendant des décennies après les perturbations, surtout lorsque la température annuelle moyenne dépasse 27.8°C, que les précipitations sont inférieures à 1614 mm et que le déficit hydrique climatique est supérieur à 829 mm. Ces découvertes révèlent que les forêts tropicales dégradées avec des conditions environnementales favorables aux lianes sont disproportionnellement plus vulnérables à la dominance des lianes, et peuvent ainsi potentiellement entraver la succession, avec d'importantes implications pour le puits de carbone mondial et devraient donc être la plus haute priorité à considérer pour la gestion de la restauration.

Lianas decelerate tropical forest thinning during succession.

The well-established pattern of forest thinning during succession predicts an increase in mean tree biomass with decreasing tree density. The forest thinning pattern is commonly assumed to be driven solely by tree-tree competition. The presence of non-tree competitors could alter thinning trajectories, thus altering the rate of forest succession and carbon uptake. We used a large-scale liana removal experiment over 7 years in a 60- to 70-year-old Panamanian forest to test the hypothesis that lianas reduce the rate of forest thinning during succession. We found that lianas slowed forest thinning by reducing tree growth, not by altering tree recruitment or mortality. Without lianas, trees grew and presumably competed more, ultimately reducing tree density while increasing mean tree biomass. Our findings challenge the assumption that forest thinning is driven solely by tree-tree interactions; instead, they demonstrate that competition from other growth forms, such as lianas, slow forest thinning and ultimately delay forest succession.

Lianas reduce carbon accumulation and storage in tropical forests.

Tropical forests store vast quantities of carbon, account for one-third of the carbon fixed by photosynthesis, and are a major sink in the global carbon cycle. Recent evidence suggests that competition between lianas (woody vines) and trees may reduce forest-wide carbon uptake; however, estimates of the impact of lianas on carbon dynamics of tropical forests are crucially lacking. Here we used a large-scale liana removal experiment and found that, at 3 y after liana removal, lianas reduced net above-ground carbon uptake (growth and recruitment minus mortality) by ∼76% per year, mostly by reducing tree growth. The loss of carbon uptake due to liana-induced mortality was four times greater in the control plots in which lianas were present, but high variation among plots prevented a significant difference among the treatments. Lianas altered how aboveground carbon was stored. In forests where lianas were present, the partitioning of forest aboveground net primary production was dominated by leaves (53.2%, compared with 39.2% in liana-free forests) at the expense of woody stems (from 28.9%, compared with 43.9%), resulting in a more rapid return of fixed carbon to the atmosphere. After 3 y of experimental liana removal, our results clearly demonstrate large differences in carbon cycling between forests with and without lianas. Combined with the recently reported increases in liana abundance, these results indicate that lianas are an important and increasing agent of change in the carbon dynamics of tropical forests.

Fast demographic traits promote high diversification rates of Amazonian trees.

The Amazon rain forest sustains the world's highest tree diversity, but it remains unclear why some clades of trees are hyperdiverse, whereas others are not. Using dated phylogenies, estimates of current species richness and trait and demographic data from a large network of forest plots, we show that fast demographic traits--short turnover times--are associated with high diversification rates across 51 clades of canopy trees. This relationship is robust to assuming that diversification rates are either constant or decline over time, and occurs in a wide range of Neotropical tree lineages. This finding reveals the crucial role of intrinsic, ecological variation among clades for understanding the origin of the remarkable diversity of Amazonian trees and forests.

Tropical forest lianas have greater non-structural carbohydrate concentrations in the stem xylem than trees.

Lianas (woody vines) are important components of tropical forests and are known to compete with host trees for resources, decrease tree growth and increase tree mortality. Given the observed increases in liana abundance in some forests and their impacts on forest function, an integrated understanding of carbon dynamics of lianas and liana-infested host trees is critical for improved prediction of tropical forest responses to climate change. Non-structural carbohydrates (NSC) are the main substrate for plant metabolism (e.g., growth, respiration), and have been implicated in enabling tree survival under environmental stress, but little is known of how they vary among life-forms or of how liana infestation impacts host tree NSC. We quantified stem total NSC (NSC) concentrations and its fractions (starch and soluble sugars) in trees without liana infestation, trees with more than 50% of the canopy covered by lianas, and the lianas infesting those trees. We hypothesized that i) liana infestation depletes NSC storage in host trees by reducing carbon assimilation due to competition for resources; ii) trees and lianas, which greatly differ in functional traits related to water transport and carbon uptake, would also have large differences in NSC storage, and that As water availability has a significant role in NSC dynamics of Amazonian tree species, we tested these hypotheses within a moist site in western Amazonia and a drier forest site in southern Amazonia. We did not find any difference in NSC, starch or soluble sugar concentrations between infested and non-infested trees, in either site. This result suggests that negative liana impact on trees may be mediated through mechanisms other than depletion of host tree NSC concentrations. We found lianas have higher stem NSC and starch than trees in both sites. The consistent differences in starch concentrations, a long term NSC reserve, between life forms across sites reflect differences in carbon gain and use of lianas and trees. Soluble sugar concentrations were higher in lianas than in trees in the moist site but indistinguishable between life forms in the dry site. The lack of difference in soluble sugars between trees and lianas in the dry site emphasize the importance of this NSC fraction for plant metabolism of plants occurring in water limited environments. Abstract in Portuguese and Spanish are available in the supplementary material.

Drought-mortality relationships for tropical forests.

*The rich ecology of tropical forests is intimately tied to their moisture status. Multi-site syntheses can provide a macro-scale view of these linkages and their susceptibility to changing climates. Here, we report pan-tropical and regional-scale analyses of tree vulnerability to drought. *We assembled available data on tropical forest tree stem mortality before, during, and after recent drought events, from 119 monitoring plots in 10 countries concentrated in Amazonia and Borneo. *In most sites, larger trees are disproportionately at risk. At least within Amazonia, low wood density trees are also at greater risk of drought-associated mortality, independent of size. For comparable drought intensities, trees in Borneo are more vulnerable than trees in the Amazon. There is some evidence for lagged impacts of drought, with mortality rates remaining elevated 2 yr after the meteorological event is over. *These findings indicate that repeated droughts would shift the functional composition of tropical forests toward smaller, denser-wooded trees. At very high drought intensities, the linear relationship between tree mortality and moisture stress apparently breaks down, suggesting the existence of moisture stress thresholds beyond which some tropical forests would suffer catastrophic tree mortality.

Active restoration accelerates the carbon recovery of human-modified tropical forests.

More than half of all tropical forests are degraded by human impacts, leaving them threatened with conversion to agricultural plantations and risking substantial biodiversity and carbon losses. Restoration could accelerate recovery of aboveground carbon density (ACD), but adoption of restoration is constrained by cost and uncertainties over effectiveness. We report a long-term comparison of ACD recovery rates between naturally regenerating and actively restored logged tropical forests. Restoration enhanced decadal ACD recovery by more than 50%, from 2.9 to 4.4 megagrams per hectare per year. This magnitude of response, coupled with modal values of restoration costs globally, would require higher carbon prices to justify investment in restoration. However, carbon prices required to fulfill the 2016 Paris climate agreement [$40 to $80 (USD) per tonne carbon dioxide equivalent] would provide an economic justification for tropical forest restoration.

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.

Lianas have a seasonal growth advantage over co-occurring trees.

The seasonal growth advantage hypothesis posits that plant species that grow well during seasonal drought will increase in abundance in forests with increasing seasonality of rainfall both in absolute numbers and also relative to co-occurring plant species that grow poorly during seasonal drought. That is, seasonal drought will give some plant species a growth advantage that they lack in aseasonal forests, thus allowing them attain higher abundance. For tropical forest plants, the seasonal growth advantage hypothesis may explain the distribution of drought-adapted species across large-scale gradients of rainfall and seasonality. We tested the seasonal growth advantage hypothesis with lianas and trees in a seasonal tropical forest in central Panama. We measured the dry-season and wet-season diameter growth of 1,117 canopy trees and 648 canopy lianas from 2011 to 2016. We also evaluated how lianas and trees responded to the 2015-2016 El Niño, which was the third strongest el Niño drought on record in Panama. We found that liana growth rate was considerably higher during the dry-season months than the wet-season months in each of the five years. Lianas achieved one-half of their annual growth during the 4-month dry season. By contrast, trees grew far more during the wet season; they realized only one-quarter of their annual growth during the dry season. During the strong 2015-2016 El Niño dry season, trees essentially stopped growing, whereas lianas grew unimpeded and as well as during any of the previous four dry seasons. Our findings support the hypothesis that seasonal growth gives lianas a decided growth advantage over trees in seasonal forests compared to aseasonal forests, and may explain why lianas peak in both absolute and relative abundance in highly seasonal tropical forests. Furthermore, the ability of lianas to grow during a strong el Niño drought suggests that lianas will benefit from the predicted increasing drought severity, whereas trees will suffer, and thus lianas are predicted to increase in relative abundance in seasonal tropical forests.

Environmental drivers of forest structure and stem turnover across Venezuelan tropical forests.

Using data from 50 long-term permanent plots from across Venezuelan forests in northern South America, we explored large-scale patterns of stem turnover, aboveground biomass (AGB) and woody productivity (AGWP), and the relationships between them and with potential climatic drivers. We used principal component analysis coupled with generalized least squares models to analyze the relationship between climate, forest structure and stem dynamics. Two major axes associated with orthogonal temperature and moisture gradients effectively described more than 90% of the environmental variability in the dataset. Average turnover was 1.91 ± 0.10% year-1 with mortality and recruitment being almost identical, and close to average rates for other mature tropical forests. Turnover rates were significantly different among regions (p < 0.001), with the lowland forests in Western alluvial plains being the most dynamic, and Guiana Shield forests showing the lowest turnover rates. We found a weak positive relationship between AGB and AGWP, with Guiana Shield forests having the highest values for both variables (204.8 ± 14.3 Mg C ha-1 and 3.27 ± 0.27 Mg C ha-1 year-1 respectively), but AGB was much more strongly and negatively related to stem turnover. Our data suggest that moisture is a key driver of turnover, with longer dry seasons favoring greater rates of tree turnover and thus lower biomass, having important implications in the context of climate change, given the increases in drought frequency in many tropical forests. Regional variation in AGWP among Venezuelan forests strongly reflects the effects of climate, with greatest woody productivity where both precipitation and temperatures are high. Overall, forests in wet, low elevation sites and with slow turnover stored the greatest amounts of biomass. Although faster stand dynamics are closely associated with lower carbon storage, stem-level turnover rates and woody productivity did not show any correlation, indicating that stem dynamics and carbon dynamics are largely decoupled from one another.

Above-ground biomass and structure of 260 African tropical forests.

We report above-ground biomass (AGB), basal area, stem density and wood mass density estimates from 260 sample plots (mean size: 1.2 ha) in intact closed-canopy tropical forests across 12 African countries. Mean AGB is 395.7 Mg dry mass ha⁻¹ (95% CI: 14.3), substantially higher than Amazonian values, with the Congo Basin and contiguous forest region attaining AGB values (429 Mg ha⁻¹) similar to those of Bornean forests, and significantly greater than East or West African forests. AGB therefore appears generally higher in palaeo- compared with neotropical forests. However, mean stem density is low (426 ± 11 stems ha⁻¹ greater than or equal to 100 mm diameter) compared with both Amazonian and Bornean forests (cf. approx. 600) and is the signature structural feature of African tropical forests. While spatial autocorrelation complicates analyses, AGB shows a positive relationship with rainfall in the driest nine months of the year, and an opposite association with the wettest three months of the year; a negative relationship with temperature; positive relationship with clay-rich soils; and negative relationships with C : N ratio (suggesting a positive soil phosphorus-AGB relationship), and soil fertility computed as the sum of base cations. The results indicate that AGB is mediated by both climate and soils, and suggest that the AGB of African closed-canopy tropical forests may be particularly sensitive to future precipitation and temperature changes.

The 2010 Amazon drought.

In 2010, dry-season rainfall was low across Amazonia, with apparent similarities to the major 2005 drought. We analyzed a decade of satellite-derived rainfall data to compare both events. Standardized anomalies of dry-season rainfall showed that 57% of Amazonia had low rainfall in 2010 as compared with 37% in 2005 (≤-1 standard deviation from long-term mean). By using relationships between drying and forest biomass responses measured for 2005, we predict the impact of the 2010 drought as 2.2 × 10(15) grams of carbon [95% confidence intervals (CIs) are 1.2 and 3.4], largely longer-term committed emissions from drought-induced tree deaths, compared with 1.6 × 10(15) grams of carbon (CIs 0.8 and 2.6) for the 2005 event.

Drought sensitivity of the Amazon rainforest.

Amazon forests are a key but poorly understood component of the global carbon cycle. If, as anticipated, they dry this century, they might accelerate climate change through carbon losses and changed surface energy balances. We used records from multiple long-term monitoring plots across Amazonia to assess forest responses to the intense 2005 drought, a possible analog of future events. Affected forest lost biomass, reversing a large long-term carbon sink, with the greatest impacts observed where the dry season was unusually intense. Relative to pre-2005 conditions, forest subjected to a 100-millimeter increase in water deficit lost 5.3 megagrams of aboveground biomass of carbon per hectare. The drought had a total biomass carbon impact of 1.2 to 1.6 petagrams (1.2 x 10(15) to 1.6 x 10(15) grams). Amazon forests therefore appear vulnerable to increasing moisture stress, with the potential for large carbon losses to exert feedback on climate change.

Low stocks of coarse woody debris in a southwest Amazonian forest.

The stocks and dynamics of coarse woody debris (CWD) are significant components of the carbon cycle within tropical forests. However, to date, there have been no reports of CWD stocks and fluxes from the approximately 1.3 million km(2) of lowland western Amazonian forests. Here, we present estimates of CWD stocks and annual CWD inputs from forests in southern Peru. Total stocks were low compared to other tropical forest sites, whether estimated by line-intercept sampling (24.4 +/- 5.3 Mg ha(-1)) or by complete inventories within 11 permanent plots (17.7 +/- 2.4 Mg ha(-1)). However, annual inputs, estimated from long-term data on tree mortality rates in the same plots, were similar to other studies (3.8 +/- 0.2 or 2.9 +/- 0.2 Mg ha(-1) year(-1), depending on the equation used to estimate biomass). Assuming the CWD pool is at steady state, the turnover time of coarse woody debris is low (4.7 +/- 2.6 or 6.1 +/- 2.6 years). These results indicate that these sites have not experienced a recent, large-scale disturbance event and emphasise the distinctive, rapid nature of carbon cycling in these western Amazonian forests.