Linking physiology, epidemiology, and demography: Understanding how lianas outcompete trees in a changing world.

Extending and safeguarding tropical forest ecosystems is critical for combating climate change and biodiversity loss. One of its constituents, lianas, is spreading and increasing in abundance on a global scale. This is particularly concerning as lianas negatively impact forests' carbon fluxes, dynamics, and overall resilience, potentially exacerbating both crises. While possibly linked to climate-change-induced atmospheric CO2 elevation and drought intensification, the reasons behind their increasing abundance remain elusive. Prior research shows distinct physiological differences between lianas and trees, but it is unclear whether these differences confer a demographic advantage to lianas with climate change. Guided by extensive datasets collected in Panamanian tropical forests, we developed a tractable model integrating physiology, demography, and epidemiology. Our findings suggest that CO2 fertilization, a climate change factor promoting forest productivity, gives lianas a demographic advantage. Conversely, factors such as extreme drought generally cause a decrease in liana prevalence. Such a decline in liana prevalence is expected from a physiological point of view because lianas have drought-sensitive traits. However, our analysis underscores the importance of not exclusively relying on physiological processes, as interactions with demographic mechanisms (i.e., the forest structure) can contrast these expectations, causing an increase in lianas with drought. Similarly, our results emphasize that identical physiological responses between lianas and trees still lead to liana increase. Even if lianas exhibit collinear but weaker responses in their performance compared to trees, a temporary liana prevalence increase might manifest driven by the faster response time of lianas imposed by their distinct life-history strategies than trees.

Global increase of lianas in tropical forests.

Lianas profoundly affect tropical forests dynamics, reducing productivity and carbon storage, which underscores the importance of monitoring change in their abundance in projecting the future of the global terrestrial carbon store. While increasing liana populations are documented within the Neotropics, the global consistency of these patterns is questioned, and remains to be determined. To evaluate pantropical trends in liana abundance comprehensively and quantitatively, we conducted a systematic literature review and meta-analysis. This approach allowed us to synthesize data from published longitudinal studies examining liana trends across the tropics. We calculated standardized effect sizes and standard errors, and applied a Bayesian hierarchical meta-analytic model to adjust for publication bias. Our analysis reveals an overall pan-tropical increase in lianas abundance, occurring at an average rate of 1.7 ± 0.7 SE% per year (~10% to 24% per decade). This upward trend, confirmed to be robust against publication bias, extends beyond Neotropical regions, indicating a widespread phenomenon. Although a global trend of increasing liana abundance is evident, significant local variation exist, attributable to differences in life cycle stages, abundance metrics, forest successional stages, and biogeographical realms. Notably, increases in stem density of saplings and biomass of canopy lianas, especially in old-growth forests, point to global climatic drivers and heightened turnover rates in tropical forests as factors promoting sustained liana growth in the canopy and clonal colonization in the understory. These trends suggest that the rise in liana abundance may not only persist but could also intensify under climate change. Considering both previous and current research on lianas, our findings confirm growing concerns about lianas' expanding impact on pan-tropical carbon storage, highlighting their significant potential effect on global carbon dynamics.

Liana optical traits increase tropical forest albedo and reduce ecosystem productivity.

Lianas are a key growth form in tropical forests. Their lack of self-supporting tissues and their vertical position on top of the canopy make them strong competitors of resources. A few pioneer studies have shown that liana optical traits differ on average from those of colocated trees. Those trait discrepancies were hypothesized to be responsible for the competitive advantage of lianas over trees. Yet, in the absence of reliable modelling tools, it is impossible to unravel their impact on the forest energy balance, light competition, and on the liana success in Neotropical forests. To bridge this gap, we performed a meta-analysis of the literature to gather all published liana leaf optical spectra, as well as all canopy spectra measured over different levels of liana infestation. We then used a Bayesian data assimilation framework applied to two radiative transfer models (RTMs) covering the leaf and canopy scales to derive tropical tree and liana trait distributions, which finally informed a full dynamic vegetation model. According to the RTMs inversion, lianas grew thinner, more horizontal leaves with lower pigment concentrations. Those traits made the lianas very efficient at light interception and significantly modified the forest energy balance and its carbon cycle. While forest albedo increased by 14% in the shortwave, light availability was reduced in the understorey (-30% of the PAR radiation) and soil temperature decreased by 0.5°C. Those liana-specific traits were also responsible for a significant reduction of tree (-19%) and ecosystem (-7%) gross primary productivity (GPP) while lianas benefited from them (their GPP increased by +27%). This study provides a novel mechanistic explanation to the increase in liana abundance, new evidence of the impact of lianas on forest functioning, and paves the way for the evaluation of the large-scale impacts of lianas on forest biogeochemical cycles.

Century-long apparent decrease in intrinsic water-use efficiency with no evidence of progressive nutrient limitation in African tropical forests.

Forests exhibit leaf- and ecosystem-level responses to environmental changes. Specifically, rising carbon dioxide (CO2 ) levels over the past century are expected to have increased the intrinsic water-use efficiency (iWUE) of tropical trees while the ecosystem is gradually pushed into progressive nutrient limitation. Due to the long-term character of these changes, however, observational datasets to validate both paradigms are limited in space and time. In this study, we used a unique herbarium record to go back nearly a century and show that despite the rise in CO2 concentrations, iWUE has decreased in central African tropical trees in the Congo Basin. Although we find evidence that points to leaf-level adaptation to increasing CO2 -that is, increasing photosynthesis-related nutrients and decreasing maximum stomatal conductance, a decrease in leaf δ13 C clearly indicates a decreasing iWUE over time. Additionally, the stoichiometric carbon to nitrogen and nitrogen to phosphorus ratios in the leaves show no sign of progressive nutrient limitation as they have remained constant since 1938, which suggests that nutrients have not increasingly limited productivity in this biome. Altogether, the data suggest that other environmental factors, such as increasing temperature, might have negatively affected net photosynthesis and consequently downregulated the iWUE. Results from this study reveal that the second largest tropical forest on Earth has responded differently to recent environmental changes than expected, highlighting the need for further on-ground monitoring in the Congo Basin.

Unraveling the relative role of light and water competition between lianas and trees in tropical forests: A vegetation model analysis.

Despite their low contribution to forest carbon stocks, lianas (woody vines) play an important role in the carbon dynamics of tropical forests. As structural parasites, they hinder tree survival, growth and fecundity; hence, they negatively impact net ecosystem productivity and long-term carbon sequestration.Competition (for water and light) drives various forest processes and depends on the local abundance of resources over time. However, evaluating the relative role of resource availability on the interactions between lianas and trees from empirical observations is particularly challenging. Previous approaches have used labour-intensive and ecosystem-scale manipulation experiments, which are infeasible in most situations.We propose to circumvent this challenge by evaluating the uncertainty of water and light capture processes of a process-based vegetation model (ED2) including the liana growth form. We further developed the liana plant functional type in ED2 to mechanistically simulate water uptake and transport from roots to leaves, and start the model from prescribed initial conditions. We then used the PEcAn bioinformatics platform to constrain liana parameters and run uncertainty analyses.Baseline runs successfully reproduced ecosystem gas exchange fluxes (gross primary productivity and latent heat) and forest structural features (leaf area index, aboveground biomass) in two sites (Barro Colorado Island, Panama and Paracou, French Guiana) characterized by different rainfall regimes and levels of liana abundance.Model uncertainty analyses revealed that water limitation was the factor driving the competition between trees and lianas at the drier site (BCI), and during the relatively short dry season of the wetter site (Paracou). In young patches, light competition dominated in Paracou but alternated with water competition between the wet and the dry season on BCI according to the model simulations.The modelling workflow also identified key liana traits (photosynthetic quantum efficiency, stomatal regulation parameters, allometric relationships) and processes (water use, respiration, climbing) driving the model uncertainty. They should be considered as priorities for future data acquisition and model development to improve predictions of the carbon dynamics of liana-infested forests. Synthesis. Competition for water plays a larger role in the interaction between lianas and trees than previously hypothesized, as demonstrated by simulations from a process-based vegetation model.