Experimental warming and its legacy effects on root dynamics following two hurricane disturbances in a wet tropical forest.

Tropical forests are expected to experience unprecedented warming and increases in hurricane disturbances in the coming decades; yet, our understanding of how these productive systems, especially their belowground component, will respond to the combined effects of varied environmental changes remains empirically limited. Here we evaluated the responses of root dynamics (production, mortality, and biomass) to soil and understory warming (+4°C) and after two consecutive tropical hurricanes in our in situ warming experiment in a tropical forest of Puerto Rico: Tropical Responses to Altered Climate Experiment (TRACE). We collected minirhizotron images from three warmed plots and three control plots of 12 m2 . Following Hurricanes Irma and María in September 2017, the infrared heater warming treatment was suspended for repairs, which allowed us to explore potential legacy effects of prior warming on forest recovery. We found that warming significantly reduced root production and root biomass over time. Following hurricane disturbance, both root biomass and production increased substantially across all plots; the root biomass increased 2.8-fold in controls but only 1.6-fold in previously warmed plots. This pattern held true for both herbaceous and woody roots, suggesting that the consistent antecedent warming conditions reduced root capacity to recover following hurricane disturbance. Root production and mortality were both related to soil ammonium nitrogen and microbial biomass nitrogen before and after the hurricanes. This experiment has provided an unprecedented look at the complex interactive effects of disturbance and climate change on the root component of a tropical forested ecosystem. A decrease in root production in a warmer world and slower root recovery after a major hurricane disturbance, as observed here, are likely to have longer-term consequences for tropical forest responses to future global change.

Experimental warming across a tropical forest canopy height gradient reveals minimal photosynthetic and respiratory acclimation.

Tropical forest canopies cycle vast amounts of carbon, yet we still have a limited understanding of how these critical ecosystems will respond to climate warming. We implemented in situ leaf-level + 3°C experimental warming from the understory to the upper canopy of two Puerto Rican tropical tree species, Guarea guidonia and Ocotea sintenisii. After approximately 1 month of continuous warming, we assessed adjustments in photosynthesis, chlorophyll fluorescence, stomatal conductance, leaf traits and foliar respiration. Warming did not alter net photosynthetic temperature response for either species; however, the optimum temperature of Ocotea understory leaf photosynthetic electron transport shifted upward. There was no Ocotea respiratory treatment effect, while Guarea respiratory temperature sensitivity (Q10 ) was down-regulated in heated leaves. The optimum temperatures for photosynthesis (Topt ) decreased 3-5°C from understory to the highest canopy position, perhaps due to upper canopy stomatal conductance limitations. Guarea upper canopy Topt was similar to the mean daytime temperatures, while Ocotea canopy leaves often operated above Topt . With minimal acclimation to warmer temperatures in the upper canopy, further warming could put these forests at risk of reduced CO2 uptake, which could weaken the overall carbon sink strength of this tropical forest.

Tropical understory herbaceous community responds more strongly to hurricane disturbance than to experimental warming.

The effects of climate change on tropical forests may have global consequences due to the forests' high biodiversity and major role in the global carbon cycle. In this study, we document the effects of experimental warming on the abundance and composition of a tropical forest floor herbaceous plant community in the Luquillo Experimental Forest, Puerto Rico. This study was conducted within Tropical Responses to Altered Climate Experiment (TRACE) plots, which use infrared heaters under free-air, open-field conditions, to warm understory vegetation and soils + 4°C above nearby control plots. Hurricanes Irma and María damaged the heating infrastructure in the second year of warming, therefore, the study included one pretreatment year, one year of warming, and one year of hurricane response with no warming. We measured percent leaf cover of individual herbaceous species, fern population dynamics, and species richness and diversity within three warmed and three control plots. Results showed that one year of experimental warming did not significantly affect the cover of individual herbaceous species, fern population dynamics, species richness, or species diversity. In contrast, herbaceous cover increased from 20% to 70%, bare ground decreased from 70% to 6%, and species composition shifted pre to posthurricane. The negligible effects of warming may have been due to the short duration of the warming treatment or an understory that is somewhat resistant to higher temperatures. Our results suggest that climate extremes that are predicted to increase with climate change, such as hurricanes and droughts, may cause more abrupt changes in tropical forest understories than longer-term sustained warming.

Altered climate leads to positive density-dependent feedbacks in a tropical wet forest.

Climate change is predicted to result in warmer and drier Neotropical forests relative to current conditions. Negative density-dependent feedbacks, mediated by natural enemies, are key to maintaining the high diversity of tree species found in the tropics, yet we have little understanding of how projected changes in climate are likely to affect these critical controls. Over 3 years, we evaluated the effects of a natural drought and in situ experimental warming on density-dependent feedbacks on seedling demography in a wet tropical forest in Puerto Rico. In the +4°C warming treatment, we found that seedling survival increased with increasing density of the same species (conspecific). These positive density-dependent feedbacks were not associated with a decrease in aboveground natural enemy pressure. If positive density-dependent feedbacks are not transient, the diversity of tropical wet forests, which may rely on negative density dependence to drive diversity, could decline in a future warmer, drier world.

Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale.

The temperature response of photosynthesis is one of the key factors determining predicted responses to warming in global vegetation models (GVMs). The response may vary geographically, owing to genetic adaptation to climate, and temporally, as a result of acclimation to changes in ambient temperature. Our goal was to develop a robust quantitative global model representing acclimation and adaptation of photosynthetic temperature responses. We quantified and modelled key mechanisms responsible for photosynthetic temperature acclimation and adaptation using a global dataset of photosynthetic CO2 response curves, including data from 141 C3 species from tropical rainforest to Arctic tundra. We separated temperature acclimation and adaptation processes by considering seasonal and common-garden datasets, respectively. The observed global variation in the temperature optimum of photosynthesis was primarily explained by biochemical limitations to photosynthesis, rather than stomatal conductance or respiration. We found acclimation to growth temperature to be a stronger driver of this variation than adaptation to temperature at climate of origin. We developed a summary model to represent photosynthetic temperature responses and showed that it predicted the observed global variation in optimal temperatures with high accuracy. This novel algorithm should enable improved prediction of the function of global ecosystems in a warming climate.

Infrared heater system for warming tropical forest understory plants and soils.

The response of tropical forests to global warming is one of the largest uncertainties in predicting the future carbon balance of Earth. To determine the likely effects of elevated temperatures on tropical forest understory plants and soils, as well as other ecosystems, an infrared (IR) heater system was developed to provide in situ warming for the Tropical Responses to Altered Climate Experiment (TRACE) in the Luquillo Experimental Forest in Puerto Rico. Three replicate heated 4-m-diameter plots were warmed to maintain a 4°C increase in understory vegetation compared to three unheated control plots, as sensed by IR thermometers. The equipment was larger than any used previously and was subjected to challenges different from those of many temperate ecosystem warming systems, including frequent power surges and outages, high humidity, heavy rains, hurricanes, saturated clayey soils, and steep slopes. The system was able to maintain the target 4.0°C increase in hourly average vegetation temperatures to within ± 0.1°C. The vegetation was heterogeneous and on a 21° slope, which decreased uniformity of the warming treatment on the plots; yet, the green leaves were fairly uniformly warmed, and there was little difference among 0-10 cm depth soil temperatures at the plot centers, edges, and midway between. Soil temperatures at the 40-50 cm depth increased about 3°C compared to the controls after a month of warming. As expected, the soil in the heated plots dried faster than that of the control plots, but the average soil moisture remained adequate for the plants. The TRACE heating system produced an adequately uniform warming precisely controlled down to at least 50-cm soil depth, thereby creating a treatment that allows for assessing mechanistic responses of tropical plants and soil to warming, with applicability to other ecosystems. No physical obstacles to scaling the approach to taller vegetation (i.e., trees) and larger plots were observed.

Tropical rainforest carbon sink declines during El Niño as a result of reduced photosynthesis and increased respiration rates.

Changes in tropical forest carbon sink strength during El Niño Southern Oscillation (ENSO) events can indicate future behavior under climate change. Previous studies revealed ˜6 Mg C ha-1  yr-1 lower net ecosystem production (NEP) during ENSO year 1998 compared with non-ENSO year 2000 in a Costa Rican tropical rainforest. We explored environmental drivers of this change and examined the contributions of ecosystem respiration (RE) and gross primary production (GPP) to this weakened carbon sink. For 1998-2000, we estimated RE using chamber-based respiration measurements, and we estimated GPP in two ways: using (1) the canopy process model MAESTRA, and (2) combined eddy covariance and chamber respiration data. MAESTRA-estimated GPP did not statistically differ from GPP estimated using approach 2, but was ˜ 28% greater than published GPP estimates for the same site and years using eddy covariance data only. A 7% increase in RE (primarily increased soil respiration) and a 10% reduction in GPP contributed equally to the difference in NEP between ENSO year 1998 and non-ENSO year 2000. A warming and drying climate for tropical forests may yield a weakened carbon sink from both decreased GPP and increased RE. Understanding physiological acclimation will be critical for the large carbon stores in these ecosystems.

Vertical leaf mass per area gradient of mature sugar maple reflects both height-driven increases in vascular tissue and light-driven increases in palisade layer thickness.

A key trait used in canopy and ecosystem function modeling, leaf mass per area (LMA), is influenced by changes in both leaf thickness and leaf density (LMA = Thickness × Density). In tall trees, LMA is understood to increase with height through two primary mechanisms: (i) increasing palisade layer thickness (and thus leaf thickness) in response to light and/or (ii) reduced cell expansion and intercellular air space in response to hydrostatic constraints, leading to increased leaf density. Our objective was to investigate within-canopy gradients in leaf anatomical traits in order to understand environmental factors that influence leaf morphology in a sugar maple (Acer saccharum Marshall) forest canopy. We teased apart the effects of light and height on anatomical traits by sampling at exposed and closed canopies that had different light conditions at similar heights. As expected, palisade layer thickness responded strongly to cumulative light exposure. Mesophyll porosity, however, was weakly and negatively correlated with light and height (i.e., hydrostatic gradients). Reduced mesophyll porosity was not likely caused by limitations on cell expansion; in fact, epidermal cell width increased with height. Palisade layer thickness was better related to LMA, leaf density and leaf thickness than was mesophyll porosity. Vein diameter and fraction of vascular tissue also increased with height and LMA, density and thickness, revealing that greater investment in vascular and support tissue may be a third mechanism for increased LMA with height. Overall, decreasing mesophyll porosity with height was likely due to palisade cells expanding into the available air space and also greater investments in vascular and support tissue, rather than a reduction of cell expansion due to hydrostatic constraints. Our results provide evidence that light influences both palisade layer thickness and mesophyll porosity and indicate that hydrostatic gradients influence leaf vascular and support tissues in mature Acer saccharum trees.

How vertical patterns in leaf traits shift seasonally and the implications for modeling canopy photosynthesis in a temperate deciduous forest.

Leaf functional traits are used in modeling forest canopy photosynthesis (Ac) due to strong correlations between photosynthetic capacity, leaf mass per area (LMA) and leaf nitrogen per area (Narea). Vertical distributions of these traits may change over time in temperate deciduous forests as a result of acclimation to light, which may result in seasonal changes in Ac To assess both spatial and temporal variations in key traits, we measured vertical profiles of Narea and LMA from leaf expansion through leaf senescence in a sugar maple (Acer saccharum Marshall) forest. To investigate mechanisms behind coordinated changes in leaf morphology and function, we also measured vertical variation in leaf carbon isotope composition (δ(13)C), predawn turgor pressure, leaf water potential and osmotic potential. Finally, we assessed potential biases in Ac estimations by parameterizing models with and without vertical and seasonal Narea variations following leaf expansion. Our data are consistent with the hypothesis that hydrostatic constraints on leaf morphology drive the vertical increase in LMA with height early in the growing season; however, LMA in the upper canopy continued to increase over time during light acclimation, indicating that light is primarily driving gradients in LMA later in the growing season. Models with no seasonal variation in Narea overestimated Ac by up to 11% early in the growing season, while models with no vertical variation in Narea overestimated Ac by up to 60% throughout the season. According to the multilayer model, the upper 25% of leaf area contributed to over 50% of Ac, but when gradients of intercellular CO2, as estimated from δ(13)C, were accounted for, the upper 25% of leaf area contributed to 26% of total Ac Our results suggest that ignoring vertical variation of key traits can lead to considerable overestimation of Ac.

Convergent Evolution towards High Net Carbon Gain Efficiency Contributes to the Shade Tolerance of Palms (Arecaceae).

Most palm species occur in the shaded lower strata of tropical rain forests, but how their traits relate to shade adaptation is poorly understood. We hypothesized that palms are adapted to the shade of their native habitats by convergent evolution towards high net carbon gain efficiency (CGEn), which is given by the maximum photosynthetic rate to dark respiration rate ratio. Leaf mass per area, maximum photosynthetic rate, dark respiration and N and P concentrations were measured in 80 palm species grown in a common garden, and combined with data of 30 palm species growing in their native habitats. Compared to other species from the global leaf economics data, dicotyledonous broad-leaved trees in tropical rainforest or other monocots in the global leaf economics data, palms possessed consistently higher CGEn, achieved by lowered dark respiration and fairly high foliar P concentration. Combined phylogenetic analyses of evolutionary signal and trait evolution revealed convergent evolution towards high CGEn in palms. We conclude that high CGEn is an evolutionary strategy that enables palms to better adapt to shady environments than coexisting dicot tree species, and may convey advantages in competing with them in the tropical forest understory. These findings provide important insights for understanding the evolution and ecology of palms, and for understanding plant shade adaptations of lower rainforest strata. Moreover, given the dominant role of palms in tropical forests, these findings are important for modelling carbon and nutrient cycling in tropical forest ecosystems.

Urgent need for warming experiments in tropical forests.

Although tropical forests account for only a fraction of the planet's terrestrial surface, they exchange more carbon dioxide with the atmosphere than any other biome on Earth, and thus play a disproportionate role in the global climate. In the next 20 years, the tropics will experience unprecedented warming, yet there is exceedingly high uncertainty about their potential responses to this imminent climatic change. Here, we prioritize research approaches given both funding and logistical constraints in order to resolve major uncertainties about how tropical forests function and also to improve predictive capacity of earth system models. We investigate overall model uncertainty of tropical latitudes and explore the scientific benefits and inevitable trade-offs inherent in large-scale manipulative field experiments. With a Coupled Model Intercomparison Project Phase 5 analysis, we found that model variability in projected net ecosystem production was nearly 3 times greater in the tropics than for any other latitude. Through a review of the most current literature, we concluded that manipulative warming experiments are vital to accurately predict future tropical forest carbon balance, and we further recommend the establishment of a network of comparable studies spanning gradients of precipitation, edaphic qualities, plant types, and/or land use change. We provide arguments for long-term, single-factor warming experiments that incorporate warming of the most biogeochemically active ecosystem components (i.e. leaves, roots, soil microbes). Hypothesis testing of underlying mechanisms should be a priority, along with improving model parameterization and constraints. No single tropical forest is representative of all tropical forests; therefore logistical feasibility should be the most important consideration for locating large-scale manipulative experiments. Above all, we advocate for multi-faceted research programs, and we offer arguments for what we consider the most powerful and urgent way forward in order to improve our understanding of tropical forest responses to climate change.

Light acclimation optimizes leaf functional traits despite height-related constraints in a canopy shading experiment.

Within-canopy gradients of leaf functional traits have been linked to both light availability and vertical gradients in leaf water potential. While observational studies can reveal patterns in leaf traits, within-canopy experimental manipulations can provide mechanistic insight to tease apart multiple interacting drivers. Our objectives were to disentangle effects of height and light environment on leaf functional traits by experimentally shading branches along vertical gradients within a sugar maple (Acer saccharum) forest. Shading reduced leaf mass per area (LMA), leaf density, area-based leaf nitrogen (N(area)), and carbon:nitrogen (C:N) ratio, and increased mass-based leaf nitrogen (N(mass)), highlighting the importance of light availability on leaf morphology and chemistry. Early in the growing season, midday leaf water potential (Ψ(mid)), LMA, and N(area) were driven primarily by height; later in the growing season, light became the most important driver for LMA and Narea. Carbon isotope composition (δ(13)C) displayed strong, linear correlations with height throughout the growing season, but did not change with shading, implying that height is more influential than light on water use efficiency and stomatal behavior. LMA, leaf density, N(mass), C:N ratio, and δ(13)C all changed seasonally, suggesting that leaf ageing effects on leaf functional traits are equally as important as microclimatic conditions. Overall, our results indicate that: (1) stomatal sensitivity to vapor pressure deficit or Ψ(mid) constrains the supply of CO2 to leaves at higher heights, independent of light environment, and (2) LMA and N(area) distributions become functionally optimized through morphological acclimation to light with increasing leaf age despite height-related constraints.

Light drives vertical gradients of leaf morphology in a sugar maple (Acer saccharum) forest.

Leaf mass per area (LMA, g m(-2)) is an essential trait for modeling canopy function due to its strong association with photosynthesis, respiration and leaf nitrogen. Leaf mass per area, which is influenced by both leaf thickness and density (LMA = thickness × density), generally increases from the bottom to the top of tree canopies, yet the mechanisms behind this universal pattern are not yet resolved. For decades, the light environment was assumed to be the most influential driver of within-canopy variation in LMA, yet recent evidence has shown hydrostatic gradients to be more important in upper canopy positions, especially in tall evergreen trees in temperate and tropical forests. The aim of this study was to disentangle the importance of various environmental drivers on vertical LMA gradients in a mature sugar maple (Acer saccharum Marshall) forest. We compared LMA, leaf density and leaf thickness relationships with height, light and predawn leaf water potential (ΨPre) within a closed and an exposed canopy to assess leaf morphological traits at similar heights but different light conditions. Contrary to our expectations and recent findings in the literature, we found strong evidence that light was the primary driver of vertical gradients in leaf morphology. At similar heights (13-23 m), LMA was greater within the exposed canopy than the closed canopy, and light had a stronger influence over LMA compared with ΨPre. Light also had a stronger influence over both leaf thickness and density compared with ΨPre; however, the increase in LMA within both canopy types was primarily due to increasing leaf thickness with increasing light availability. This study provides strong evidence that canopy structure and crown exposure, in addition to height, should be considered as a parameter for determining vertical patterns in LMA and modeling canopy function.

Native trees show conservative water use relative to invasive trees: results from a removal experiment in a Hawaiian wet forest.

While the supply of freshwater is expected to decline in many regions in the coming decades, invasive plant species, often 'high water spenders', are greatly expanding their ranges worldwide. In this study, we quantified the ecohydrological differences between native and invasive trees and also the effects of woody invasive removal on plot-level water use in a heavily invaded mono-dominant lowland wet tropical forest on the Island of Hawaii. We measured transpiration rates of co-occurring native and invasive tree species with and without woody invasive removal treatments. Twenty native Metrosideros polymorpha and 10 trees each of three invasive species, Cecropia obtusifolia, Macaranga mappa and Melastoma septemnervium, were instrumented with heat-dissipation sap-flux probes in four 100 m(2) plots (two invaded, two removal) for 10 months. In the invaded plots, where both natives and invasives were present, Metrosideros had the lowest sap-flow rates per unit sapwood, but the highest sap-flow rates per whole tree, owing to its larger mean diameter than the invasive trees. Stand-level water use within the removal plots was half that of the invaded plots, even though the removal of invasives caused a small but significant increase in compensatory water use by the remaining native trees. By investigating the effects of invasive species on ecohydrology and comparing native vs. invasive physiological traits, we not only gain understanding about the functioning of invasive species, but we also highlight potential water-conservation strategies for heavily invaded mono-dominant tropical forests worldwide. Native-dominated forests free of invasive species can be conservative in overall water use, providing a strong rationale for the control of invasive species and preservation of native-dominated stands.

Tropical forest carbon balance in a warmer world: a critical review spanning microbial- to ecosystem-scale processes.

Tropical forests play a major role in regulating global carbon (C) fluxes and stocks, and even small changes to C cycling in this productive biome could dramatically affect atmospheric carbon dioxide (CO(2) ) concentrations. Temperature is expected to increase over all land surfaces in the future, yet we have a surprisingly poor understanding of how tropical forests will respond to this significant climatic change. Here we present a contemporary synthesis of the existing data and what they suggest about how tropical forests will respond to increasing temperatures. Our goals were to: (i) determine whether there is enough evidence to support the conclusion that increased temperature will affect tropical forest C balance; (ii) if there is sufficient evidence, determine what direction this effect will take; and, (iii) establish what steps should to be taken to resolve the uncertainties surrounding tropical forest responses to increasing temperatures. We approach these questions from a mass-balance perspective and therefore focus primarily on the effects of temperature on inputs and outputs of C, spanning microbial- to ecosystem-scale responses. We found that, while there is the strong potential for temperature to affect processes related to C cycling and storage in tropical forests, a notable lack of data combined with the physical, biological and chemical diversity of the forests themselves make it difficult to resolve this issue with certainty. We suggest a variety of experimental approaches that could help elucidate how tropical forests will respond to warming, including large-scale in situ manipulation experiments, longer term field experiments, the incorporation of a range of scales in the investigation of warming effects (both spatial and temporal), as well as the inclusion of a diversity of tropical forest sites. Finally, we highlight areas of tropical forest research where notably few data are available, including temperature effects on: nutrient cycling, heterotrophic versus autotrophic respiration, thermal acclimation versus substrate limitation of plant and microbial communities, below-ground C allocation, species composition (plant and microbial), and the hydraulic architecture of roots. Whether or not tropical forests will become a source or a sink of C in a warmer world remains highly uncertain. Given the importance of these ecosystems to the global C budget, resolving this uncertainty is a primary research priority.

Comparative water use of native and invasive plants at multiple scales: a global meta-analysis.

Ecohydrology and invasive ecology have become increasingly important in the context of global climate change. This study presents the first in-depth analysis of the water use of invasive and native plants of the same growth form at multiple scales: leaf, plant, and ecosystem. We reanalyzed data for several hundred native and invasive species from over 40 published studies worldwide to glean global trends and to highlight how patterns vary depending on both scale and climate. We analyzed all pairwise combinations of co-occurring native and invasive species for higher comparative resolution of the likelihood of an invasive species using more water than a native species and tested for significance using bootstrap methods. At each scale, we found several-fold differences in water use between specific paired invasive and native species. At the leaf scale, we found a strong tendency for invasive species to have greater stomatal conductance than native species. At the plant scale, however, natives and invasives were equally likely to have the higher sap flow rates. Available data were much fewer for the ecosystem scale; nevertheless, we found that invasive-dominated ecosystems were more likely to have higher sap flow rates per unit ground area than native-dominated ecosystems. Ecosystem-scale evapotranspiration, on the other hand, was equally likely to be greater for systems dominated by invasive and native species of the same growth form. The inherent disconnects in the determination of water use when changing scales from leaf to plant to ecosystem reveal hypotheses for future studies and a critical need for more ecosystem-scale water use measurements in invasive- vs. native-dominated systems. The differences in water use of native and invasive species also depended strongly on climate, with the greater water use of invasives enhanced in hotter, wetter climates at the coarser scales.