Tana E. Wood

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 (CO2) 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.

Urgent need for warming experiments in tropical forests

Although tropical forests account for only a fraction of the planets 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.

Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought.

Global climate models project a decrease in the magnitude of precipitation in tropical regions. Changes in rainfall patterns have important implications for the moisture content and redox status of tropical soils, yet little is known about how these changes may affect microbial community structure. Specifically, does exposure to prior stress confer increased resistance to subsequent perturbation? Here we reduced the quantity of precipitation throughfall to tropical forest soils in the Luquillo Mountains, Puerto Rico. Treatments included newly established throughfall exclusion plots (de novo excluded), plots undergoing reduction for a second time (pre-excluded) and ambient control plots. Ten months of throughfall exclusion led to a small but statistically significant decline in soil water potential and bacterial populations clearly adapted to increased osmotic stress. Although the water potential decline was small and microbial biomass did not change, phylogenetic diversity in the de novo-excluded plots decreased by ∼40% compared with the control plots, yet pre-excluded plots showed no significant change. On the other hand, the relative abundances of bacterial taxa in both the de novo-excluded and pre-excluded plots changed significantly with throughfall exclusion compared with control plots. Changes in bacterial community structure could be explained by changes in soil pore water chemistry and suggested changes in soil redox. Soluble iron declined in treatment plots and was correlated with decreased soluble phosphorus concentrations, which may have significant implications for microbial productivity in these P-limited systems.

Soil nutrient availability and reproductive effort drive patterns in nutrient resorption in Pentaclethra macroloba

The removal of nutrients from senescing tissues, nutrient resorption, is a key strategy for conserving nutrients in plants. However, our understanding of what drives patterns of nutrient resorption in tropical trees is limited. We examined the effects of nutrient sources (stand-level and tree-level soil fertility) and sinks (reproductive effort) on nitrogen (N) and phosphorus (P) resorption. We evaluated resorption efficiency (percentage of original nutrients removed during senescence) and resorption proficiency (indicated by senesced-leaf nutrient concentrations) in a symbiotic N-fixing tree species, Pentaclethra macroloba, common to tropical forests in Costa Rica. Although tree-level soil P alone did not drive patterns in nutrient resorption, P efficiency and proficiency declined with increasing tree-level soil P when reproductive status was also considered. Nutrient resorption declined with increasing tree-level soil P in trees that were actively fruiting or that experienced high seedfall the year prio...

Sensitivity of soil respiration to variability in soil moisture and temperature in a humid tropical forest.

Precipitation and temperature are important drivers of soil respiration. The role of moisture and temperature are generally explored at seasonal or inter-annual timescales; however, significant variability also occurs on hourly to daily time-scales. We used small (1.54 m2), throughfall exclusion shelters to evaluate the role soil moisture and temperature as temporal controls on soil CO2 efflux from a humid tropical forest in Puerto Rico. We measured hourly soil CO2 efflux, temperature and moisture in control and exclusion plots (n = 6) for 6-months. The variance of each time series was analyzed using orthonormal wavelet transformation and Haar-wavelet coherence. We found strong negative coherence between soil moisture and soil respiration in control plots corresponding to a two-day periodicity. Across all plots, there was a significant parabolic relationship between soil moisture and soil CO2 efflux with peak soil respiration occurring at volumetric soil moisture of approximately 0.375 m3/m3. We additionally found a weak positive coherence between CO2 and temperature at longer time-scales and a significant positive relationship between soil temperature and CO2 efflux when the analysis was limited to the control plots. The coherence between CO2 and both temperature and soil moisture were reduced in exclusion plots. The reduced CO2 response to temperature in exclusion plots suggests that the positive effect of temperature on CO2 is constrained by soil moisture availability.

Biotic and abiotic controls on diurnal fluctuations in labile soil phosphorus of a wet tropical forest

The productivity of many tropical wet forests is generally limited by bioavailable phosphorus (P). Microbial activity is a key regulator of P availability in that it determines both the supply of P through organic matter decomposition and the depletion of bioavailable P through microbial uptake. Both microbial uptake and mineralization occur rapidly, and their net effect on P availability varies with soil moisture, temperature, and soil organic matter quantity and quality. Exploring the mechanisms driving P availability at fine temporal scales can provide insight into the coupling of carbon, water, and nutrient cycles, and ultimately, the response of tropical forests to climate change. Despite the recognized importance of P cycling to the dynamics of wet tropical forests and their potential sensitivity to short-term fluctuations in bioavailable P, the diurnal pattern of P remains poorly understood. This study quantifies diurnal fluctuations in labile soil P and evaluates the importance of biotic and abiotic factors in driving these patterns. To this end, measurements of labile P were made every other hour in a Costa Rican wet tropical forest oxisol. Spatial and temporal variation in Bray-extractable P were investigated in relation to ecosystem carbon flux, soil CO2 efflux, soil moisture, soil temperature, solar radiation, and sap-flow velocity. Spatially averaged bi-hourly (every two hours) labile P ranged from 0.88 to 2.48 microg/g across days. The amplitude in labile P throughout the day was 0.61-0.82 microg/g (41-54% of mean P concentrations) and was characterized by a bimodal pattern with a decrease at midday. Labile P increased with soil CO2 efflux and soil temperature and declined with increasing sap flow and solar radiation. Together, soil CO2 efflux, soil temperature, and sap flow explained 86% of variation in labile P.

Belowground Response to Drought in a Tropical Forest Soil. I. Changes in Microbial Functional Potential and Metabolism

Global climate models predict a future of increased severity of drought in many tropical forests. Soil microbes are central to the balance of these systems as sources or sinks of atmospheric carbon (C), yet how they respond metabolically to drought is not well-understood. We simulated drought in the typically aseasonal Luquillo Experimental Forest, Puerto Rico, by intercepting precipitation falling through the forest canopy. This approach reduced soil moisture by 13% and water potential by 0.14 MPa (from -0.2 to -0.34). Previous results from this experiment have demonstrated that the diversity and composition of these soil microbial communities are sensitive to even small changes in soil water. Here, we show prolonged drought significantly alters the functional potential of the community and provokes a clear osmotic stress response, including the production of compatible solutes that increase intracellular C demand. Subsequently, a microbial population emerges with a greater capacity for extracellular enzyme production targeting macromolecular carbon. Significantly, some of these drought-induced functional shifts in the soil microbiota are attenuated by prior exposure to a short-term drought suggesting that acclimation may occur despite a lack of longer-term drought history.

Tropical forests in a warming world.

Global models suggest tropical forests could face significant and unprecedented warming within the next two decades (Diffenbaugh & Scherer, 2011). These findings, combined with evidence that tropical forests may be near a high temperature threshold, suggest that these systems may be more vulnerable to climate change than previously believed (Clark et al., 2003; Doughty & Goulden, 2008). Currently, our ability to predict tropical forest responses to rising temperatures is limited, due in large part to a lack of data on tropical forest and tree processes (Saxe et al., 2001). Given the immense amount of carbon (C) cycled through these forests, even a slight change to tropical net C fluxes could have significant consequences for global C cycling and future climate. The organized oral session From Leaf to Biosphere: The Effects of a Warming Climate on Tropical Forests at the 2011 Ecological Society of America meeting in Austin, Texas brought together 10 scientists from a range of fields to synthesize existing data on tropical forest responses to increasing temperature and to facilitate cross-disciplinary dialogue. These scientists presented research and offered perspectives spanning molecular to global scales (Fig. 1). Here, we synthesize the key conclusions.

Infrared heater system for warming tropical forest understory plants and soils

Abstract 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.

Evaluating the Classical Versus an Emerging Conceptual Model of Peatland Methane Dynamics

We appreciate discussions with M. Firestone and S. Blazewicz. We received assistance in the field and lab from K. Smetak, H. Dang, and A. McDowell. This research was funded by grants to W.L.S. from the U.S. National Science Foundation (ATM-0842385 and DEB-0543558) and the California Department of Fish and Wildlife (CDFW) and California Department of Water Resources (DWR) contract 4600011240. The data used are listed in the references, tables, supporting information, and the Illinois Digital Environment for Access to Learning and Scholarship (IDEALS) repository at https://www.ideals.illinois.edu/.