Leafcutter ants enhance microbial drought resilience in tropical forest soil.

We conducted a research campaign in a neotropical rainforest in Costa Rica throughout the drought phase of an El-Nino Southern Oscillation event to determine microbial community dynamics and soil C fluxes. Our study included nests of the leafcutter ant Atta cephalotes, as soil disturbances made by these ecosystem engineers may influence microbial drought response. Drought decreased the diversity of microbes and the abundance of core microbiome taxa, including Verrucomicrobial bacteria and Sordariomycete fungi. Despite initial responses of decreasing diversity and altered composition, 6 months post-drought the microbiomes were similar to pre-drought conditions, demonstrating the resilience of soil microbial communities to drought events. A. cephalotes nests altered fungal composition in the surrounding soil, and reduced both fungal mortality and growth of Acidobacteria post-drought. Drought increased CH4 consumption in soils due to lower soil moisture, and A. cephalotes nests decrease the variability of CH4 emissions in some soil types. CH4 emissions were tracked by the abundance of methanotrophic bacteria and fungal composition. These results characterize the microbiome of tropical soils across both time and space during drought and provide evidence for the importance of leafcutter ant nests in shaping soil microbiomes and enhancing microbial resilience during climatic perturbations.

Systematic approaches to assessing high-temperature limits to fertility in animals.

Critical thermal limits (CTLs) gauge the physiological impact of temperature on survival or critical biological function, aiding predictions of species range shifts and climatic resilience. Two recent Drosophila species studies, using similar approaches to determine temperatures that induce sterility (thermal fertility limits [TFLs]), reveal that TFLs are often lower than CTLs and that TFLs better predict both current species distributions and extinction probability. Moreover, many studies show fertility is more sensitive at less extreme temperatures than survival (thermal sensitivity of fertility [TSF]). These results present a more pessimistic outlook on the consequences of climate change. However, unlike CTLs, TFL data are limited to Drosophila, and variability in TSF methods poses challenges in predicting species responses to increasing temperature. To address these data and methodological gaps, we propose 3 standardized approaches for assessing thermal impacts on fertility. We focus on adult obligate sexual terrestrial invertebrates but also provide modifications for other animal groups and life-history stages. We first outline a "gold-standard" protocol for determining TFLs, focussing on the effects of short-term heat shocks and simulating more frequent extreme heat events predicted by climate models. As this approach may be difficult to apply to some organisms, we then provide a standardized TSF protocol. Finally, we provide a framework to quantify fertility loss in response to extreme heat events in nature, given the limitations in laboratory approaches. Applying these standardized approaches across many taxa, similar to CTLs, will allow robust tests of the impact of fertility loss on species responses to increasing temperatures.

Precipitation-drainage cycles lead to hot moments in soil carbon dioxide dynamics in a Neotropical wet forest.

Soil CO2 concentrations and emissions from tropical forests are modulated seasonally by precipitation. However, subseasonal responses to meteorological events (e.g., storms, drought) are less well known. Here, we present the effects of meteorological variability on short-term (hours to months) dynamics of soil CO2 concentrations and emissions in a Neotropical wet forest. We continuously monitored soil temperature, moisture, and CO2 for a three-year period (2015-2017), encompassing normal conditions, floods, a dry El Niño period, and a hurricane. We used a coupled model (Hydrus-1D) for soil water propagation, heat transfer, and diffusive gas transport to explain observed soil moisture, soil temperature, and soil CO2 concentration responses to meteorology, and we estimated soil CO2 efflux with a gradient-flux model. Then, we predicted changes in soil CO2 concentrations and emissions under different warming climate change scenarios. Observed short-term (hourly to daily) soil CO2 concentration responded more to precipitation than to other meteorological variables (including lower pressure during the hurricane). Observed soil CO2 failed to exhibit diel patterns (associated with diel temperature fluctuations in drier climates), except during the drier El Niño period. Climate change scenarios showed enhanced soil CO2 due to warmer conditions, while precipitation played a critical role in moderating the balance between concentrations and emissions. The scenario with increased precipitation (based on a regional model projection) led to increases of +11% in soil CO2 concentrations and +4% in soil CO2 emissions. The scenario with decreased precipitation (based on global circulation model projections) resulted in increases of +4% in soil CO2 concentrations and +18% in soil CO2 emissions, and presented more prominent hot moments in soil CO2 outgassing. These findings suggest that soil CO2 will increase under warmer climate in tropical wet forests, and precipitation patterns will define the intensity of CO2 outgassing hot moments.

Diel pattern driven by free convection controls leaf-cutter ant nest ventilation and greenhouse gas emissions in a Neotropical rain forest.

Leaf-cutter ant nests are biogeochemical hot spots where ants live and import vegetation to grow fungus. Metabolic activity and (in wet tropical forests) soil gas flux to the nest may result in high nest CO2 concentrations if not adequately ventilated. Wind-driven ventilation mitigates high CO2 concentrations in grasslands, but little is known about exchange for forest species faced with prolonged windless conditions. We studied Atta cephalotes nests located under dense canopy (leaf area index > 5) in a wet tropical rainforest in Costa Rica, where wind events are infrequent. We instrumented nests with thermocouples and flow-through CO2 sensing chambers. The results showed that CO2 concentrations exiting leaf-cutter ant nests follow a diel pattern with higher values at night. We developed an efflux model based on pressure differences that evaluated the observed CO2 diel pattern in terms of ventilation by (1) free convection (warm, less dense air rises out the nest more prominently at night) and (2) episodic wind-forced convection events providing occasional supplemental ventilation during daytime. Average greenhouse gas emissions were estimated through nest vents at about 78 kg CO2eq nest-1 year-1. At the ecosystem level, leaf-cutter ant nest vents accounted for 0.2% to 1% of total rainforest soil emissions. In wet, clayey tropical soils, leaf-cutter ant nests act as free convection-driven conduits for exporting CO2 and other greenhouse gases produced within the nest (fungus and ant respiration, refuse decay), and by roots and soil microbes surrounding the nest. This allows A. cephalotes nests to be ventilated without reliable wind conditions.

Can deuterium tracing be used for reliably estimating water use of tropical trees and bamboo?

Reliable estimates of water use by trees and other woody plants are crucial for an improved understanding of plant physiology and for water resource management. Since the 1980s, the thermal dissipation probe (TDP) method has been widely applied in trees, proved to be fairly accurate but is challenging in remote areas. Also in the 1980s, the deuterium (D(2)O or deuterium oxide) tracing method was proposed, which so far has less often been applied. However, deuterium tracing requires less sophisticated equipment in the field and new analytical methods reduce costs and increase sample throughput. The objectives of this study were (i) to compare plant water use estimates of the TDP and D(2)O method and (ii) to determine whether the D(2)O method is appropriate for assessing absolute magnitudes of plant water use. The two methods were employed on five tropical tree species and a bamboo species growing in a reforestation stand in the Philippines and an agroforestry system in Indonesia. For bamboo, an increase in D(2)O values in neighbouring, non-labelled culms suggests that injected D(2)O was partly redistributed among culms, which would seriously limit the accurate estimation of water use for the target culm. For trees, water use estimates resulting from the D(2)O tracing method were proportional to the TDP results (r(2) = 0.85, P < 0.001), but absolute values were, on average, about seven times higher. This overestimation may be due to the assumptions underlying the D(2)O tracing method, such as the conservation of tracer mass, not being met. Further, it cannot be excluded that underestimation of water use by the TDP method contributed partly to the observed difference. However, when considering known sources of error, a large part of the observed difference remains unexplained. Based on our results, the use of the D(2)O tracing method cannot be recommended without further experimental testing if absolute values of whole-plant water use are a major goal. However, the D(2)O tracing method appears suitable for answering other questions, such as relative differences in water use among trees, water redistribution among neighbours and internal water transport and storage processes in plants.

Unravelling the relationship between stem temperature and air temperature to correct for errors in sap-flow calculations using stem heat balance sensors.

Results from measurement of sap flow by heat balance sensors on the stem of a young oak tree (Quercus robur L.) revealed that thermal disequilibrium (i.e. heat storage) within the heated stem segment can introduce considerable errors in the measured sap-flow rates. The magnitude, sign and significance of these errors depend on the sap-flow rate and on the relationship between stem temperature and air temperature. Sap-flow rates were found to be more prone to errors caused by heat storage effects under low flow conditions than at higher rates of sap flow. Furthermore, daytime fluctuations of air temperature and stem temperature inside the heat balance sensor were either in phase when a low, or in opposite phase when a high sap-flow rate was passing through the stem of the young tree. To investigate this relationship, we developed an experimental set-up with cut stem segments through which tap water could be pressed. This set-up allowed the effects of air temperature and sap-flow rates on stem temperatures within heat balance sensors to be clearly separated. Good mathematical relationships were obtained and were successfully used to assess the relative importance of air temperature and sap-flow rate with respect to the fluctuations in stem temperature of the young oak tree. Based on the established relationships, a novel approach was put forward to correct for errors introduced into sap-flow calculations caused by heat storage effects if no measured data on stem temperature are available.