Leaf-Cutter Ant Engineered Nest Soil CO2 Dynamics in a Neotropical Rainforest

Leaf-cutter ants are one of the most conspicuous inhabitants of New World forests and plantations. They amaze visitors and worry farmers when thousands of them march in endless parades carrying leaf fragments to their massive underground nests, or when they go back in the opposite direction to collect more. However, rather than eating the hundreds of kilograms of vegetation they harvest each year, they shred them to create a substrate to feed a fungus that has been their fundamental diet for 50 Ma. They are indeed the first farmers on Earth’s natural history and, as any farmer, they have learned to optimize the conditions required by their gardens by engineering their surroundings. Here we present a series of studies designed to shed light on the effects of leaf-cutter ants on soil CO2 dynamics in Neotropical soils, an important part of the rainforest carbon cycle. We studied soil CO2 concentrations at different depths in several nonnest, nest, and abandoned nest soils for three years to understand the seasonal effects of the nest structure in soil CO2. In two selected locations, we monitored soil CO2 concentrations at high frequency (every 30 minutes) along with soil moisture and soil temperature to understand the effect of weather in the short-term, and how the nest presence impacts their dynamics. In addition, we measured soil surface CO2 efflux with closed chambers, and nest vent efflux with our own novel flow-through chambers, which we describe for the first time, that we equipped with thermocouples to monitor temperature gradients. We present statistical and conceptual models to account for differences in soil CO2 and to understand the fluid dynamics of CO2 in nests. Nest soils exhibited lower CO2 accumulation than nonnest soils for the same precipitation amounts. During wet periods, soil CO2 concentrations increased across all depths, but were significantly less in nest than in nonnest soils. Differences were nonsignificant during drier periods. In the short-term, precipitation events impacted soil CO2 concentration more than any other variable, and dramatically increased tortuosity, which leaded to the observed seasonal increases of soil CO2 concentration during wet periods. Surface efflux was equal across nest and nonnest plots (5 μmol CO2 m-2 s-1), suggesting that nest soils do not have enhanced surface emissions. However, vent efflux was substantially (103 to 105 times) greater and followed a diel pattern driven by free convection (warm and moist, less dense air rises out the nest more markedly at night). Episodic wind-forced convection events also provide supplemental ventilation during the day. Nest tunnel CO2 concentrations were less than in soil, suggesting CO2 efflux from the soil matrix into the nest. This is supported by the short-term diel pattern showed in nest soil CO2 concentration that did not occur in nonnest soils, except for a very dry period (El Niño, 2016). Thanks to the nest structure, the nest air is better ventilated than the soil, and CO2 produced in the soil matrix finds a faster way out of the soil through the nest tunnels. The diel pattern in nest vent CO2 efflux seems to regulate the diffusion of CO2 from the soil matrix by affecting the CO2 concentration gradient. These findings indicate that leaf-cutter ant nests provide alternative transport pathways to soil CO2 that increase total emissions and decrease soil CO2 concentrations, and have a lasting impact. We estimate average greenhouse gas emissions of about 78 kg CO2eq nest-1 yr 1. At the ecosystem level, leaf-cutter ant nests can account for 0.2% to 1% of the total forest soil emissions. However, balancing vegetation inputs and emissions, and considering their carbon cycle, these ant nests are a net carbon store in the soil that can persist for a decade or more