Leaf-cutter ants engineer large nitrous oxide hot spots in tropical forests

Abstract

Though tropical forest ecosystems are among the largest natural sources of the potent greenhouse gas nitrous oxide (N 2 O), the spatial distribution of emissions across landscapes is often poorly resolved. Leaf cutter ants (LCA; Atta and Acromyrmex, Myrmicinae) are dominant herbivores throughout Central and South America, and influence multiple aspects of forest structure and function. In particular, their foraging creates spatial heterogeneity by concentrating large quantities of organic matter (including nitrogen, N) from the surrounding canopy into their colonies, and ultimately into colony refuse dumps. Here, we demonstrate that refuse piles created by LCA species Atta colombica in tropical rainforests of Costa Rica provide ideal conditions for extremely high rates of N 2 O production (high microbial biomass, potential denitrification enzyme activity, N content and anoxia) and may represent an unappreciated source of heterogeneity in tropical forest N 2 O emissions. Average instantaneous refuse pile N 2 O fluxes surpassed background emissions by more than three orders of magnitude (in some cases exceeding 80 000 µg N 2 O-N m −2 h −1 ) and generating fluxes comparable to or greater than those produced by engineered systems such as wastewater treatment tanks. Refuse-concentrating Atta species are ubiquitous in tropical forests, pastures and production ecosystems, and increase density strongly in response to disturbance. As such, LCA colonies may represent an unrecognized greenhouse gas point source throughout the Neotropics.

First field estimation of greenhouse gas release from European soil-dwelling Scarabaeidae larvae targeting the genus Melolontha

“…There are also a few studies available from other soil faunal groups, e.g. ants [ 54 ] and one laboratory-based study on Scarabaeidae larvae [ 55 ], but earthworms are the only faunal group for which a considerable amount of literature on soil N 2 O emissions is available [ 9 ]. Earthworms are not host to an endemic denitrifier community in their gut system, but in their presence N 2 O emissions can increase by more than 40% due to the activation of ingested nitrate- and nitrite-reducing soil bacteria during earthworm gut passage [ 14 ].…”

Welcome to the Atta world: A framework for understanding the effects of leaf‐cutter ants on ecosystem functions

“…High decomposition rates, coupled with increased inputs of carbon and nutrients, create hot spots of heat, CO 2 , N 2 O, volatile hydrocarbons and sulphidic gases (Soper et al, ). Break down of organic matter partly occurs under anaerobic conditions via specialized archaea and bacteria and produces CH 4 (Jílková et al, ).…”

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

“…However, after this initial increase, the damage in the canopy may lead to the opposite effect, and may open the soil to drying and to large diurnal variations in soil CO 2 respiration (Vargas & Allen, 2008a); this is a major driver of the nitrogen cycling and belowground carbon dynamics (Hasselquist, Santiago, & Allen, 2010). Regardless of mechanisms, short‐term fluctuations in soil CO 2 concentrations (and other greenhouse gases) lead to variability in soil emissions (Barcellos et al., 2018; Fernandez‐Bou, Dierick, & Harmon, 2020; Fernandez‐Bou et al, 2018; Harms & Grimm, 2008; Haverd, Ahlström, Smith, & Canadell, 2017; Kuzyakov & Blagodatskaya, 2015; Leon et al., 2014; Lubbers, Berg, Deyn, van der Putten, & van Groenigen, 2019; Soper et al., 2019; Swanson et al., 2019; Vargas et al., 2018). In this work, we monitor soil CO 2 concentration over multiple years to better understand its short‐term dynamics and potential influence on tropical soil CO 2 emissions.…”