High intermediary mutualist density provides consistent biological control in a tripartite mutualism

Abstract

Understanding the ecology of mutualisms becomes a particularly important task when considering agroecosystems, as many ecosystem services are associated with mutualistic interactions. Here we report on experiments associated with an indirect pest control mutualism between the arboreal nesting ant Azteca sericeasur and coffee. This system is particularly interesting because the indirect Azteca-Coffea mutualism emerges from an Aztecascale insect mutualism that takes place on the coffee plant. We describe this interaction structure as a mutualismdependent mutualism and ask whether the density of intermediary mutualist (scale insects, Coccus) that benefits Azteca also influences the benefits provided to coffee plants. We found that indeed Azteca's benefit to Coffea is consistent when Coccus density is high. Furthermore, we also found that at low Coccus density Azteca only benefits Coffea in the beginning of the rainy season, and this effect is likely due to the fact that Coccus produces less sugars with higher precipitation. We suggest a framework for thinking about context-dependency in agroecosystem mutualisms that may provide a more mechanistic way to tease apart the prevalent contextdependent results in ecological literature. Finally, we address some past recommendations as it pertains to the management of the Azteca-Coffea-Coccus complex in coffee agroecosystems.

Vegetation connectivity increases ant activity and potential for ant‐provided biocontrol services in a tropical agroforest

“…However, the green coffee scale is not a major pest in the region of study, in contrast to the economically significant coffee berry borer (Morris et al., ). Furthermore, a recent study evaluating the benefits associated with the indirect Azteca ‐ Coffea mutualism found that the protective benefit ants provide to coffee plants is positively associated with high densities of the scale (Rivera‐Salinas, Hajian‐Forooshani, Jiménez‐Soto, Cruz‐Rodríguez, & Philpott, ). This suggests that the enhanced CBB control by ants outweighs the costs associated with scale damage.…”

Evaluating community effects of a Keystone Ant,Azteca sericeasur,onInga michelianaleaf litter decomposition in a shaded coffee agro‐ecosystem

“…Past research has suggested that A. sericeasur are not sugar limited at the start of the rainy season, as they have not shown a preference for high density C. viridis patches (Rivera- Salinas et al, 2018).…”

“…and C. viridis ) may alter the food sources available to A. sericeasur, but the dietary needs of A. sericeasur also change between seasons. Past research has suggested that A. sericeasur are not sugar limited at the start of the rainy season, as they have not shown a preference for high density C. viridis patches (Rivera‐Salinas et al., 2018). However, despite the complications that distinct seasonality presents, the timing of our sampling is consistent with past work on A. sericeasur where they have been found to exclude other ant species (Ennis, 2010, Rivera‐Salinas, 2019).…”

“…helmet scale (Livingston et al., 2008), both of which provide alternative sources of sugar for A. sericeasur . Moreover, during the rainy season, when the study was conducted, C. viridis has reduced sugar content (Rivera‐Salinas, Hajian‐Forooshani, Jiménez‐Soto, Cruz‐Rodríguez, & Philpott, 2018), while extrafloral nectaries are more productive (Rico‐Gray, García‐Franco, Palacios‐Rios, Íz‐Castelazo, Parra‐Tabla, & Navarro, 1998). Further, C. viridis occurs in lower densities around I. micheliana with Octolecanium, suggesting competition between the scale species and a preference of A. sericeasur for Octolecaium (Livingston et al., 2008).…”

An aggressive nonconsumptive effect mediates pest control and multipredator interactions in a coffee agroecosystem

“…Variability in the intensity of this interaction or in the proportion of nonconsumptive to consumptive interactions by ants may have important impacts on the dynamics and efficacy of pest control in this system. Interestingly, because this nonconsumptive interaction is driven by enemy aggression, rather than prey defense, these dynamics may be governed by the availability of honeydew resources for ants from scale insects on coffee, which previous research suggests may influence Azteca 's reduction of CBB damage (Rivera‐Salinas et al, 2018 ). Although it is not always clear how honeydew availability (Clark & Singer, 2018 ) or hemipteran insect density (Kaplan & Eubanks, 2005 ) influences ant–plant defensive interactions more generally, research on other species of Azteca ants in this region has demonstrated that seasonal variability in plant carbon pools may impact scale insect honeydew and the strength of ant–plant defense (Pringle et al, 2013 ).…”