Drivers of leafcutter ant populations and their inter‐trophic relationships in Amazonian forest islands

Ana Filipa Palmeirim,Inara R Leal,Carlos A Peres,Maíra Benchimol

doi:10.1002/ecs2.3518

Abstract

AbstractUnder habitat loss and fragmentation, the intensity of local ecological processes involving species interactions changes pervasively, accelerating local species extinctions, and disrupting essential ecosystem functions. We addressed this issue by examining the direct population drivers of apex predators (five felid species), armadillo mesopredators, leafcutter ants (Atta sexdens and Atta cephalotes), and the indirect effects mediated by their inter‐trophic relationships in a ~25‐yr‐old land‐bridge island system formed by a hydroelectric dam in the Central Amazon. These trophic groups and pioneer tree abundance were surveyed across 34 variable‐sized islands and three continuous forest sites. Leafcutter populations were characterized in relation to their occurrence, colony density, and proportion of inactive colonies, and for each leafcutter response, we considered the direct and/or indirect effects of forest area on each trophic group. Leafcutter occupancy was best explained by the direct model, colony density by either the direct or the indirect model, and proportion of inactive colonies by an indirect model via the effects of pioneer tree abundance. The direct forest area effects were positive for apex predators and leafcutter occupancy, but negative for armadillos and pioneer trees. Yet leafcutter colony density declined in increasingly larger forest areas. The absence or low abundance of apex predators on small islands released armadillo hyper‐abundance, which contrary to expectation from top‐down control, covaried positively with leafcutter colony density. Finally, the indirect model showed that leafcutter colonies were more active under higher pioneer tree abundances. That leafcutter density increases on smaller islands whenever present is likely attributed to the hyper‐abundance of pioneer plants and canopy gaps. Although apex predators apparently suppressed armadillos, the remaining fraction of the food web seems to be controlled by bottom‐up mechanisms most likely related the overall low foliage palatability typical of wet evergreen forests. Our findings can be used to inform the long‐term viability of forest ecosystems affected by hydropower development in lowland Amazonia.

Highlights

Under habitat loss and fragmentation—typically involving reduced habitat area, increased isolation, and edge effects (Fahrig 2003, Ewers and Didham 2007)—the intensity of local ecological processes concerning species interactions changes pervasively, accelerating local species extinctions, and disrupting essential ecosystem functions (Crooks and Soule 1999, Tylianakis v www.esajournals.orgMay 2021 v Volume 12(5) v Article e03518 PALMEIRIM ET AL.et al 2008)
As habitat conditions further deteriorate, all large predators may eventually be extirpated from forest remnants, triggering first-order consumers to proliferate, which may lead to the population collapse of the lowest levels of the food web (Adler and Levins 1994, Terborgh et al 2006), culminating in a top-down trophic cascade (Estes et al 2011)
We considered a tetra-trophic system comprised of the abundance of apex predators, mesopredators, leafcutter ants (Atta sexdens and Atta cephalotes: Vasconcelos 1988, Nogueira 2009), and the basal area density of adult pioneer trees, all of which were surveyed within 34 forest islands and three continuous forest sites within an archipelagic landscape

Summary

Introduction

Under habitat loss and fragmentation—typically involving reduced habitat area, increased isolation, and edge effects (Fahrig 2003, Ewers and Didham 2007)—the intensity of local ecological processes concerning species interactions changes pervasively, accelerating local species extinctions, and disrupting essential ecosystem functions (Crooks and Soule 1999, Tylianakis v www.esajournals.orgMay 2021 v Volume 12(5) v Article e03518 PALMEIRIM ET AL.et al 2008). Top-predators, due to their low population densities and large spatial requirements (Carbone and Gittleman 2002), are highly susceptible to local extinctions (Lomolino et al 1989, Woodroffe and Ginsberg 1998) In their absence, top-down forces become more relaxed (Hairston et al 1960, Estes 1996) and intermediate trophic levels, such as mesopredators, are released into higher abundances (Crooks and Soule 1999). In resource-limited environments, intraguild species interactions may be more intense, so that competition (e.g., for prey or nesting sites) negates their release from predators (Gruner 2004) In this case, the effects of resource depletion often promote a bottom-up cascade in which lower trophic levels propagate upward to nonadjacent higher levels (Hunter and Price 1992, Kagata and Ohgushi 2006). Despite the vast literature on the relative importance of bottom-up vs top-down forces (Hunter and Price 1992, Walker and Jones 2001), only a few studies have investigated these mechanisms in fragmented tropical forest ecosystems (but see Morante-Filho et al 2016, 2018, Hernandez-Ruedas et al 2018, Wang et al 2020)

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Results

Conclusion