Birds and bats enhance cacao yield despite suppressing arthropod mesopredation

Abstract

Bird-and bat-mediated biocontrol benefits the productivity of tropical commodity crops such as cacao, but the ecological interactions driving these ecosystem services remain poorly understood. Whereas birds and bats prey on herbivorous arthropods, they may also prey on arthropod mesopredators such as ants, with poorly understood consequences for pest biocontrol. We used a full-factorial experiment excluding birds, bats, and ants to assess their effects on (a) the abundance of multiple arthropod groups; (b) predation pressure on arthropods evaluated through artificial sentinel caterpillars; and (c) cacao yield over 1 year in shaded agroforestry systems of native cacao varieties in Peru. Birds and bats increased cacao yield by 118%, which translates in smallholder benefits of ca.US $959 ha −1 year −1 . Birds and bats decreased predation by ants and other arthropods, but contributed to the control of phytophagous taxa such as aphids and mealybugs. By contrast, ant presence increased the abundance of these sap-sucking insects, with negative impacts for cacao yield.Notably, high abundances of the dominant ant Nylanderia sp., known to attend sap-sucking insects, were associated with lower cacao yield along a distance gradient from the closest forest edge. According to these results, arthropod predation by birds and bats, rather than mesopredation by arthropods, was most responsible for increases in cacao yield. Moving forward, detailed research about their trophic interactions will be necessary to identify the cause of such benefits. Retaining and restoring the large benefits of birds and bats as well as minimizing disservices by other taxa in cacao agroforests can benefit from management schemes that prioritize preservation of shade trees and adjacent forests within agroforestry landscapes.

Insectivorous birds and bats outperform ants in the top-down regulation of arthropods across strata of a Japanese temperate forest

“…This was unexpected, as we did not anticipate birds to feed abundantly on sapsuckers. Their small size and sessility likely make them inconspicuous to vertebrate insectivores which is consistent with recent findings in tropical areas (Ferreira et al, 2023; Ocampo-Ariza et al, 2023). It, therefore, seems likely that the increase in their densities observed here is due to an indirect interaction with vertebrate insectivores, since some insectivorous birds (e.g., Parus minor, Sitta europaea ) found abundantly in Tomakomai forest consume other taxa, such as mesopredators (ants, wasps or spiders), and mutualists (ants) (Eguchi, 1980; Wesołowski et al, 2019), that positively affect the sapsuckers by relieving predation pressure.…”

“…Unfortunately, research on trophic cascades has so far predominantly focused on easily accessible forest understories (Denmead et al, 2017;Ocampo-Ariza et al, 2023), limiting our understanding of their full extent (e.g., forest canopy).…”

“…Given the complexity of food webs, the degree of top-down control is context-dependent, leading to variations even within a single forest and among different forest strata. Unfortunately, research on trophic cascades has so far predominantly focused on easily accessible forest understories (Denmead et al, 2017; Ocampo-Ariza et al, 2023), limiting our understanding of their full extent (e.g., forest canopy).…”

“…The ambiguity persists because only a limited number of studies have aimed to exclude ants whilst also considering vertebrate predators. Additionally, these studies often focus either on the forest understory (Denmead et al, 2017; Ocampo-Ariza et al, 2023) or the canopy (Singer et al, 2017). Findings have been mixed, with studies showing both negative (Denmead et al, 2017; Singer et al, 2017) and positive (Ocampo-Ariza et al, 2023) effects of ants on the abundance of mesopredators and herbivorous arthropods.…”

“…This uncertainty emerges because predators can also function as intraguild predators, consuming predatory arthropods. This can have a negative effect on plants, and consequently, when predators simultaneously consume predatory arthropods and herbivores, their net effect on plants could be dependent on the balance between these two factors (Gras et al, 2016; Ocampo-Ariza et al, 2023). While the theory on trophic interactions predicts that the effect of vertebrate exclusion might be moderately counterbalanced by the release of spiders, carabid beetles and other predatory arthropods (Hölldobler & Wilson, 1990), the existence of such release in the absence of ants appears to be minimal, at least in tropical habitats (Gras et al, 2016).…”