Birds and bats enhance cacao yield despite suppressing arthropod mesopredation.

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.

Socio-ecological benefits of fine-flavor cacao in its center of origin.

In the tropics, combining food security with biodiversity conservation remains a major challenge. Tropical agroforestry systems are among the most biodiversity-friendly and productive land-use systems, and 70% of cocoa is grown by >6 million smallholder farmers living on <2$ per day. In cacao's main centre of diversification, the western Amazon region, interest is growing to achieve premium prices with the conversion of high-yielding, but mostly bulk-quality cacao to native fine-flavor cacao varieties, culturally important since pre-Columbian times. Conversion to native cacao can be expected to favor adaptation to regional climate and growth conditions, and to enhance native biodiversity and ecosystem services such as biological pest control and pollination, but possibly also imply susceptibility to diseases. Experience from successful conversion of non-native cacao plantations to fine-flavor cacao agroforestry with rejuvenation by grafting and under medium-canopy cover levels (30%-40%) can ensure a smooth transition with only minor temporary productivity gaps. This includes ongoing selection programs of high yielding and disease resistant native fine-flavor cacao genotypes and organizing in cooperatives to buffer the high market volatility. In conclusion, the recent interest on converting bulk cacao to a diversity of native fine-flavor varieties in countries like Peru is a challenge, but offers promising socio-ecological perspectives.

Quantifying services and disservices provided by insects and vertebrates in cacao agroforestry landscapes.

Animals provide services such as pollination and pest control in cacao agroforestry systems, but also disservices. Yet, their combined contributions to crop yield and fruit loss are mostly unclear. In a full-factorial field experiment in northwestern Peru, we excluded flying insects, ants, birds and bats from cacao trees and assessed several productivity indicators. We quantified the contribution of each group to fruit set, fruit loss and marketable yield and evaluated how forest distance and canopy closure affected productivity. Fruit set dropped (from 1.7% to 0.3%) when flying insects were excluded and tripled at intermediate (40%) compared to high (greater than 80%) canopy cover in the non-exclusion treatment. Fruit set also dropped with bird and bat exclusion, potentially due to increased abundances of arthropods preying on pollinators or flower herbivores. Overall, cacao yields more than doubled when birds and bats had access to trees. Ants were generally associated with fruit loss, but also with yield increases in agroforests close to forest. We also evidenced disservices generated by squirrels, leading to significant fruit losses. Our findings show that several functional groups contribute to high cacao yield, while trade-offs between services and disservices need to be integrated in local and landscape-scale sustainable cacao agroforestry management.

Transforming Tropical Agroforestry towards High Socio-Ecological Standards.

Growing demand for tropical commodities that are socially and environmentally more sustainable is changing the global market for agroforestry products such as coffee and cocoa. Transforming mass production of cash crops towards higher socio-ecological standards includes challenges, but also novel opportunities to protect ecosystem services and human health and well-being alike.