Cacao flower visitation: Low pollen deposition, low fruit set and dominance of herbivores

Pollination services of cacao are crucial for global chocolate production, yet remain critically understudied, particularly in regions of origin of the species. Notably, uncertainties remain concerning the identity of cacao pollinators, the influence of landscape (forest distance) and management (shade cover) on flower visitation and the role of pollen deposition in limiting fruit set. Here, we aimed to improve understanding of cacao pollination by studying limiting factors of fruit set in Peru, part of the centre of origin of cacao. Flower visitors were sampled with sticky insect glue in 20 cacao agroforests in two biogeographically distinct regions of Peru, across gradients of shade cover and forest distance. Further, we assessed pollen quantities and compared fruit set between naturally and manually pollinated flowers. The most abundant flower visitors were aphids, ants and thrips in the north and thrips, midges and parasitoid wasps in the south of Peru. We present some evidence of increasing visitation rates from medium to high shade (40%–95% canopy closure) in the dry north, and opposite patterns in the semi-humid south, during the wet season. Natural pollination resulted in remarkably low fruit set rates (2%), and very low pollen deposition. After hand pollination, fruit set more than tripled (7%), but was still low. The diversity and high relative abundances of herbivore flower visitors limit our ability to draw conclusions on the functional role of different flower visitors. The remarkably low fruit set of naturally and even hand pollinated flowers indicates that other unaddressed factors limit cacao fruit production. Such factors could be, amongst others, a lack of effective pollinators, genetic incompatibility or resource limitation. Revealing efficient pollinator species and other causes of low fruit set rates is therefore key to establish location-specific management strategies and develop high yielding native cacao agroforestry systems in regions of origin of cacao. © 2022 The Authors. Ecological Solutions and Evidence published by John Wiley & Sons Ltd on behalf of British Ecological Society

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

Birds and bats enhance cacao yield despite suppressing arthropod mesopredation

Bird- and bat-mediated biocontrol benefits the productivity of tropicalcommodity crops such as cacao, but the ecological interactions drivingthese ecosystem services remain poorly understood. Whereas birds and batsprey on herbivorous arthropods, they may also prey on arthropodmesopredators such as ants, with poorly understood consequences for pestbiocontrol. We used a full-factorial experiment excluding birds, bats, andants to assess their effects on (a) the abundanceof multiple arthropodgroups; (b) predation pressure on arthropods evaluated through artificialsentinel caterpillars; and (c) cacao yield over 1 year in shaded agroforestrysystems of native cacao varieties in Peru. Birds and bats increasedcacao yield by 118%, which translates in smallholder benefits of ca.US $959 ha−1year−1. Birds and bats decreased predation by ants and otherarthropods, but contributed to thecontrol of phytophagous taxa such asaphids and mealybugs. By contrast, ant presence increased the abundanceof these sap-sucking insects, with negative impacts for cacao yield.Notably, high abundances of the dominant antNylanderiasp., known toattend sap-sucking insects, were associated with lower cacao yield along adistance gradient from the closest forest edge. According to these results,arthropod predation by birds and bats, rather than mesopredation byarthropods, was most responsible forincreases in cacao yield. Moving for-ward, detailed research about their trophic interactions will be necessary toidentify the cause of such benefits. Retaining and restoring the large bene-fits of birds and bats as well as minimizing disservices by other taxa incacao agroforests can benefit from management schemes that prioritizepreservation of shade trees and adjacent forests within agroforestrylandscapes

Global South leadership towards inclusive tropical ecology and conservation

Strengthening participation of Global South researchers in tropical ecology and conservation is a target of our scientific community, but strategies for fostering increased engagement are mostly directed at Global North institutions and researchers. Whereas such approaches are crucial, there are unique challenges to addressing diversity, equity and inclusion (DEI) within the Global South given its socio-economic, cultural and scientific contexts. Sustainable solutions protecting biodiversity in the tropics depend on the leadership of Global South communities, and therefore DEI improvements in the Global South are paramount in our field. Here, we propose ten key actions towards equitable international collaborations in tropical ecology, which, led by Global South researchers, may improve DEI at institutional, national and international levels. At an institutional level, we recommend (1) becoming role models for DEI, (2) co-developing research with local stakeholders, and (3) promoting transparent funding management favouring local scientists. At a national level, we encourage (4) engagement in political actions protecting scientists and their research in tropical countries, (5) participation in improving biodiversity research policies, and (6) devising research that reaches society. At an international level, we encourage Global South researchers in international collaborations to (7) lead and direct funding applications, (8) ensure equitable workloads, and (9) procure equal benefits among national and foreign collaborators. Finally, (10) we propose that Global South leadership in DEI efforts has the most potential for worldwide improvements, supporting positive long-lasting changes in our entire scientific community. Supplementary materials provide this abstract in 18 other languages spoken in the Global South

Bird and bat predation services in tropical forests and agroforestry landscapes

Understanding distribution patterns and multitrophic interactions is critical for managing batâ and birdâ mediated ecosystem services such as the suppression of pest and nonâ pest arthropods. Despite the ecological and economic importance of bats and birds in tropical forests, agroforestry systems, and agricultural systems mixed with natural forest, a systematic review of their impact is still missing. A growing number of bird and bat exclosure experiments has improved our knowledge allowing new conclusions regarding their roles in food webs and associated ecosystem services. Here, we review the distribution patterns of insectivorous birds and bats, their local and landscape drivers, and their effects on trophic cascades in tropical ecosystems. We report that for birds but not bats community composition and relative importance of functional groups changes conspicuously from forests to habitats including both agricultural areas and forests, here termed â forestâ agriâ habitats, with reduced representation of insectivores in the latter. In contrast to previous theory regarding trophic cascade strength, we find that birds and bats reduce the density and biomass of arthropods in the tropics with effect sizes similar to those in temperate and boreal communities. The relative importance of birds versus bats in regulating pest abundances varies with season, geography and management. Birds and bats may even suppress tropical arthropod outbreaks, although positive effects on plant growth are not always reported. As both bats and birds are major agents of pest suppression, a better understanding of the local and landscape factors driving the variability of their impact is needed.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/134094/1/brv12211_am.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/134094/2/brv12211.pd

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

Animals provide services such as pollination and pest control in cacao agro- forestry systems, but also disservices. Yet, their combined contributions to crop yield and fruit loss are mostly unclear. In a full-factorial field exper- iment in northwestern Peru, we excluded flying insects, ants, birds and bats from cacao trees and assessed several productivity indicators. We quan- tified the contribution of each group to fruit set, fruit loss and marketable yield and evaluated how forest distance and canopy closure affected pro- ductivity. 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 squir- rels, 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 managemen

Bats in the anthropogenic matrix: Challenges and opportunities for the conservation of chiroptera and their ecosystem services in agricultural landscapes

Intensification in land-use and farming practices has had largely negative effects on bats, leading to population declines and concomitant losses of ecosystem services. Current trends in land-use change suggest that agricultural areas will further expand, while production systems may either experience further intensification (particularly in developing nations) or become more environmentally friendly (especially in Europe). In this chapter, we review the existing literature on how agricultural management affects the bat assemblages and the behavior of individual bat species, as well as the literature on provision of ecosystem services by bats (pest insect suppression and pollination) in agricultural systems. Bats show highly variable responses to habitat conversion, with no significant change in species richness or measures of activity or abundance. In contrast, intensification within agricultural systems (i.e., increased agrochemical inputs, reduction of natural structuring elements such as hedges, woods, and marshes) had more consistently negative effects on abundance and species richness. Agroforestry systems appear to mitigate negative consequences of habitat conversion and intensification, often having higher abundances and activity levels than natural areas. Across biomes, bats play key roles in limiting populations of arthropods by consuming various agricultural pests. In tropical areas, bats are key pollinators of several commercial fruit species. However, these substantial benefits may go unrecognized by farmers, who sometimes associate bats with ecosystem disservices such as crop raiding. Given the importance of bats for global food production, future agricultural management should focus on “wildlife-friendly” farming practices that allow more bats to exploit and persist in the anthropogenic matrix so as to enhance provision of ecosystem services. Pressing research topics include (1) a better understanding of how local-level versus landscape-level management practices interact to structure bat assemblages, (2) the effects of new pesticide classes and GM crops on bat populations, and (3) how increased documentation and valuation of the ecosystem services provided by bats could improve attitudes of producers toward their conservation

Crop pests and predators exhibit inconsistent responses to surrounding landscape composition

The idea that noncrop habitat enhances pest control and represents a win–win opportunity to conserve biodiversity and bolster yields has emerged as an agroecological paradigm. However, while noncrop habitat in landscapes surrounding farms sometimes benefits pest predators, natural enemy responses remain heterogeneous across studies and effects on pests are inconclusive. The observed heterogeneity in species responses to noncrop habitat may be biological in origin or could result from variation in how habitat and biocontrol are measured. Here, we use a pest-control database encompassing 132 studies and 6,759 sites worldwide to model natural enemy and pest abundances, predation rates, and crop damage as a function of landscape composition. Our results showed that although landscape composition explained significant variation within studies, pest and enemy abundances, predation rates, crop damage, and yields each exhibited different responses across studies, sometimes increasing and sometimes decreasing in landscapes with more noncrop habitat but overall showing no consistent trend. Thus, models that used landscape-composition variables to predict pest-control dynamics demonstrated little potential to explain variation across studies, though prediction did improve when comparing studies with similar crop and landscape features. Overall, our work shows that surrounding noncrop habitat does not consistently improve pest management, meaning habitat conservation may bolster production in some systems and depress yields in others. Future efforts to develop tools that inform farmers when habitat conservation truly represents a win–win would benefit from increased understanding of how landscape effects are modulated by local farm management and the biology of pests and their enemies