Economic trade-offs between carbon sequestration,timber production,and crop pollination in tropical forested landscapes

The Millennium Ecosystem Assessment distinguishes between supporting, regulating, provisioning, and cultural ecosystem services. We focus on three services, namely the provision of timber, the regulation of atmospheric carbon dioxide, and the supporting service of bee pollination for coffee production. Possible trade-offs between the different ecosystem services might result in a reduced attractiveness of afforestation projects when taking pollination services into account. We found that economic losses due to a limited reduction of tree density of a Cordia alliodora plantation can be overcompensated by generating pollination services to adjacent coffee agroforestry systems. Thus, for moderate silvicultural interventions such trade-offs do not necessarily occur. Including additional ecosystem services such as biological pest control or seed dispersal, which are also associated with the enhanced functional biodiversity in less dense tree plantations, might further emphasize the hump-shaped relationship between tree density and forest revenues.     

Interaction complexity matters: disentangling services and disservices of ant communities driving yield in tropical agroecosystems

Owing to complex direct and indirect effects, impacts of higher trophic levels on plants is poorly understood. In tropical agroecosystems, ants interact with crop mutualists and antagonists, but little is known about how this integrates into the final ecosystem service, crop yield. We combined ant exclusion and introduction of invasive and native-dominant species in cacao agroecosystems to test whether (i) ant exclusion reduces yield, (ii) dominant species maximize certain intermediate ecosystem services (e.g. control of specific pests) rather than yield, which depends on several, cascading intermediate services and (iii) even, species-rich ant communities result in highest yields. Ants provided services, including reduced leaf herbivory and fruit pest damage and indirect pollination facilitation, but also disservices, such as increased mealybug density, phytopathogen dissemination and indirect pest damage enhancement. Yields were highest with unmanipulated, species-rich, even communities, whereas ant exclusion decreased yield by 27%. Introduction of an invasive-dominant ant decreased species density and evenness and resulted in 34% lower yields, whereas introduction of a non-invasive-dominant species resulted in similar species density and yields as in the unmanipulated control. Species traits and ant community structure affect services and disservices for agriculture in surprisingly complex ways, with species-rich and even communities promoting highest yield.     

Status of pollinators and their efficiency in coffee fruit set in a fragmented landscape mosaic in South India

The region of Kodagu, South India, comprises a fragmented landscape with a high density of remnant forest patches dispersed within a mosaic dominated by shaded coffee agro-forests. We evaluated the role of self, wind and insect pollination to Coffea canephora production in this landscape. The giant Asian honeybee, Apis dorsata, which nests in remnant forests, was the main pollinator of coffee (accounting for 58% of the floral visitors). The proportion of flowers that developed into fruits was highest when hand cross-pollinated (44%), followed by open- (insect and wind combined; 33%) and wind- (22.1%) pollination treatments. Pollination by bees therefore increases fruit production by 50% over that achieved by wind. Self-pollination (1.7%) and no pollination (1%) treatments produced very low fruit set, emphasizing the importance of cross-pollination in C. canephora. Unlike measures of pollination success, initial fruit set (five weeks after flowering) proved an unreliable proxy for final fruit set. Size of adjoining forest fragments (mostly 0.3–20 ha, with a few exceeding 200 ha) positively influenced pollinator visitation to coffee flowers, but distance to such fragments had no influence on pollination. This study demonstrates the importance of cross-pollination for crop production in C. canephora, the important contribution that pollinating insects make to coffee production, and the benefits of relatively large forest fragments within the landscape mosaic to support insect pollinators of coffee. A comparison of pollinator composition to that of 100 years ago indicated that coffee pollination services remained intact despite changes in pollinator community composition.     

Utilisation of plant functional diversity in wildflower strips for the delivery of multiple agroecosystem services

Increased plant diversity in cropping systems can play an important role in agriculture by enhancing arthropod‐mediated ecosystem services, including biological control and pollination. However, there is limited research investigating the concurrent influence of plant functional diversity within cultivated systems on different arthropod functional groups, the provision of multiple ecosystem services, and crop yield. During a field experiment, repeated over 2 years, we measured the effect of increasing plant functional diversity on community structure of arthropod visitors, the abundance of multiple pests and induced crop damage, and fruit production in two varieties of tomato. Plant resources (floral and extra‐floral nectar and pollen) were included within experimental plots in four levels, with each level increasing the plant functional group richness, based on floral morphology and availability of resources, in a replacement series. The presence of sown flower mixtures in experimental plots was associated with increased abundance and diversity of natural enemy functional groups and an enhanced abundance of bees (Hymenoptera: Apiformes). However, we only detected relatively small variability in arthropod visitors among types of mixtures, and increased abundance of natural enemies did not translate into stronger pest suppression or reduced crop damage. Lepidoptera pest damage was significantly higher in plots adjacent to wildflower strips, an ecosystem disservice, but a significantly higher crop productivity was recorded from these plots. Our results provide evidence that inclusion of non‐crop plant resources in agroecosystems can improve the conservation of beneficial arthropods and may lead to increased crop productivity.     

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

In natural and managed systems, connections between trees are important structural resources for arboreal ant communities with ecosystem‐level effects. However, ongoing agricultural intensification in agroforestry systems, which reduces shade trees and connectivity between trees and crop plants, may hinder ant recruitment rates to resources and pest control services provided by ants. We examined whether increasing connectivity between coffee plants and shade trees in coffee plantations increases ant activity and enhances biological control of the coffee berry borer, the most devastating insect pest of coffee. Further, we examined whether artificial connections buffer against the loss of vegetation connectivity in coffee plants located at larger distances from the nesting tree. We used string to connect Inga micheliana shade trees containing Azteca sericeasur ant nests to coffee plants to compare ant activity before and after placement of the strings, and measured borer removal by ants on coffee plants with and without strings. Ant activity significantly increased after the addition of strings on connected plants, but not on control plants. Borer removal by ants was also three times higher on connected plants after string placement. Greater distance from the nesting tree negatively influenced ant activity on control coffee plants, but not on connected plants, suggesting that connections between coffee plants and nest trees could potentially compensate for the negative effects that larger distances pose on ant activity. Our study shows that favoring connectivity at the local scale, by artificially adding connections, promotes ant activity and may increase pest removal in agroecosystems. Abstract in Spanish is available with online material.     

Augmenting flower trait diversity in wildflower strips to optimise the conservation of arthropod functional groups for multiple agroecosystem services

Sown wildflower strips are increasingly being established in Europe for enhancing arthropod conservation and the provision of ecosystem services, including biotic pollination and natural pest control. Here we use floral traits to identify different plant functional effect groups. Floral resources were provided in four experimental levels characterised by a cumulatively increasing flower trait diversity and vegetation stand complexity. The first level consisted of a bare control strip, whilst in each subsequent level three wildflower species with different functional traits were added (Level 0: control; Level 1: three Apiaceae species; Level 2: three Apiaceae and three Fabaceae species; Level 3: three Apiaceae, three Fabaceae species, and Centaurea jacea (Asteraceae), Fagopyrum esculentum (Polygonaceae), Sinapis alba (Brassicaceae)). Plots with sown wildflower strip mixtures were located adjacent to experimental plots of organically-managed tomato crop, which is attacked by multiple pests and partially relies on bees for fruit production, and hence dependent on the provision of pollination and pest control services. Results obtained here show that the inclusion of functionally diverse wildflower species was associated with an augmented availability of floral resources across time, and this increased the abundance of bees and anthocorids throughout the crop season. Several natural enemy groups, such as parasitoids, coccinelids and ground-dwelling predators, were not significantly enhanced by the inclusion of additional flower traits within the strips but the presence of flower resources was important to enhance their conservation in an arable cropping system.     

Pollinator supplementation mitigates pollination deficits in smallholder avocado (Persea americana Mill.) production systems in Kenya

Avocado (Persea americana Mill.) is a major horticultural crop that relies on insect mediated pollination. In avocado production, a knowledge gap exists as to the importance of insect pollination, especially in East African smallholder farms. In this study, conducted in a leading smallholder avocado production region in Kenya, we assessed the dependence of avocado fruit set on insect pollination and whether current smallholder production systems suffer from a deficit in pollination services. Furthermore, we assessed if supplementation with colonies of the Western honey bee (Apis mellifera L.) to farms mitigated potential pollination deficits. Our results revealed a very high reliance of avocado on insect pollinators, with a significantly lower fruit set observed for self- and wind-pollinated (17.4%) or self-pollinated flowers (6.4%) in comparison with insect-pollinated flowers (89.5%). We found a significant pollination deficit across farms, with hand-pollinated flowers on average producing 20.7% more fruits than non-treated open flowers prior to fruit abortion. This pollination deficit could be compensated by the supplementation of farms with A. mellifera colonies. Our findings suggest that pollination is limiting fruit set in avocado and that A. Mellifera supplementation on farms is a potential option to increase fruit yield.     

The effectiveness of flower strips and hedgerows on pest control,pollination services and crop yield: a quantitative synthesis

Floral plantings are promoted to foster ecological intensification of agriculture through provisioning of ecosystem services. However, a comprehensive assessment of the effectiveness of different floral plantings, their characteristics and consequences for crop yield is lacking. Here we quantified the impacts of flower strips and hedgerows on pest control (18 studies) and pollination services (17 studies) in adjacent crops in North America, Europe and New Zealand. Flower strips, but not hedgerows, enhanced pest control services in adjacent fields by 16% on average. However, effects on crop pollination and yield were more variable. Our synthesis identifies several important drivers of variability in effectiveness of plantings: pollination services declined exponentially with distance from plantings, and perennial and older flower strips with higher flowering plant diversity enhanced pollination more effectively. These findings provide promising pathways to optimise floral plantings to more effectively contribute to ecosystem service delivery and ecological intensification of agriculture in the future.     

Pollinator‐mediated interactions between cultivated papaya and co‐flowering plant species

Many modern crop varieties rely on animal pollination to set fruit and seeds. Intensive crop plantations usually do not provide suitable habitats for pollinators so crop yield may depend on the surrounding vegetation to maintain pollination services. However, little is known about the effect of pollinator‐mediated interactions among co‐flowering plants on crop yield or the underlying mechanisms. Plant reproductive success is complex, involving several pre‐ and post‐pollination events; however, the current literature has mainly focused on pre‐pollination events in natural plant communities. We assessed pollinator sharing and the contribution to pollinator diet in a community of wild and cultivated plants that co‐flower with a focal papaya plantation. In addition, we assessed heterospecific pollen transfer to the stigmatic loads of papaya and its effect on fruit and seed production. We found that papaya shared at least one pollinator species with the majority of the co‐flowering plants. Despite this, heterospecific pollen transfer in cultivated papaya was low in open‐pollinated flowers. Hand‐pollination experiments suggest that heterospecific pollen transfer has no negative effect on fruit production or weight, but does reduce seed production. These results suggest that co‐flowering plants offer valuable floral resources to pollinators that are shared with cultivated papaya with little or no cost in terms of heterospecific pollen transfer. Although HP reduced seed production, a reduced number of seeds per se are not negative, given that from an agronomic perspective the number of seeds does not affect the monetary value of the papaya fruit.     

Forest bolsters bird abundance,pest control and coffee yield

Efforts to maximise crop yields are fuelling agricultural intensification, exacerbating the biodiversity crisis. Low‐intensity agricultural practices, however, may not sacrifice yields if they support biodiversity‐driven ecosystem services. We quantified the value native predators provide to farmers by consuming coffee's most damaging insect pest, the coffee berry borer beetle (Hypothenemus hampei). Our experiments in Costa Rica showed birds reduced infestation by ~ 50%, bats played a marginal role, and farmland forest cover increased pest removal. We identified borer‐consuming bird species by assaying faeces for borer DNA and found higher borer‐predator abundances on more forested plantations. Our coarse estimate is that forest patches doubled pest control over 230 km² by providing habitat for ~ 55 000 borer‐consuming birds. These pest‐control services prevented US$75–US$310 ha‐year⁻¹ in damage, a benefit per plantation on par with the average annual income of a Costa Rican citizen. Retaining forest and accounting for pest control demonstrates a win–win for biodiversity and coffee farmers.     

Fruit set of highland coffee increases with the diversity of pollinating bees

The worldwide decline of pollinators may negatively affect the fruit set of wild and cultivated plants. Here, we show that fruit set of the self-fertilizing highland coffee (Coffea arabica) is highly variable and related to bee pollination. In a comparison of 24 agroforestry systems in Indonesia, the fruit set of coffee could be predicted by the number of flower-visiting bee species, and it ranged from ca. 60% (three species) to 90% (20 species). Diversity, not abundance, explained variation in fruit set, so the collective role of a species-rich bee community was important for pollination success. Additional experiments showed that single flower visits from rare solitary species led to higher fruit set than with abundant social species. Pollinator diversity was affected by two habitat parameters indicating guild-specific nesting requirements: the diversity of social bees decreased with forest distance, whereas the diversity of solitary bees increased with light intensity of the agroforestry systems. These results give empirical evidence for a positive relationship between ecosystem functions such as pollination and biodiversity. Conservation of rainforest adjacent to adequately managed agroforestry systems could improve the yields of farmers.     

High effectiveness of tailored flower strips in reducing pests and crop plant damage

Providing key resources to animals may enhance both their biodiversity and the ecosystem services they provide. We examined the performance of annual flower strips targeted at the promotion of natural pest control in winter wheat. Flower strips were experimentally sown along 10 winter wheat fields across a gradient of landscape complexity (i.e. proportion non-crop area within 750 m around focal fields) and compared with 15 fields with wheat control strips. We found strong reductions in cereal leaf beetle (CLB) density (larvae: 40%; adults of the second generation: 53%) and plant damage caused by CLB (61%) in fields with flower strips compared with control fields. Natural enemies of CLB were strongly increased in flower strips and in part also in adjacent wheat fields. Flower strip effects on natural enemies, pests and crop damage were largely independent of landscape complexity (8–75% non-crop area). Our study demonstrates a high effectiveness of annual flower strips in promoting pest control, reducing CLB pest levels below the economic threshold. Hence, the studied flower strip offers a viable alternative to insecticides. This highlights the high potential of tailored agri-environment schemes to contribute to ecological intensification and may encourage more farmers to adopt such schemes.     

Bats are Not Birds – Different Responses to Human Land‐use on a Tropical Mountain

Land‐use intensification has consequences for biodiversity and ecosystem functioning, with various taxonomic groups differing widely in their sensitivity. As land‐use intensification alters habitat structure and resource availability, both factors may contribute to explaining differences in animal species diversity. Within the local animal assemblages the flying vertebrates, bats and birds, provide important and partly complementary ecosystem functions. We tested how bats and birds respond to land‐use intensification and compared abundance, species richness, and community composition across a land‐use gradient including forest, traditional agroforests (home garden), coffee plantations and grasslands on Mount Kilimanjaro, Tanzania. Furthermore, we asked how sensitive different habitat and feeding guilds of bats and birds react to land‐use intensification and the associated alterations in vegetation structure and food resource availability. In contrast to our expectations, land‐use intensification had no negative effect on species richness and abundance of all birds and bats. However, some habitat and feeding guilds, in particular forest specialist and frugivorous birds, were highly sensitive to land‐use intensification. Although the habitat guilds of both, birds and bats, depended on a certain degree of vegetation structure, total bat and bird abundance was mediated primarily by the availability of the respective food resources. Even though the highly structured southern slopes of Mount Kilimanjaro are able to maintain diverse bat and bird assemblages, the sensitivity of avian forest specialists against land‐use intensification and the dependence of the bat and bird habitat guilds on a certain vegetation structure demonstrate that conservation plans should place special emphasis on these guilds.     

Diverse pollinator communities enhance plant reproductive success

Understanding the functional consequences of biodiversity loss is a major goal of ecology. Animal-mediated pollination is an essential ecosystem function and service provided to mankind. However, little is known how pollinator diversity could affect pollination services. Using a substitutive design, we experimentally manipulated functional group (FG) and species richness of pollinator communities to investigate their consequences on the reproductive success of an obligate out-crossing model plant species, Raphanus sativus. Both fruit and seed set increased with pollinator FG richness. Furthermore, seed set increased with species richness in pollinator communities composed of a single FG. However, in multiple-FG communities, highest species richness resulted in slightly reduced pollination services compared with intermediate species richness. Our analysis indicates that the presence of social bees, which showed roughly four times higher visitation rates than solitary bees or hoverflies, was an important factor contributing to the positive pollinator diversity–pollination service relationship, in particular, for fruit set. Visitation rate at different daytimes, and less so among flower heights, varied among social bees, solitary bees and hoverflies, indicating a niche complementarity among these pollinator groups. Our study demonstrates enhanced pollination services of diverse pollinator communities at the plant population level and suggests that both the niche complementarity and the presence of specific taxa in a pollinator community drive this positive relationship.     

Potential negative effects of exotic honey bees on the diversity of native pollinators and yield of highland coffee plantations

• 1 The honey bee Apis mellifera is native to Eurasia and Africa, although it is commonly introduced into crop fields of different parts of the world because of the assumption that it improves yield. This bee is, however, a poor pollinator of several crops compared with native insects. Indeed, honey bees can displace native pollinators and reduce their diversity. The present study evaluated the potential impacts of A. mellifera on the diversity of native pollinators of highland coffee (Coffea arabica) and its putative consequences for coffee production at the state of Veracruz, Mexico.
• 2 The abundance of A. mellifera and diversity of native pollinators were assessed during blooming at 12 shade coffee plantations and pollination experiments were conducted to determine the impacts of pollinators on coffee fruit production. Regression analyses were used to assess whether the abundance of honey bees was related to native pollinator diversity, and whether fruit production was influenced by both the diversity of pollinators and the abundance of A. mellifera.
• 3 Native pollinator diversity decreased as the number of honey bees increased. Furthermore, although coffee fruit production was positively related to the diversity of native pollinators, an increasing abundance of A. mellifera was correlated with a decrease in fruit production.
• 4 Highland shade coffee plantations are considered as reservoirs of the Mexican insect fauna. Thus, native pollinator diversity could be better preserved if beekeepers reduced the number of managed hives that they brought into plantations. This may also help to increase coffee yield by decreasing the putative negative effects of A. mellifera on native pollinators.

     

Stability of pollination services decreases with isolation from natural areas despite honey bee visits

Sustainable agricultural landscapes by definition provide high magnitude and stability of ecosystem services, biodiversity and crop productivity. However, few studies have considered landscape effects on the stability of ecosystem services. We tested whether isolation from florally diverse natural and semi-natural areas reduces the spatial and temporal stability of flower-visitor richness and pollination services in crop fields. We synthesised data from 29 studies with contrasting biomes, crop species and pollinator communities. Stability of flower-visitor richness, visitation rate (all insects except honey bees) and fruit set all decreased with distance from natural areas. At 1 km from adjacent natural areas, spatial stability decreased by 25, 16 and 9% for richness, visitation and fruit set, respectively, while temporal stability decreased by 39% for richness and 13% for visitation. Mean richness, visitation and fruit set also decreased with isolation, by 34, 27 and 16% at 1 km respectively. In contrast, honey bee visitation did not change with isolation and represented > 25% of crop visits in 21 studies. Therefore, wild pollinators are relevant for crop productivity and stability even when honey bees are abundant. Policies to preserve and restore natural areas in agricultural landscapes should enhance levels and reliability of pollination services.     

Flowering banker plants for the delivery of multiple agroecosystem services

Ecosystem services provided by agricultural ecosystems include natural pest control and pollination, and these are important to ensure crop productivity. This study investigates the use of the banker plant Calendula officinalis L. to provide multiple ecosystem services by increasing the abundance of natural enemies for biological control of tomato pests, providing forage resources to wild bees, and improving crop yield. C. officinalis was selected for this experiment as it is used as a banker plant for Dicyphini (Hemiptera: Miridae) predators. Strips of flowering C. officinalis were established in the field edges of tomato fields and arthropod visitation to C. officinalis strips and tomato was measured. Crop damage from multiple pests of tomato was assessed in fields with C. officinalis strips and control sites. The contribution of pollination to crop yield was assessed through a pollinator exclusion experiment. The inclusion of C. officinalis in tomato fields was associated with increased abundance of Dicyphini, parasitoids, bees and other arthropod groups within these strips. A reduction in the total leaf crop damage from Lepidoptera pests was recorded in fields with C. officinalis strips. Increased fruit set and biomass were recorded in open-pollinated tomato but this was not significantly different between control and C. officinalis fields. Results presented here demonstrate that the inclusion of a companion plant can improve the conservation of beneficial arthropods and the delivery of agroecosystem services but efficacy is likely to be improved with the addition of plants, with different functional traits, and with improved attractiveness to crop pollinators.     

Vertical and Horizontal Vegetation Structure across Natural and Modified Habitat Types at Mount Kilimanjaro

In most habitats, vegetation provides the main structure of the environment. This complexity can facilitate biodiversity and ecosystem services. Therefore, measures of vegetation structure can serve as indicators in ecosystem management. However, many structural measures are laborious and require expert knowledge. Here, we used consistent and convenient measures to assess vegetation structure over an exceptionally broad elevation gradient of 866–4550m above sea level at Mount Kilimanjaro, Tanzania. Additionally, we compared (human)-modified habitats, including maize fields, traditionally managed home gardens, grasslands, commercial coffee farms and logged and burned forests with natural habitats along this elevation gradient. We distinguished vertical and horizontal vegetation structure to account for habitat complexity and heterogeneity. Vertical vegetation structure (assessed as number, width and density of vegetation layers, maximum canopy height, leaf area index and vegetation cover) displayed a unimodal elevation pattern, peaking at intermediate elevations in montane forests, whereas horizontal structure (assessed as coefficient of variation of number, width and density of vegetation layers, maximum canopy height, leaf area index and vegetation cover) was lowest at intermediate altitudes. Overall, vertical structure was consistently lower in modified than in natural habitat types, whereas horizontal structure was inconsistently different in modified than in natural habitat types, depending on the specific structural measure and habitat type. Our study shows how vertical and horizontal vegetation structure can be assessed efficiently in various habitat types in tropical mountain regions, and we suggest to apply this as a tool for informing future biodiversity and ecosystem service studies.     

Hand pollination of global crops – A systematic review

Global pollinator declines and land-use change can lead to pollination limitation with implications for agricultural productivity. Hand pollination is used in agricultural production as a technique to manually pollinate crops. But the prevalence of hand pollination, as well as benefits and costs, remain unknown. We systematically reviewed the literature for examples, methods, drivers, and economic motivations of hand pollination. Furthermore, we discuss the risks, constraints, and opportunities of hand pollination. We found evidence for 20 hand-pollinated crops, including minor but also economically important crops (e.g. apple, oil palm, cacao). The lack of pollinators was the most important reason for the application of hand pollination (50% of crops), while insufficient proportion or proximity of pollinizers (8% of crops) and skewed sex ratio or dichogamy (8% of crops) were second most important. The main economic motivations for practicing or recommending hand pollination were to increase fruit set, and/or fruit quality (78% of crops). Hand pollination is practiced in large- and small-scale farming, home gardens, and greenhouses. Opportunities of hand pollination are the control of pollen origin and quantity, pollination timing and frequency as well as independence from environmental fluctuations. Farmers can increase yields, improve fruit quality, avoid fruit abortion, increase employment, and secure subsistence food. The main constraints of hand pollination are high labor inputs, high material costs, and required skills. Major risks of hand pollination include management ignoring pollinator conservation, high food prices, over-pollination, labor accidents, and unfair labor. We conclude that in the face of global change, hand pollination allows improved control of pollination and is likely to increase in importance. The benefits of hand pollination need to outweigh the costs and fair labor is essential. Altogether, hand pollination can be a valuable tool for crop systems where pollinators are absent or are not reliable for sustaining high-quality crop production.     

Native bees buffer the negative impact of climate warming on honey bee pollination of watermelon crops

If climate change affects pollinator‐dependent crop production, this will have important implications for global food security because insect pollinators contribute to production for 75% of the leading global food crops. We investigate whether climate warming could result in indirect impacts upon crop pollination services via an overlooked mechanism, namely temperature‐induced shifts in the diurnal activity patterns of pollinators. Using a large data set on bee pollination of watermelon crops, we predict how pollination services might change under various climate change scenarios. Our results show that under the most extreme IPCC scenario (A1F1), pollination services by managed honey bees are expected to decline by 14.5%, whereas pollination services provided by most native, wild taxa are predicted to increase, resulting in an estimated aggregate change in pollination services of +4.5% by 2099. We demonstrate the importance of native biodiversity in buffering the impacts of climate change, because crop pollination services would decline more steeply without the native, wild pollinators. More generally, our study provides an important example of how biodiversity can stabilize ecosystem services against environmental change.