Pollinator-dependent Crops Research Articles

Resampling of wild bees across fifteen years reveals variable species declines and recoveries after extreme weather

Despite concerns about the status of wild bees, there have been few studies with repeated sampling of these insects at the same locations using the same method. There is an urgent need for longitudinal studies to understand species- and population-level dynamics and the drivers of change, especially in pollinator-dependent crop systems. We sampled wild bees in highbush blueberry fields in three multi-year sampling periods between 2004 and 2018 to determine changes in the wild bee community active during bloom. We captured 35% (162 species) of the known Michigan bee fauna across the three sampling periods. Andrena, Lasioglossum and Ceratina were the dominant genera, though species composition varied significantly between sampling periods. Wild bee abundance (measured as captures in the pan traps) declined 61% and richness declined 33% between the first (2004–2006) and second (2013–2014) sampling periods. This was followed by limited recovery in species abundance and richness in the third sampling period (2017–2018). Some species showed dramatic abundance declines, particularly the blueberry specialist Andrena carolina. By contrast, other species showed stable or increasing prevalence, and population trajectories were not correlated with life history traits. Potential causes of the observed decline include increased use of insecticides and extreme spring weather in 2012. While farms varied in pest management intensity and overall insecticide program risk increased over time, there was no correlation between bee declines and insecticide use. Insecticide program risk increased between the second and third sampling periods, while most species increased in abundance. We therefore conclude the observed declines were most likely caused by extreme spring weather in 2012 resulting in widespread damage to flowering plants that provide resources for bees. Long-term monitoring to identifying species more vulnerable to environmental perturbations can help guide conservation recommendations as extreme weather events become more common.

Managed honeybees and South American bumblebees exhibit complementary foraging patterns in highbush blueberry

Despite Apis mellifera being the most widely managed pollinator to enhance crop production, they are not the most suitable species for highbush blueberries, which possess restrictive floral morphology and require buzz-pollination. Thus, the South American bumblebee Bombus pauloensis is increasingly managed as an alternative species in this crop alongside honeybees. Herein, we evaluated the foraging patterns of the two species, concerning the potential pollen transfer between two blueberry co-blooming cultivars grown under open high tunnels during two seasons considering different colony densities. Both managed pollinators showed different foraging patterns, influenced by the cultivar identity which varied in their floral morphology and nectar production. Our results demonstrate that both species are efficient foragers on highbush blueberry and further suggest that they contribute positively to its pollination in complementary ways: while bumblebees were more effective at the individual level (visited more flowers and carried more pollen), the greater densities of honeybee foragers overcame the difficulties imposed by the flower morphology, irrespective of the stocking rate. This study supports the addition of managed native bumblebees alongside honeybees to enhance pollination services and emphasizes the importance of examining behavioural aspects to optimize management practices in pollinator-dependent crops.

Using RNA-seq to characterize pollen\u2013stigma interactions for pollination studies

Insects are essential for the reproduction of pollinator-dependent crops and contribute to the pollination of 87% of wild plants and 75% of the world’s food crops. Understanding pollen flow dynamics between plants and pollinators is thus essential to manage and conserve wild plants and ensure yields are maximized in food crops. However, the determination of pollen transfer in the field is complex and laborious. We developed a field experiment in a pollinator-dependent crop and used high throughput RNA sequencing (RNA-seq) to quantify pollen flow by measuring changes in gene expression between pollination treatments across different apple (Malus domestica Borkh.) cultivars. We tested three potential molecular indicators of successful pollination and validated these results with field data by observing single and multiple visits by honey bees (Apis mellifera) to apple flowers and measured fruit set in a commercial apple orchard. The first indicator of successful outcrossing was revealed via differential gene expression in the cross-pollination treatments after 6 h. The second indicator of successful outcrossing was revealed by the expression of specific genes related to pollen tube formation and defense response at three different time intervals in the stigma and the style following cross-pollination (i.e. after 6, 24, and 48 h). Finally, genotyping variants specific to donor pollen could be detected in cross-pollination treatments, providing a third indicator of successful outcrossing. Field data indicated that one or five flower visits by honey bees were insufficient and at least 10 honey bee flower visits were required to achieve a 25% probability of fruit set under orchard conditions. By combining the genotyping data, the differential expression analysis, and the traditional fruit set field experiments, it was possible to evaluate the pollination effectiveness of honey bee visits under orchards conditions. This is the first time that pollen-stigma-style mRNA expression analysis has been conducted after a pollinator visit (honey bee) to a plant (in vivo apple flowers). This study provides evidence that mRNA sequencing can be used to address complex questions related to stigma–pollen interactions over time in pollination ecology.

Insect pollination and sustainable agriculture in Sub-Saharan Africa

We are currently seeing an expansion of pollinator-dependent crops in many parts of the world, but also growing evidence for pollinator population declines and loss of pollinator habitat. Climate change and population growth will place additional demands on crop production, especially in Sub-Saharan Africa (SSA). Despite the wealth of evidence that improved management of insect pollinators can lead to substantial gains in crop yield, agricultural improvement strategies in SSA still emphasize the manipulation of abiotic factors and do not fully exploit the value of pollinators. In this article we review the importance of pollination services in sustainable agriculture, how global perspectives can inform our understanding of the situation in SSA, discuss successful pollination management, highlight where research and development are required, and suggest possible solutions to enhance the contribution of pollination services to sustainable agriculture in the region.

Wild insect diversity increases inter-annual stability in global crop pollinator communities.

While an increasing number of studies indicate that the range, diversity and abundance of many wild pollinators has declined, the global area of pollinator-dependent crops has significantly increased over the last few decades. Crop pollination studies to date have mainly focused on either identifying different guilds pollinating various crops, or on factors driving spatial changes and turnover observed in these communities. The mechanisms driving temporal stability for ecosystem functioning and services, however, remain poorly understood. Our study quantifies temporal variability observed in crop pollinators in 21 different crops across multiple years at a global scale. Using data from 43 studies from six continents, we show that (i) higher pollinator diversity confers greater inter-annual stability in pollinator communities, (ii) temporal variation observed in pollinator abundance is primarily driven by the three-most dominant species, and (iii) crops in tropical regions demonstrate higher inter-annual variability in pollinator species richness than crops in temperate regions. We highlight the importance of recognizing wild pollinator diversity in agricultural landscapes to stabilize pollinator persistence across years to protect both biodiversity and crop pollination services. Short-term agricultural management practices aimed at dominant species for stabilizing pollination services need to be considered alongside longer term conservation goals focussed on maintaining and facilitating biodiversity to confer ecological stability.

Honey bee hives decrease wild bee abundance, species richness, and fruit count on farms regardless of wildflower strips

Pollinator refuges such as wildflower strips are planted on farms with the goals of mitigating wild pollinator declines and promoting crop pollination services. It is unclear, however, whether or how these goals are impacted by managed honey bee (Apis mellifera L.) hives on farms. We examined how wildflower strips and honey bee hives and/or their interaction influence wild bee communities and the fruit count of two pollinator-dependent crops across 21 farms in the Mid-Atlantic U.S. Although wild bee species richness increased with bloom density within wildflower strips, populations did not differ significantly between farms with and without them whereas fruit counts in both crops increased on farms with wildflower strips during one of 2 years. By contrast, wild bee abundance decreased by 48%, species richness by 20%, and strawberry fruit count by 18% across all farm with honey bee hives regardless of wildflower strip presence, and winter squash fruit count was consistently lower on farms with wildflower strips with hives as well. This work demonstrates that honey bee hives could detrimentally affect fruit count and wild bee populations on farms, and that benefits conferred by wildflower strips might not offset these negative impacts. Keeping honey bee hives on farms with wildflower strips could reduce conservation and pollination services.

Economic Dependence and Vulnerability of United States Agricultural Sector on Insect-Mediated Pollination Service.

Deficits in insect-mediated pollination service undermine ecosystem biodiversity and function, human nutrition, and economic welfare. Global pollinator supply continues to decline, while production of pollination-dependent crops increases. Using publicly available price and production data and existing pollination field studies, we quantify economic dependence of United States crops on insect-mediated pollination service at the county level and update existing coefficients of insect dependence of sample crops when possible. Economic value dependent on pollination service totals 34.0 billion USD in 2012. Twenty percent of US counties produce 80% of total economic value attributable to insect pollinators. We compile county-level data and consider the spatial relationship between economic value dependent on insect-mediated pollination, region-specific forage suitability, and crop-specific agricultural areas within US landscapes. We identify vulnerable, highly dependent areas where habitat for wild pollinators has been reduced. These results can help inform future efforts to conserve and bolster managed and wild pollinator populations to ensure sustainable production of key agricultural crops.

Restoring farmlands for food and nature

Changes in the intensity and extent of farmland have a profound impact on life on Earth. Although nature-rich farmlands have conservation value, their promotion competes with the protection and restoration of natural habitat. Restoring the productive capacity of existing farmland can help maximize opportunities for the restoration of both nature-rich farmlands and natural habitat.

Higher richness and abundance of flower-visiting insects close to natural vegetation provide contrasting effects on mustard yields

The conservation of pollinating insects in agriculture is a global concern since the diversity of such organisms may affect the productivity of pollination-dependent crops. In this study, we assessed (i) how distances from natural vegetation affect the diversity (guilds, richness, abundance) of flower-visiting insects within mustard crops in Nepal, (ii) how insect richness and abundance are related to mustard yields (weight of seeds) and (iii) the contribution of flower-visiting insects to mustard pollination by conducting pollinator exclusion experiments. To analyse these data, we carried out (i) hierarchical clustering followed by a Procrustes analysis as well as a generalized linear mixed model and (ii), (iii) linear mixed models. We found that the guild composition was not similar near and far from natural vegetation, indicating a tendency for Apis bees to displace in opposite directions relative to non-Apis bees. Nevertheless, while both richness and abundance were higher nearer natural vegetation, the former showed a stronger and more positive effect on mustard yields than the latter. Furthermore, we found that mustard flowers have a significant requirement for insect pollination since productivity increased by ~70% with insect visitation. Overall, our data suggest that the diversity of flower-visiting insects enlarges nearer to natural vegetation. However, the results indicate that species richness may be more relevant than abundance to mustard production. As such, we suggest that the maintenance of natural vegetation could be considered a strategy for ensuring the presence of multiple pollinator species within mustard fields to promote its long-term sustainability in Nepal.

Reconciling coffee productivity and natural vegetation conservation in an agroecosystem landscape in Brazil

Politicians have approved significant changes to the Brazilian Forest Code (Brazilian Law n. 12.651/2012), providing partial pardons for illegal deforestation in 2012. Nonetheless, the New Forest Code (NFC) may cause economic harm, since ecosystem services may be affected, and the productivity of several crops may end up decreasing. Here, we explored two sets of factors, one at a narrow-scale – the loss of close natural vegetation cover – and another at a wide-scale considering implications at a landscape level to measure the effects of the presence/absence of forest remnants, and consequently, of pollinators, on coffee productivity. The narrow-scale perspective used manipulative experiments in ten coffee plantations, and the wide-scale perspective considered secondary data on coffee productivity in planted and native forests of 61 municipalities to test the hypotheses: i) coffee branches with pollinator access are more productive; ii) coffee crops in contact with native forest remnants are more productive; iii) coffee plants located near to native forest remnants are more productive; iv) coffee productivity increases with the municipality area occupied by native forest remnants, and, v) coffee productivity decreases with the municipality area occupied by Eucalyptus spp. At the narrow-scale, we detected 32 % higher coffee productivity when pollinators were present (hypothesis i) and 15 % higher productivity when forest remnants were in contact with the plantation (hypothesis ii), but no differences related to forest remnants in the broader area (hypothesis iii). At the wide-scale, we observed that a higher amount of native forest cover increased coffee productivity (hypothesis iv), while increased Eucalyptus spp. plantations reduced coffee productivity (hypothesis v). The corroboration of hypotheses i, ii, and iv illustrates the importance of animal pollination and native vegetation remnants fr coffee productivity. The findings for hypothesis v reinforce that Eucalyptus spp. plantations are not good surrogates for native vegetation as part of management recovery action for deforested areas. Following the New Forest Code’s recommendations in Article 22 (Chapter IV, Section II), the preservation of native vegetation, species diversity, and native species regeneration should be attended to in legally instituted natural reserves. Our findings improve discernment that natural areas' devastation or its coverage using planted forest may reduce productivity levels of coffee plantations, representing a disruption of natural complexity, of organisms' connectivity, and consequently of ecosystem services as the pollination and pollinator-dependent crops' productivity, as the coffee.

Learning of a Mimic Odor within Beehives Improves Pollination Service Efficiency in a Commercial Crop

The growing global demand for pollination services leads producers to consider new strategies in pollinator management to improve its efficiency in agroecosystems [1-3]. Central place foragers, like honeybees, learn floral cues not only in the field but also inside the nest, where resource cues introduced into the hive improve foraging by guiding bees toward the learned stimuli [4]. In this regard, attempts to condition bees with crop-odor-scented food produced ambiguous results and lacked yield measurements [5-7]. To deepen our understanding of the use of odors as part of a precision pollination strategy, we developed a simple synthetic odorant mixture that bees generalized with the natural floral scent of sunflower for hybrid seed production, an economically important and highly pollinator-dependent crop [8]. Encompassing different experimental approaches, our results show that feeding colonies food scented with the sunflower mimic (SM) odor enabled the establishment of olfactory memories that biased bees to the sunflower crop. The offering of a rewarded odor mimicking the sunflower floral fragrance promoted higher foraging activity, increased the proportion of dances advertising the target inflorescences and reduced delays in dance onset, positively affected the density of bees on the crop, and increased yields from 29% to 57% in different sunflower hybrids. This study highlights the role of olfactory learning within the social context of the hive to bias foraging preferences in a novel agricultural environment and suggest that improvements in the tested parameters were due to beeś anticipated response to the sunflower scent.

Comparison of Biochemical Constituents and Contents in Floral Nectar of Castanea spp.

Pollination is essential for efficient reproduction in pollinator-dependent crops that rely on the attraction of pollinators to flowers. Especially, floral nectar is considered to be an important factor attracting pollinator like honey bees, but differences among major chestnut species (Castanea crenata, C. mollissima, C. dentata, and C. sativa) are still little explored. This study aims to evaluate the value of honey source by analyzing floral nectar characteristics and comparing the composition of volatile organic compounds (VOCs) that mediate plant-pollinator interaction. In this study, we analyzed nectar samples obtained from male flowers using HPLC and HS-SPME/GC–MS. The five chestnuts showed significant differences between the volume of secreted nectar, free sugar composition, amino acid content and VOCs composition. Furthermore, C. crenata (Japanese cultivar ‘Ungi’) was revealed to emit the highest total amounts of VOCs and high levels of benzenoid compounds that are generally associated with flower-visiting insects. The sugar content per catkin, which is used to determine the honey yield, was the highest in C. crenata, suggesting that C. crenata ‘Ungi’ can be highly valued as a honey tree. Therefore, a better understanding of the relationship between pollinator and nectar characteristics of C. crenara could contribute to a prospective honey plant.

Do farmers care about pollinators? A cross-site comparison of farmers’ perceptions, knowledge, and management practices for pollinator-dependent crops

ABSTRACT Pollinator conservation has become a key challenge to achieve sustainable agricultural landscapes and safeguard food supplies. Considering the potential negative effects of pollinator decline, international efforts have been developed to promote agri-environmental measures and pollinator-friendly management practices. However, little effort has been devoted to farmers’ perceptions and knowledge about pollinators, or to farmers’ role in enhancing pollination. We administered 376 face-to-face questionnaires in four areas of Spain with different dominant pollinator-dependent crops, to assess the factors behind farmers’ perceptions, knowledge, and practices adopted to promote pollination. Overall, 92.7% of the respondents recognized that pollinator insects are necessary for crop production, and 73.4% perceived pollinator decline in their farms. We found that farmers had moderate knowledge about pollinators (6.1 ± 1.8, on a 1–10 scale). The most applied practices to promote pollinators were reducing insecticide spraying (53.2% of respondents), diversifying crops (42.8%), and increasing fallow fields (39.1%). Factors such as education, age, concern about the pollinator crisis, and professional dedication to agriculture strongly influenced farmers’ knowledge and current application of pollinator-friendly practices. Implications of our results for the ongoing reform of the Common Agricultural Policy are discussed, highlighting the need to increase engagement and trust of farmers through communication and technical assistance.

Crop production in the USA is frequently limited by a lack of pollinators.

Most of the world's crops depend on pollinators, so declines in both managed and wild bees raise concerns about food security. However, the degree to which insect pollination is actually limiting current crop production is poorly understood, as is the role of wild species (as opposed to managed honeybees) in pollinating crops, particularly in intensive production areas. We established a nationwide study to assess the extent of pollinator limitation in seven crops at 131 locations situated across major crop-producing areas of the USA. We found that five out of seven crops showed evidence of pollinator limitation. Wild bees and honeybees provided comparable amounts of pollination for most crops, even in agriculturally intensive regions. We estimated the nationwide annual production value of wild pollinators to the seven crops we studied at over $1.5 billion; the value of wild bee pollination of all pollinator-dependent crops would be much greater. Our findings show that pollinator declines could translate directly into decreased yields or production for most of the crops studied, and that wild species contribute substantially to pollination of most study crops in major crop-producing regions.

Pollen Loads of Flower Visitors to Açaí Palm (Euterpe oleracea) and Implications for Management of Pollination Services.

Understanding the functional roles of different pollinator species is crucial to the development of sustainable farming practices in pollinator-dependent crops. However, this can be challenging for crop plants in tropical regions with hyper-diverse pollinator communities. Here, we assess pollen loads of different insect visitors to inflorescences of açaí palm (Euterpe oleracea), the most important native crop in the Amazon estuary region. Flower-visiting insects were collected from pistillate (female) inflorescences at eight sites, including four managed floodplain forests and four plantations. Pollinator Importance Value Index (PIVI) and Relative Importance (RI) scores were calculated for common visitor taxa (≥ 10 individuals) using sum visit frequencies and median pollen loads. Pollen load analyses revealed that over seventy insect taxa, including bees, flies, beetles, wasps and ants, were effective vectors of E. oleracea pollen. Native bees, including both solitary and eusocial taxa, were the most efficient pollen vectors, with median pollen loads at least eight times higher than those of the next best insect group (flies). Insect pollen loads were at their highest between 0800 and 1300 hours, and four insect taxa had RI scores > 0.05, including two meliponine bees belonging to the Trigona genus (Trigona branneri Cockerell and Trigona pallens Fabricius) and two halictid bee genera (Augochloropsis and Dialictus). Our results suggest that native bees play an important role in açaí pollination and should be the primary focus of pollinator management in açaí production systems.

Are All Colonies Created Equal? The Role of Honey Bee Colony Strength in Almond Pollination Contracts

This paper examines how honey bee population dynamics, the scale and timing of almond bloom, and unmarketability of almond honey interact to create misaligned incentives for growers and beekeepers in the California almond pollination services market. We combine economic contract theory with data from the first pollination contract survey to examine the design of pollination contracts. 89.2% of respondents used contracts with minimum colony population requirements, suggesting that all colonies are not considered to be equal providers of pollination services. Contracts that involved enforcement every year provided the highest pollination fees on average, while those with no enforcement provided the lowest fees. We contribute to the literature regarding pollination services by demonstrating that the number of hives and price per hive present an incomplete picture of almond pollination transactions without information regarding colony strength requirements and enforcement. We also provide a theoretical rationale for why almond pollination agreements have anecdotally become more formal over time: as the marginal value of colony strength increases, the grower offers the beekeeper stronger incentives to provide high colony strength. California almond production is an extreme case of a crop relying almost solely on managed pollinators, but ultimately could reflect the future for many pollinator-dependent crops if pollinator populations continue to decrease while monoculture crop production increases.

The Role of Flies as Pollinators of Horticultural Crops: An Australian Case Study with Worldwide Relevance.

Australian horticulture relies heavily on the introduced managed honey bee, Apis mellifera Linnaeus 1758 (Hymenoptera: Apidae), to pollinate crops. Given the risks associated with reliance upon a single species, it would be prudent to identify other taxa that could be managed to provide crop pollination services. We reviewed the literature relating to the distribution, efficiency and management potential of a number of flies (Diptera) known to visit pollinator-dependent crops in Australia and worldwide. Applying this information, we identified the taxa most suitable to play a greater role as managed pollinators in Australian crops. Of the taxa reviewed, flower visitation by representatives from the dipteran families Calliphoridae, Rhiniidae and Syrphidae was frequently reported in the literature. While data available are limited, there was clear evidence of pollination by these flies in a range of crops. A review of fly morphology, foraging behaviour and physiology revealed considerable potential for their development as managed pollinators, either alone or to augment honey bee services. Considering existing pollination evidence, along with the distribution, morphology, behaviour and life history traits of introduced and endemic species, 11 calliphorid, two rhiniid and seven syrphid species were identified as candidates with high potential for use in Australian managed pollination services. Research directions for the comprehensive assessment of the pollination abilities of the identified taxa to facilitate their development as a pollination service are described. This triage approach to identifying species with high potential to become significant managed pollinators at local or regional levels is clearly widely applicable to other countries and taxa.

Pollination ecosystem services: A comprehensive review of economic values, research funding and policy actions

Economic valuation of crop pollination services, including potential monetary losses in agricultural production induced by insufficient pollination, is a strategy to quantify the impacts of this critical ecosystem service on food production, food security and the global economy, and to drive policy actions. We examined how the economic valuation of crop pollination services has been investigated across the ecological and economics literature and review estimates of monetary values of crop pollination services, as well as the investments (research funding/grants) and policy actions associated with pollinators and pollination. We documented an increase in the number of economic valuation studies on pollination services in the last two decades, with a substantial growth over the last five years, which represented 54% of all publications. However, we emphasize that there is a marked lack of data on regionally important commercial crops that are essential for the food security of many millions of people, particularly in developing countries. Estimated global values of the crop pollination service, adjusted for inflation in March/2020, range widely from US$195 billion to ~US$387 (US$267–657) billion annually — due to methodology, input data and a historical increase in production costs of pollinator-dependent crops. There is an increasing trend over time in the values of crop pollination service estimates for the full set of main globally-grown crops, although estimates for specific crops are widely variable at local to regional scales. Research funding on pollination/pollinators is mainly in developed countries, which have published all the reviewed policy papers on the economic value of crop pollination services. Although the valuation of pollination services, and associated economics and policy remain embryonic areas of research, animal-mediated pollination is clearly a high-value environmental service, which greatly strengthens conservation arguments worldwide.

Bees increase crop yield in an alleged pollinator-independent almond variety

Wild pollinators are declining and the number of managed honey bee colonies is growing slower than agricultural demands for pollination. Because of these contrasting trends in pollinator demand and availability, breeding programs for many pollinator-dependent crops have focused on reducing the need for pollinators. Although numerous crop varieties are now available in the market with the label of pollinator-independent, the real dependence of these varieties on pollinators is mostly unknown. We evaluated the hypothesis of pollinator independence in the Independence almond variety, the fastest growing variety in California that is the main almond production region in the world. In this presumed pollinator-independent variety, we measured the effect of honey bees on fruit set, yield, and kernel nutritional quality at tree level. Fruit set was 60% higher in bee-pollinated than bee-isolated trees, which translated into a 20% increase in kernel yield. Despite its effect on almond production, there was no evidence that bee visitation affected almond nutritional quality. Based on these results, we recommend the use of bees, whether they are wild or managed, to maximize yield even in self-fertile almond varieties.

Cucurbits as a model system for crop pollination management

Cucurbit crops have steadily increased in production over the last 50 years, particularly in Asia where pioneering technological advancements and genetic improvements have created new hybrid varieties. Generally, cucurbits are dependent on insect-pollination for fruit set and are popular species for pollination studies. This review systematically summarises pollination research conducted in the major food genera of cucurbits: Cucurbita, Cucumis, and Citrullus, to ask: 1) what are cucurbits’ requirement for pollination and their most effective pollinators? And 2) Does pollinator management increase pollinator visitation to, and yield of, cucurbit crops? These accounts of cucurbit pollination demonstrate that wild bee species such as Bombus terrestris, B. impatiens and Eucera spp. were frequently able to fulfil the pollination requirements of multiple cucurbit species. However, pollinator behaviour, pollen deposition on stigmas, and pollinators’ contribution to yield vary between cucurbit species and study site. Nonetheless, the provision of additional floral resources at both field and farm scales may help to encourage pollination of cucurbit species whilst supporting pollinators’ nutritional requirements beyond those already provided by the cucurbit crop. Synthesising studies on cucurbits’ requirement for pollination and how pollinators vary spatially and temporally in the landscape can extend beyond cucurbit systems to inform growers and pollination ecologists of other pollinator-dependent crop species wishing to maximise pollination services, species conservation; or both.