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ARS Home » Pacific West Area » Logan, Utah » Pollinating Insect-Biology, Management, Systematics Research » Research » Research Project #437810

Research Project: Sustainable Crop Production and Wildland Preservation through the Management, Systematics, and Conservation of a Diversity of Bees

Location: Pollinating Insect-Biology, Management, Systematics Research

2024 Annual Report


Objectives
Objective 1: Improve crop pollination by alfalfa leafcutting bees, bumble bees and mason bees by identifying the environmental and biological factors that impact bee health during propagation and pollination and develop new and improved bee management strategies to ensure healthy, sustainable pollinator populations. Subobjective 1.1: Improve best management practices for pollinator use in cropping systems that result in sustainable pollinator supply for continued crop pollination. Subobjective 1.2: Identify impacts of xenobiotic factors on managed bee health (climatic factors, phenological mismatch, temperature range, etc.), host-plant [nutritional value/ host plant chemicals], invasives, pesticides. Subobjective 1.3: Examine the linkage between nutrition and bee performance in non-Apis bees (immunity, longevity, and reproduction). Subobjective 1.4: Develop effective treatments of pathogen, pest, and parasites in non-Apis bees. Subobjective 1.5. Devise new sampling and diagnostic methods for bee pests and diseases. Objective 2: Improve bee systematics and develop new tools for rapid bee identification to enhance the understanding of wild bee diversity and the identification of environmental and biological factors that promote wild bee sustainability. Subobjective 2.1: Evaluate bee biodiversity and improve the taxonomic and systematic knowledge needed to achieve effective bee conservation stewardship.


Approach
Objective 1: Improve crop pollination by alfalfa leafcutting bees, bumble bees and mason bees by identifying the environmental and biological factors that impact bee health during propagation and pollination and develop new and improved bee management strategies to ensure healthy, sustainable pollinator populations. 1.1. Hypotheses will be tested using field studies with measurement of bee health and pollination performance to improve management of mason bees and bumble bees. Experiments will examine interactions of mason with honey bees in co-deployment and impacts on pathogens as detected using molecular methods. 1.2. Exposure to agrichemicals via soil and leaf pieces by solitary bees will be quantified. The hypothesis that sublethal exposure agrichemicals including adjuvants impacts bee health will be tested for honey bees and alfalfa leafcutting bees using experimental manipulation and examine interactions with pathogens. 1.3. Hypotheses will be tested that nutrition (amino acid and sugar sources) can impact the reproduction and life span of alfalfa leafcutting bees. We will determine how the nutritional requirements of a bumble bee colony changes during colony age, as well as the maximal and minimal foraging range of Bombus huntii. 1.4. Hypotheses to examine control of chalkbrood and pollen ball formation via antimicrobial disinfectants will be tested for solitary bees. The life cycle and control of a major emerging parasitoid (Melittobia sp.) in alfalfa leafcutting bees will be determined. 1.5. Molecular methods will identify parasites, parasitoids, and pathogens of mason bees and alkali bees. Non-lethal methods to sample bumble bees parasites and pathogens will be developed. With molecular data, we will identify the species of Melittobia found in managed bees and characterize genetic diversity across populations. Objective 2: Improve bee systematics and develop new tools for rapid bee identification to enhance the understanding of wild bee diversity and the identification of environmental and biological factors that promote wild bee sustainability. We will 1) develop up-to-date taxonomies informed by phylogeny, 2) produce web-accessible bee identification tools, and 3) capture biological data present in museum specimens. To accomplish this, we will continue our efforts to survey bees across the western U.S, digitize bee collections, and conduct systematic studies of groups in need of revision. We will use molecular data, especially phylogenomic information derived from DNA sequences using ultra-conserved elements, to build phylogenies and refine species boundaries. The sequence information will be combined with taxonomic keys and images to allow non-experts to more easily identify bees.


Progress Report
This report documents FY 2024 progress for Project 2080-21000-019-000D “Sustainable Crop Production and Wildland Preservation through the Management, Systematics and Conservation of a Diversity of Bees”, which started in March 2020. Of the 20,000 bee species worldwide, few are successfully managed to pollinate agricultural crops; although, pollination by native bees species can impact crop yield and quality. ARS scientists in Logan, Utah, continue research to improve production and management of social and solitary bees, seek novel pollinators to meet pollination needs, and learn how native bee populations contribute to crop pollination. The project has two goals: (1) Improve crop pollination by non-Apis bees by identifying factors impacting bee health and develop bee management strategies to ensure pollinator populations; (2) Improve bee systematics and develop new tools for bee identification for understanding of wild bee diversity and presence. Research was reported on solitary bees, bumble bees, and honey bees to the general public, alfalfa seed producers, almond growers, fruit growers, bee producers, honey bee keepers, and agencies such as: Animal and Plant Health Inspection Service (APHIS) Plant Protection and Quarantine Program, U.S. Forest Service (USFS), Natural Resources Conservation Service (NRCS), U.S. Fish and Wildlife Service (FWS), Bureau of Land Management (BLM), National Parks Service (NPS), U.S. Geological Services (USGS), and U.S. Environmental Protection Agency (EPA). In support of Sub-objective 1.1, research was performed in almond orchards in California, berry crops in Utah, and alfalfa seed production in western states. Berry crops benefit from insect pollination and common managed pollinators do not maximize yields. Three mason bee species (Osmia lignaria, O. ribifloris, and O. bruneri) were tested as alternative managed pollinators in berry crops (currants, blueberries, strawberries, raspberries, blackberries), by monitoring nesting activity, analyzing collected pollen, and observing crop flowers. Results suggest that O. ribifloris should be further explored as a managed pollinator for blueberry pollination and O. bruneri for pollination of currants. A multi-year study examining impacts of warming temperatures on Osmia lignaria was completed in California almonds and demonstrated that O. lignaria can adapt to warming environments. The bee has better reproduction and greater efficiency in pollination when populations are acclimated to their environment. For Sub-objective 1.2, research on impacts of pesticides and minimizing these effects is being done. Wildflower plantings are planted to support wild bees and provide bees critical resources (pollen, nectar, nesting resources). How these plantings mitigate pesticide exposures was tested by ARS researchers in Logan, Utah, by measuring pesticide residues associated with wildflower plantings near blueberry fields in Michigan. Wildflowers in plantings were contaminated with pesticides by drift and did not reduce bumble bees’ pesticide exposure. The timing of pesticide applications impacts effectiveness against target pests. Having accurate pesticide dissipation models is needed for predicting how long an application will be effective against target pests and in determining when a crop will be dangerous to pollinators. In collaboration with colleagues at Utah State University (USU), ARS researchers used data from field applications to build dissipation models for four insecticides used by alfalfa seed growers. Insecticides were applied to experimental alfalfa, followed by collecting plant materials at set time intervals, and measuring residue levels. Data were used to optimize the Pesticide Dissipation from Agricultural Land (PeDAL) model, developed by USU. Chemical control is needed to control pests in alfalfa seed production. Lygus bugs are particularly damaging during flowering when bees are needed for pollination. Finding chemical control options that are safe for bees is a priority. ARS researcherstested the safety of two insecticides (afidopyropen and sulfoxaflor) on alfalfa leafcutting bees. Both can be used during bloom for Lygus bug control. Afidopyropen appears safe for alfalfa leafcutting bees, with no measurable effects. Sulfoxaflor increased bee mortality and should be used with caution during bloom when bees are foraging. For Sub-objective 1.3, research is being done on new pollinator seed mixes. For sustainable production of bees and improved colony health of honey bees, can tailored pollinator seed mixes be established to support wild and managed bees in the Great Basin with no supplemental irrigation, low rainfall, and prolonged droughts? In collaboration with the Forage and Range Unit, ARS researchers developed a pollinator planting seed mix and are testing its establishment at Great Basin sites. Research is testing if plant establishment increases via use of artificial and biological snow fences to trap winter snow. Bee communities are being documented before and after planting establishment. In 2025, bumble bees, honey bees, and mason bees will be placed in the plantings to document use of floral resources, reproduction, and bee health. In support of Sub-objective 1.5, research on pathogens was done for several bee species. For honey bees, bumble bees, and the blue orchard bee, the viral pathogens were characterized. Honey bees from colonies in almond orchards had at least seven viral pathogens (ssRNA viruses and a DNA virus). When colonies were moved into a non-Ag, forest in Utah, the number of viruses and titers decreased. The colonies were infected with a DNA virus (Apis mellifera filamentous virus, AmFV) at high levels. Bumble bee colonies had increased viral detections when placed into areas with honey bees and other bee species, but ssRNA viruses were not associated with colony death nor impacts on queen production. The AmFV virus was in newly emerged queens, not a result of pathogen spillover from honey bees, and highly correlated with death of bumble colonies. The solitary bee Osmia lignaria was found to clear all ssRNA viruses at metamorphosis into pupae, without impact on survival. AmFV was found in wild populations of O. lignaria and caused death when fed to larvae. Additional research on host-specificity and impacts of AmFV is needed. For Sub-objective 2.1, ARS researchers in Logan, Utah, are collaborating with the Office of the Chief Scientist, researchers in NRCS (Plants database), other USDA researchers, and Environmental Systems Research Institute, Inc. (ESRI) to create a knowledge graph that allows for analysis of plant/pollinator interactions. In addition, collaboration with international researchers and data scientists was made to create plant/pollinator interaction terms for use in databasing via a WorldFAIR project. ARS researchers in Logan, Utah, are testing if wildfire mitigation practices, such as thinning and creation of slash piles, impact the wild bee community in the Uinta Mountains, Utah. Part of the thinning process is creation of wood piles, called slash piles. Slash piles are eventually burned, with unknown impact on the cavity nesting bee community. Wild bee community data is being collected at sites with wildfire treatments (thinning) and slash pile management (burning or letting piles remain). Tests were done for differences in genetic diversity and structure of four bumble bee species in the western United States by ARS researchers in Logan, Utah, and collaborators. In bumble bee species, there are differences in how habitat heterogeneity correlates to genetic structure and isolation. Focused study on population genetics of the rusty patched bumble bee demonstrates the relationship between genetic diversity and location, providing context for the potential risks of translocation programs by conservation biologists. This work helps set clear recovery targets for endangered bumble bee species and can guide conservation efforts. New research on use of non-lethal methods for identification of bees in bee surveys is being done at the Sacramento River Wildlife Refuge, California. For the first time, non-lethal methods (including eDNA, artificial flowers, and imaging) are being used for a bee survey. If successful, this will revolutionize the way bee surveys are conducted for conservation. Collaborative research by ARS researchers and Kansas State University (KSU) increased the utility of an app that uses high quality images and artificial intelligence algorithms for species level identification. The “Bee Machine” developed by KSU has been expanded for identification of all U.S. bumble bee species and identification of other bees to the genera level. ARS scientists are working to develop a reference library of DNA barcodes for U.S. bees and to create a low-cost protocol for barcoding using the Oxford Nanopore Minion. A protocol to generate full- and mini-DNA barcodes using the MinION sequencer was validated, with multiple primers and tissues being tested. In the Beenome100+, ARS scientists in Logan, Utah, are helping to sequence reference genomes for 100+ U.S. bee species. Progress to collect, sequence samples, assemble, and analyze genomic sequence data continues. To date, 207 species have been collected and submitted for sequencing. Some data have been generated for 170 species and complete data for 82 species. ARS scientists are co-investigators on a collaborative project with scientists at Washington State University and Utah State University to improve and understand bee phylogeny and evolution using genomic methods. Low coverage genomic data and ultraconserved element phylogenomic data have been generated for bees from several genera.


Accomplishments
1. Pollinator plantings adjacent to blueberry fields do not reduce pesticide exposure in bees. Wildflower pollinator plantings installed to support wild bees adjacent to blueberry fields in Michigan were evaluated for their role in reducing pesticide exposures in wild bees. A research team led by an ARS researcher in Logan, Utah, found that presence of pollinator plantings did not reduce pesticide exposure in bumble bee collected pollen compared to sites without pollinator plantings. Wildflowers in plantings were contaminated with pesticides, sometimes at high levels, due to pesticide drift. These results provide evidence to growers, pesticide applicators, regulators, and researchers that pollinator plantings adjacent to agricultural fields can be sources of high-risk pesticide exposures for wild bees, and mitigation measures to reduce pesticide drift are needed. For growers that depend upon bee pollination for crop production, this is critical information.

2. Insecticides for Lygus bugs tested for bee safety and preservation of pollination services for alfalfa seed production. Alfalfa seed production requires bees for pollination and seed production. However, Lygus bugs are a major pest and often require use of pesticides to minimize crop damage during bloom. Bee-safe insecticides are needed to minimize harm to bees while protecting seed yields. ARS researchers in Logan, Utah, tested two insecticides (afidopyropen and sulfoxaflor) for impacts on alfalfa leafcutting bees. Afidopyropen appears to be a good candidate for pest control in blooming alfalfa fields when bees are also needed for pollination, with no measurable effects on bees. Sulfoxaflor increased bee mortality and should be used with caution during bloom. Alfalfa seed growers in western states will benefit from this research to ensure production of alfalfa seed.

3. Combined use of the blue orchard bee and honey bees in pear and cherry orchards results in increased yield, even in bad weather. Pollination of sweet cherries and pears can be difficult with unpredictable spring weather. ARS researchers in Logan, Utah, found that when blue orchard bees were added to honey bees in sweet cherry and pear orchards in Washington state, pollination efficacy increased by 12%. These results positively impact cherry and pear growers, especially those in Washington state or other areas where spring weather has become variable and cold snaps are common. The blue orchard bee flies at much cooler temperatures than honey bees, therefore acting as an added pollination insurance for the orchard growers.

4. Genomic data resolve species boundaries in the western bumble bee, a species of conservation concern. The western bumble bee, Bombus occidentalis, was once widespread in the western United States, but in the 1990s the species underwent a large decline. This bee is currently being considered for listing under the endangered species act. Uncertainty exists as to whether B. occidentalis is composed of one, two, or more species, making it hard to establish conservation targets. ARS researchers in Logan, Utah, in collaboration with university scientists, used genomic data to test species boundaries in B. occidentalis and found support for the existence of two, geographically separated species, B. mckayi in the north (Canada to Alaska), and B. occidentalis in the south (Canada and the contiguous United States). Both species occur in the United States and will need to be separately assessed for their conservation status. This data will support regulatory agencies and conservation measures.

5. Honey bees do not negatively impact other bee species when colony numbers do not exceed the amount of available floral resources. Honey bees have been in North America for more than 500 years and are critical pollinators for many crops, given the ability to move colonies into crops like almonds and fruit for pollination. Controversy about negative impacts of honey bees on other bee species caused stakeholders to ask for research to thoroughly investigate potential impacts of honey bee colonies on reproduction, interactions with floral hosts, and impacts of disease in other bee species. ARS researchers in Logan, Utah, conducted a controlled experiment with sentinel bumble bee colonies, solitary bees, and honey bees. In cages with limited floral resources, competition did impact all three types of bees equally. No negative interactions were observed on flowers. In the field, presence of 48 colonies of honey bees did not impact reproduction of bumble bees nor solitary bees. No negative impacts of disease transmission were found among the three types of bees. Conclusions were that the amount of floral resources or carrying capacity was critical in determining how many honey bee colonies could be supported without negative impacts on other bee species. Other factors such as climate (drought and heat) and other uses (grazing by cows or sheep) need to also be considered, given impacts on floral resources. This data is important for land managers, growers, and bee keepers; each want to conserve bee species for pollination.

6. Reproduction of solitary bees is greatly impacted by extreme drought. The western United States has been greatly impacted by increased drought and hot weather. ARS researchers in Logan, Utah, conducted experiments for three years monitoring reproduction of a solitary bee (Osmia bruneri) that nests in cavities. During the three years, drought ranged from moderate, to severe, to extreme. During the extreme years with decreased floral resources, the female bees reproduced significantly less, forming fewer nest cells. Significantly, the sex ratio (how many females versus males) greatly shifted also, going from a 1:1 ratio of females to males to a 1:3 ratio (one female per three males). This resulted in many fewer female bees for pollination in the next season; and this observation may explain significant population decreases being observed for some species. This impact of climate change is of concern, given the role of solitary bees in pollination or plant reproduction for crops and plants in natural ecosystems. This information is required by land managers, conservation biologists, and growers.

7. Insight into impacts of climate change on desert bees. What might happen to pollinators with changes in climate? A long-term study by ARS researchers in Logan, Utah, and with collaboration by university scientists tracked how populations of very diverse groups of bees changed across dry and wet years in a desert region. The 16-year study compared bee declines with how the bees respond to heat and dryness. The data were used to predict bee communities into the future. Drought had the most impact, affecting three out of four species. Forecasts for the future suggest declines for nearly half of the bee species with continued drought and heat. While overall abundance of bees is predicted to remain the same, this loss of species could affect pollination of plants, since some plants are pollinated by specific bees. Results of this study provide evidence that changes in climate directly threaten bee diversity. These findings are of value to land managers and policy makers.

8. No evidence of pollination limitation in a rare plant, the Las Vegas bear poppy. Arctomecon californica, the Las Vegas bear poppy, is a rare plant that is pollinator dependent for reproduction. Populations of the plant fluctuate year to year, as do the associated bee communities. ARS researchers in Logan, Utah, documented wild bee visitations and seed production at eight poppy populations in 2022 and 2023. No evidence was found for reproduction of these poppies being pollination limited. The poppies had high rates of seed production, even in a severe drought year with lower bee activity. These results are being used by the U.S. Fish and Wildlife Service in their species status assessment in considering an endangered species listing for the Las Vegas bear poppy.

9. Mojave Poppy Bee populations evaluated as a possible threatened species. The Mojave Poppy Bee, a rare bee of the eastern Mojave Desert, is being considered for listing as a threatened species. Fieldwork in 2024 by ARS researchers in Logan, Utah, concluded five years of searching for this bee. The bee remains present in many historic locations, but not all. The bee appears now to be extinct in southwestern Utah. This bee requires rare bear poppies or prickly poppies for food for its offspring. These plants only live for a few years so are not always found at known locations. This research also found that this bee can remain as an immature larva for at least three years, presumably to wait for good conditions. These findings on the current distribution and biology of this solitary bee will be shared with federal agencies for their evaluation.

10. Insight into the biology the Hunt bumble bee, a pollinator of agricultural importance, by development of high-quality genome. The Hunt bumble bee is an important pollinator found widely in western North America. To learn more about its biology and help with studies on its populations and breeding, ARS researchers in Logan, Utah, Hilo, Hawaii, and Stoneville, Mississippi, decoded the entire genetic code of a single male bee. Using advanced sequencing technologies, the ARS researchers put together a detailed map of its genome with high accuracy. This map shows how the bee's genetic material is organized into 18 chromosomes, covering a total of 317.4 million base pairs. This analysis indicates that over 97.6% of the genome is complete and correctly arranged. Importantly, the methods employed by the ARS researchers achieved high-quality genome assembly through efficient methods for studying and understanding genomes. This research benefits others wanting to create genomic information or protecting this bee’s health for pollination of crops and other plants.

11. New method of evaluating floral resources for plant management and pollinator health. Diverse flowers are needed to support healthy pollinator populations and important for plant reproduction. Traditional ways of counting flowers take a lot of time and people. Especially in large areas, these methods might miss changes in where and when flowers grow. Unmanned aerial vehicles (drones) can now be used to determine the distribution of flowers across big areas. ARS researchers in Logan, Utah used pictures from drones and a machine learning algorithm to count flowers in places like fields and forests, where land shapes, plants, and flower sizes change. The ARS researchers found seven types of flowers covering 2,138 square meters, which is 0.5% of the whole area studied. The researchers determined when flowers bloom by looking at how flower areas changed in the pictures. These models worked well even though there were very few flowers in the unmanned aerial vehicles pictures. This method of using images from drones to determine the diversity and number of flowers resources will greatly aid in management of lands to support healthy pollinators and plants by beekeepers, growers, and land managers.

12. New reference genome for the Mojave poppy bee, a species of conservation concern. The Mojave poppy bee, Perdita meconis, is an important pollinator of poppy plants in the Mojave Desert in southern Utah, Nevada, and California. The species is of conservation concern due to its limited distribution and reliance on few host-plant species and because it faces threats from urbanization, climate change, and other factors. To better understand the genetics of this species, ARS researchers in Logan, Utah, in collaboration with university partners, extracted DNA from a single male specimen of the species and generated a high-quality reference genome using long-read sequencing technology. The reference genome is the first for a major lineage of bees, and it will serve as an important tool for assessing the conservation status of P. meconis.

13. Insight into world-wide distribution of bee species via a new dataset. Specific information on where organisms such as bees have been found is essential for scientific research and communication, yet gathering these records from multiple sources is a major accessibility issue. ARS researchers in Logan, Utah, in collaboration with university scientists, created a new global bee occurrence dataset, providing data on distribution, seasonality, and floral relationships. Existing bee occurrence data were merged and standardized from major data repositories and private datasets using a reproducible R-workflow. The dataset gives a common taxonomic name, location, and collection date. The computer code used to merge, edit, flag, and filter the data are provided, allowing for periodic updates. This tool will be invaluable to researchers, land managers, and growers wanting pollination of specific crops.

14. New phylogeny leads to improved systematics of stingless bees. Stingless bees are globally valuable as pollinators and honey producers and are also of interest for their diverse morphology and social behaviors. The group includes over 570 species and is primarily tropical to subtropical; however, at least one species has been introduced into the United States. ARS scientists in Logan, Utah, in collaboration with an international group of researchers, generated a large, genome-scale molecular dataset for the group and unraveled the group's family tree in unprecedented detail, discovering separate New- and Old-World lineages of species and finding taxonomic problems with two genera. This work provides a new framework for studying the taxonomy and biology of stingless bees and will serve as an important resource for understanding the group's role as pollinators in tropical environments.


Review Publications
Tepedino, V.J., Griswold, T.L. 2023. Reproductive biology and flower visitors of two rare pecies of Sclerocactus (Cactaceae) in the Southwestern United States. Western North American Naturalist. 83(4):445-453. https://doi.org/10.3398/064.083.0402.
Longino, J.T., Branstetter, M.G. 2024. Threats to ant diversity in Mesoamerica. In: Leon-Cortes, J.L., Cordoba-Aguilar, A., editors. Insect Decline and Conservation in the Neotropics. Cham, CH: Springer, Cham. p. 251–262. https://doi.org/10.1007/978-3-031-49255-6_12.
Sless, T.J., Branstetter, M.G., Mikat, M., Odanaka, K.A., Tobin, K.B., Rehan, S.M. 2024. Phylogenomics and biogeography of the small carpenter bees (Apidae: Xylocopinae: Ceratina). Molecular Phylogenetics and Evolution. 198. Article 108133. https://doi.org/10.1016/j.ympev.2024.108133.
De Wint, F.C., Oorts, D., Branstetter, M.G., De Graaf, D., Dekoninck, W., Jocque, M., Martin, T.E., Sudworth, J., Van Osselaer, R., Hamer, M.T. 2024. Ants in the clouds: A preliminary checklist of the ant (Hymenoptera, Formicidae) fauna of a Honduran cloud forest ecosystem, featuring a key to country genera. Neotropical Biology and Conservation. 19(2):157-185. https://doi.org/10.3897/neotropical.19.e119775.
Dorey, J.B., Fischer, E.E., Chesshire, P.R., Nava-Bolanos, A.N., O'Rielly, R.L., Bossert, S., Collins, S.M., Lichtenberg, E.M., Tucker, E.M., Smith-Pardo, A., Falcon-Brindis, A., Guevara, D.A., Ribeiro, B., De Pedro, D., Pickering, J., Hung, K.J., Parys, K.A., McCabe, L.M., Rogan, M.S., Minckley, R.L., Velzco, J.E., S., Griswold, T.L., Zarillo, T.A., Jetz, W., Sica, Y.V., Orr, M.C., Guzman, L.M., Ascher, J.S., Hughes, A.C., Cobb, N.S. 2023. A globally synthesized and flagged bee occurrence dataset and cleaning workflow. Scientific Data - Nature. 10(747):2023. https://doi.org/10.1038/s41597-023-02626-w.
Ohler, B.J., Reyes Corral, C.A., Cooper, W.R., Horton, D.R., Waters, T.D. 2023. Targeted RT-PCR based gut content analysis for potato psyllid predation in laboratory assays. American Journal of Potato Research. 100:371-381. https://doi.org/10.1007/s12230-023-09920-8.
Allen-Perkins, A., Magrach, A., Dainese, M., Garibaldi, L.A., Kleijn, D., Rader, R., Reilly, J.R., Winfree, R., Lundin, O., McGrady, C.M., Brittian, C., Biddinger, D.J., Artz, D.R., Elle, E., Hoffman, G., Ellis, J.D., Daniels, J., Gibbs, J., Campbell, J.W., et al. 2022. CropPol: A dynamic, open and global database on crop pollination. Ecology. 103(3). Article e3614. https://doi.org/10.1002/ecy.3614.