ABSTRACTLand use change threatens global biodiversity and compromises ecosystem functions, including pollination and food production. Reduced taxonomic α‐diversity is often reported under land use change, yet the impacts could be different at larger spatial scales (i.e., γ‐diversity), either due to reduced β‐diversity amplifying diversity loss or increased β‐diversity dampening diversity loss. Additionally, studies often focus on taxonomic diversity, while other important biodiversity components, including phylogenetic diversity, can exhibit differential responses. Here, we evaluated how agricultural and urban land use alters the taxonomic and phylogenetic α‐, β‐, and γ‐diversity of an important pollinator taxon—bees. Using a multicontinental dataset of 3117 bee assemblages from 157 studies, we found that taxonomic α‐diversity was reduced by 16%–18% in both agricultural and urban habitats relative to natural habitats. Phylogenetic α‐diversity was decreased by 11%–12% in agricultural and urban habitats. Compared with natural habitats, taxonomic and phylogenetic β‐diversity increased by 11% and 6% in urban habitats, respectively, but exhibited no systematic change in agricultural habitats. We detected a 22% decline in taxonomic γ‐diversity and a 17% decline in phylogenetic γ‐diversity in agricultural habitats, but γ‐diversity of urban habitats was not significantly different from natural habitats. These findings highlight the threat of agricultural expansions to large‐scale bee diversity due to systematic γ‐diversity decline. In addition, while both urbanization and agriculture lead to consistent declines in α‐diversity, their impacts on β‐ or γ‐diversity vary, highlighting the need to study the effects of land use change at multiple scales.

Pesticide use and habitat loss are major anthropogenic drivers of bee decline, raising global concerns about impaired crop pollination. However, the relative importance of these stressors and their combined impact on bee assemblages comprising species with different traits, such as body size or nesting strategy, remains unknown. Here we addressed these key knowledge gaps in a global quantitative synthesis analysing bee assemblage data from 681 crop fields across three continents. We found that both local pesticide hazards and decreasing proportions of semi-natural habitats in surrounding landscapes negatively affected wild bee abundance and species richness in crop fields, while pesticides additionally reduced functional and phylogenetic diversity. Semi-natural habitat availability did not buffer against these negative pesticide effects, nor did we identify any specific traits rending bees more vulnerable to one of the two drivers. Our findings highlight the pressing need to reduce non-target effects of pesticide use and emphasize that conservation and restoration of semi-natural habitats successfully promote wild bees, but are insufficient strategies to mitigate pesticide-driven losses of wild bee pollinators from crop fields.

Assessing the relative contributions of different pollinator taxa to pollination services is a central task in both basic eco-evolutionary research and applied conservation and agriculture. To that end, many studies have quantified single-visit pollen deposition and visitation frequency, which together determine a pollinator species' rate of conspecific pollen delivery. However, for plant species that require or benefit from outcrossing, pollination service quality further depends upon the ratio of outcross to self-pollen deposited, which is determined by two additional pollinator traits: pollen carryover and movement patterns among genetically compatible plant individuals. Here, we compare the pollination capacities of managed honey bees, native bumble bees, and native mining bees in apple-a varietally self-incompatible commercial crop-when pollen carryover and pollinator movement patterns are considered. We constructed simulation models of outcross pollen deposition parameterized using empirically measured single-visit pollen deposition, visitation frequency, and probabilities of intertree movement exhibited by each pollinator type, as well as pollen carryover patterns simulated based on parameters reported in the literature. In these models, we also explicitly specified the spatial relationships among cross-compatible trees based on field-realistic orchard layout schemes. We found that estimated pollination service delivery was considerably reduced for all pollinator types when pollen carryover and pollinator movement patterns were considered, as compared to when only single-visit pollen deposition and visitation frequency were considered. We also found that the performance of different pollinator types varied greatly across simulated orchard layout schemes and pollen carryover scenarios, including one instance where bumble and mining bees reversed their relative rankings. In all simulations, native bumble and mining bees outperformed managed honey bees in terms of both outcross pollen delivery per unit time and per flower visited, with disparities being greatest under scenarios of low pollen carryover. We demonstrate the degree to which pollination studies may reach inaccurate conclusions regarding pollination service delivery when pollen carryover and pollinator movement patterns are ignored. Our finding of the strong context dependence of pollination efficiency, even within a single plant-pollinator taxon pair, cautions that future studies in both basic and applied pollination biology should explicitly consider the ecological context in which pollination interactions take place.

Megachile rotundata (F.) is an important pollinator of alfalfa in the United States. Enhancing landscapes with wildflowers is a primary strategy for conserving pollinators and may improve the sustainability of M. rotundata. Changing cold storage temperatures from a traditionally static thermal regime (STR) to a fluctuating thermal regime (FTR) improves overwintering success and extends M. rotundata’s shelf life and pollination window. Whether floral resources enhance overwintering survival and/or interact with a thermal regime are unknown. We tested the combined effects of enhancing alfalfa fields with wildflowers and thermal regime on survival and macronutrient stores under extended cold storage (i.e., beyond one season). Megachile rotundata adults were released in alfalfa plots with and without wildflower strips. Completed nests were harvested in September and stored in STR. After a year, cells were randomly assigned to remain in STR for 6 months or in FTR for a year of extended cold storage; emergence rates were observed monthly. Macronutrient levels of emerged females were assessed. FTR improved M. rotundata survival but there was no measurable effect of wildflower strips on overwintering success or nutrient stores. Timing of nest establishment emerged as a key factor: offspring produced late in the season had lower winter survival and dry body mass. Sugars and glycogen stores increased under FTR but not STR. Trehalose levels were similar across treatments. Total lipid stores depleted faster under FTR. While wildflowers did not improve M. rotundata survival, our findings provide mechanistic insight into benefits and potential costs of FTR for this important pollinator.

Seventy five percent of the world's food crops benefit from insect pollination. Hence, there has been increased interest in how global change drivers impact this critical ecosystem service. Because standardized data on crop pollination are rarely available, we are limited in our capacity to understand the variation in pollination benefits to crop yield, as well as to anticipate changes in this service, develop predictions, and inform management actions. Here, we present CropPol, a dynamic, open, and global database on crop pollination. It contains measurements recorded from 202 crop studies, covering 3,394 field observations, 2,552 yield measurements (i.e., berry mass, number of fruits, and fruit density [kg/ha], among others), and 47,752 insect records from 48 commercial crops distributed around the globe. CropPol comprises 32 of the 87 leading global crops and commodities that are pollinator dependent. Malus domestica is the most represented crop (32 studies), followed by Brassica napus (22 studies), Vaccinium corymbosum (13 studies), and Citrullus lanatus (12 studies). The most abundant pollinator guilds recorded are honey bees (34.22% counts), bumblebees (19.19%), flies other than Syrphidae and Bombyliidae (13.18%), other wild bees (13.13%), beetles (10.97%), Syrphidae (4.87%), and Bombyliidae (0.05%). Locations comprise 34 countries distributed among Europe (76 studies), North America (60), Latin America and the Caribbean (29), Asia (20), Oceania (10), and Africa (7). Sampling spans three decades and is concentrated on 2001-2005 (21 studies), 2006-2010 (40), 2011-2015 (88), and 2016-2020 (50). This is the most comprehensive open global data set on measurements of crop flower visitors, crop pollinators and pollination to date, and we encourage researchers to add more datasets to this database in the future. This data set is released for non-commercial use only. Credits should be given to this paper (i.e., proper citation), and the products generated with this database should be shared under the same license terms (CC BY-NC-SA).

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.

Pollinators face multiple pressures and there is evidence of populations in decline. As demand for insect-pollinated crops increases, crop production is threatened by shortfalls in pollination services. Understanding the extent of current yield deficits due to pollination and identifying opportunities to protect or improve crop yield and quality through pollination management is therefore of international importance. To explore the extent of "pollination deficits," where maximum yield is not being achieved due to insufficient pollination, we used an extensive dataset on a globally important crop, apples. We quantified how these deficits vary between orchards and countries and we compared "pollinator dependence" across different apple varieties. We found evidence of pollination deficits and, in some cases, risks of overpollination were even apparent for which fruit quality could be reduced by too much pollination. In almost all regions studied we found some orchards performing significantly better than others in terms of avoiding a pollination deficit and crop yield shortfalls due to suboptimal pollination. This represents an opportunity to improve production through better pollinator and crop management. Our findings also demonstrated that pollinator dependence varies considerably between apple varieties in terms of fruit number and fruit quality. We propose that assessments of pollination service and deficits in crops can be used to quantify supply and demand for pollinators and help to target local management to address deficits although crop variety has a strong influence on the role of pollinators.

Pollinator declines coupled with increasing demand for insect pollinated crops have the potential to cause future pollinator shortages for our most nutritious and valuable crops. Ensuring adequate crop pollination may necessitate a shift in pollination management, from one that primarily relies on the managed European honeybee (Apis melliferaL.) to one that integrates alternative pollinators. While a growing body of scientific evidence supports significant contributions made by naturally occurring, native bees for crop pollination, translating research to practice requires buy-in from growers. The intention of agricultural extension is to address grower needs and concerns; however, few studies have assessed grower knowledge, perceptions and attitudes about native pollinators. Here we present findings from questionnaire-based surveys of over 600 apple growers in New York State and Pennsylvania, coupled with ecological data from bee surveys. This hybrid sociological and biological survey allows us to compare grower knowledge and perceptions to an actual pollinator census. While up to 93% of respondents highly valued importance of native bees, 20% growersdid not knowhow much native bees actually contribute to their orchard pollination. Despite the uncertainty, a majority of growers were open to relying on native bees (up to 60% in NY and 67% in PA) and to making low-cost changes to their farm's management that would benefit native pollinators (up to 68 in NY and 85% in PA). Growers consistently underestimated bee diversity, but their estimates corresponded to major bee groups identifiable by lay persons, indicating accurate local knowledge about native bees. Grower reliance on honeybees increased with farm size; because native bee abundance did not measurably decrease with farm size, renting honeybees may be motivated by risk avoidance rather than grower perception of lower native bee activity. Demonstrated effectiveness of native pollinators and clear guidelines for their management were the most important factors influencing grower decision to actively manage orchards for native bees. Our results highlight a pressing need for an active and research-based extension program to support diversification of pollination strategies in the region.

Bees play a key role in the functioning of human-modified and natural ecosystems by pollinating agricultural crops and wild plant communities. Global pollinator conservation efforts need large-scale and long-term monitoring to detect changes in species’ demographic patterns and shifts in bee community structure. The objective of this project was to test a molecular sequencing pipeline that would utilize a commonly used locus, produce accurate and precise identifications consistent with morphological identifications, and generate data that are both qualitative and quantitative. We applied this amplicon sequencing pipeline to native bee communities sampled across Conservation Reserve Program (CRP) lands and native grasslands in eastern North Dakota. We found the 28S LSU locus to be more capable of discriminating between species than the 18S SSU rRNA locus, and in some cases even resolved instances of cryptic species or morphologically ambiguous species complexes. Overall, we found the amplicon sequencing method to be a qualitatively accurate representation of the sampled bee community richness and species identity, especially when a well-curated database of known 28S LSU sequences is available. Both morphological identification and molecular sequencing revealed similar patterns in native bee community structure across CRP lands and native prairie. Additionally, a genetic algorithm approach to compute taxon-specific correction factors using a small subset of the most concordant samples demonstrated that a high level of quantitative accuracy could be possible if the specimens are fresh and processed soon after collection. Here we provide a first step to a molecular pipeline for identifying insect pollinator communities. This tool should prove useful for future national monitoring efforts as use of molecular tools becomes more affordable and as numbers of 28S LSU sequences for pollinator species increase in publicly-available databases.

Elinor M. Lichtenberg1,2*, Christina M. Kennedy3, Claire Kremen4, Péter Batáry5, Frank Berendse6, Riccardo Bommarco7, Nilsa A. Bosque-Pérez8, Luísa G. Carvalheiro9,10, William E. Snyder1, Neal M. Williams11, Rachael Winfree12, Björn Klatt5,13,14, Sandra Åström15, Faye Benjamin12, Claire Brittain11, Rebecca Chaplin-Kramer16, Yann Clough13, Heather Connelly17, Bryan Danforth17, Tim Diekötter18, Sanford D. Eigenbrode8, Johan Ekroos13, Elizabeth Elle19, Breno M. Freitas20, Yuki Fukuda21, Hannah R. Gaines-Day22, Claudio Gratton22, Andrea Holzschuh23, Rufus Isaacs24, Marco Isaia25, Shalene Jha26, Dennis Jonason27, Vincent P. Jones28, Alexandra-Maria Klein29, Jochen Krauss23, Deborah K. Letourneau30, Sarina Macfadyen31, Rachel E. Mallinger22, Emily A. Martin23, Eliana Martinez32, Jane Memmott33, Lora Morandin34, Lisa Neame35, Mark Otieno36, Mia G. Park17,37, Lukas Pfiffner38, Michael Pocock39, Carlos Ponce40, Simon G. Potts41, Katja Poveda17, Mariangie Ramos42, Jay A. Rosenheim11, Maj Rundlöf14, Hilary Sardiñas4, Manu E. Saunders43, Nicole L. Schon44, Amber R. Sciligo4, C. Sheena Sidhu45, Ingolf SteffanDewenter23, Teja Tscharntke5, Milan Veselý46, Wolfgang W. Weisser47, Julianna K. Wilson24, David W. Crowder1

The objective of this protocol is to prepare amplicon sequencing libraries for high-throughput sequencing (via Illumina MiSeq) of the 18S SSU rRNA and 28 LSU rRNA loci for molecular identification of bee communities.

Land-use change threatens global biodiversity and may reshape the tree of life by favoring some lineages over others. Whether phylogenetic diversity loss compromises ecosystem service delivery remains unknown. We address this knowledge gap using extensive genomic, community, and crop datasets to examine relationships among land use, pollinator phylogenetic structure, and crop production. Pollinator communities in highly agricultural landscapes contain 230 million fewer years of evolutionary history; this loss was strongly associated with reduced crop yield and quality. Our study links landscape-mediated changes in the phylogenetic structure of natural communities to the disruption of ecosystem services. Measuring conservation success by species counts alone may fail to protect ecosystem functions and the full diversity of life from which they are derived.

Pollinator declines coupled with increasing demand for insect pollinated crops have the potential to cause future pollinator shortages for our most nutritious and valuable crops. Ensuring adequate crop pollination may necessitate a shift in pollination management, from one that primarily relies on the managed European honeybee (Apis mellifera L.) to one that integrates alternative pollinators. While a growing body of scientific evidence supports significant contributions made by naturally occurring, native bees for crop pollination, translating research to practice requires buy-in from growers. The intention of agricultural extension is to address grower needs and concerns; however, few studies have assessed grower knowledge, perceptions and attitudes about native pollinators. Here we present findings from questionnaire-based surveys of over 600 apple growers in New York State and Pennsylvania, coupled with ecological data from bee surveys. This hybrid sociological and biological survey allows us to compare grower knowledge and perceptions to an actual pollinator census. While up to 93% of respondents highly valued importance of native bees, 20% growers did not know how much native bees actually contribute to their orchard pollination. Despite the uncertainty, a majority of growers were open to relying on native bees (up to 60% in NY and 67% in PA) and to making low-cost changes to their farm’s management that would benefit native pollinators (up to 68 in NY and 85% in PA). Growers consistently underestimated bee diversity, but their estimates corresponded to major bee groups identifiable by lay persons, indicating accurate local knowledge about native bees. Grower reliance on honeybees increased with farm size; because native bee abundance did not measurably decrease with farm size, renting honeybees may be motivated by risk avoidance rather than grower perception of lower native bee activity. Demonstrated effectiveness of native pollinators and clear guidelines for their management were the most important factors influencing grower decision to actively manage orchards for native bees. Our results highlight a pressing need for an active and research-based extension program to support diversification of pollination strategies in the region.

Agricultural intensification is a leading cause of global biodiversity loss, which can reduce the provisioning of ecosystem services in managed ecosystems. Organic farming and plant diversification are farm management schemes that may mitigate potential ecological harm by increasing species richness and boosting related ecosystem services to agroecosystems. What remains unclear is the extent to which farm management schemes affect biodiversity components other than species richness, and whether impacts differ across spatial scales and landscape contexts. Using a global metadataset, we quantified the effects of organic farming and plant diversification on abundance, local diversity (communities within fields), and regional diversity (communities across fields) of arthropod pollinators, predators, herbivores, and detritivores. Both organic farming and higher in-field plant diversity enhanced arthropod abundance, particularly for rare taxa. This resulted in increased richness but decreased evenness. While these responses were stronger at local relative to regional scales, richness and abundance increased at both scales, and richness on farms embedded in complex relative to simple landscapes. Overall, both organic farming and in-field plant diversification exerted the strongest effects on pollinators and predators, suggesting these management schemes can facilitate ecosystem service providers without augmenting herbivore (pest) populations. Our results suggest that organic farming and plant diversification promote diverse arthropod metacommunities that may provide temporal and spatial stability of ecosystem service provisioning. Conserving diverse plant and arthropod communities in farming systems therefore requires sustainable practices that operate both within fields and across landscapes.

A growing body of evidence suggests that wild bees play an important role in agricultural pollination. It is very difficult, however, to accurately quantify the contribution of wild bees relative to honeybees in most crop systems. We quantified the relative contribution of honeybees and wild bees to the pollination of an economically important, insect-pollinated crop (apple). We use an empirical dataset to identify which of three functional traits (body size, pollen load purity, and flower handling behavior) contribute significantly to seed set. We find that flower handling behavior and abundance were the only functional traits that significantly predict seed set. When we take into account flower handling behavior and abundance, wild bees contributed significantly more to seed set than honeybees in the apple orchards we surveyed. Our findings suggest that land managers may benefit from focusing on supporting communities of wild bees, rather than investing in honeybee hive rental.

Declines in honey bee health and increasing demand for pollination services highlight a need to optimize crop pollination by wild bees. Apple is an economically important crop in eastern North America, requires insect pollination, and is visited by a diverse bee fauna, but a direct assessment of wild bee pollination in apple orchards is lacking. We combined measurements of two facets of pollination service, per-visit efficiency (fruit and seed set) and relative abundance, to estimate orchard-level, pollinator importance of mining bees (Andrena subgenus Melandrena), bumble bees (Bombus), and honey bees (Apis mellifera L.). Average pollinator importance provided a relative measure that allowed comparison of pollination service among the three focal bees across the study region. On average, a wild bee visit resulted in higher pollen transfer to stigmas, but had the same probability of setting fruit and seed as a honey bee visit. Regionally, pollinator importance of Melandrena and Bombus were 32 and 14 % that of honey bees, respectively. Because per-visit performances were similar, such disparities in importance were based largely on differences in relative abundance. Although the summed pollinator importance of Melandrena and Bombus was less than that of the honey bee, these, and other, wild pollinators have a role to play in filling future pollination gaps, and thus, warrant further study and conservation.

Understanding the importance of biodiversity in applied settings is a central theme for ecologists. Pollination is an essential ecosystem service, which may rely on biodiversity for effectiveness and stability. Empirical examples which link functional outcomes of increased biodiversity to pollination services are rare. To investigate the importance of wild and managed pollinator communities to apple production, we assessed the effect of wild and managed bee abundance and diversity on pollen limitation and seed set on commercial farms in New York State. Seed set increased and pollen limitation decreased with increasing wild bee species richness, functional group diversity (based on nesting, sociality, and size traits), and abundance, but not with honey bee abundance. Functional group diversity explained more variation in apple seed set than species richness. Our findings demonstrate the important role of functional complementarity of wild bees, defined here as functional group diversity, to crop pollination even in the presence of large populations of managed honey bees. Therefore, our results suggest that management of diverse pollinator communities may decrease reliance on managed honey bees for pollination services and enhance crop yields. (C) 2016 Elsevier B.V. All rights reserved.

Bees are important pollinators of agricultural crops, and bee diversity has been shown to be closely associated with pollination, a valuable ecosystem service. Higher functional diversity and species richness of bees have been shown to lead to higher crop yield. Bees simultaneously represent a mega-diverse taxon that is extremely challenging to sample thoroughly and an important group to understand because of pollination services. We sampled bees visiting apple blossoms in 28 orchards over 6 years. We used species rarefaction analyses to test for the completeness of sampling and the relationship between species richness and sampling effort, orchard size, and percent agriculture in the surrounding landscape. We performed more than 190 h of sampling, collecting 11,219 specimens representing 104 species. Despite the sampling intensity, we captured <75% of expected species richness at more than half of the sites. For most of these, the variation in bee community composition between years was greater than among sites. Species richness was influenced by percent agriculture, orchard size, and sampling effort, but we found no factors explaining the difference between observed and expected species richness. Competition between honeybees and wild bees did not appear to be a factor, as we found no correlation between honeybee and wild bee abundance. Our study shows that the pollinator fauna of agroecosystems can be diverse and challenging to thoroughly sample. We demonstrate that there is high temporal variation in community composition and that sites vary widely in the sampling effort required to fully describe their diversity. In order to maximize pollination services provided by wild bee species, we must first accurately estimate species richness. For researchers interested in providing this estimate, we recommend multiyear studies and rarefaction analyses to quantify the gap between observed and expected species richness.

Wild bee communities provide underappreciated but critical agricultural pollination services. Given predicted global shortages in pollination services, managing agroecosystems to support thriving wild bee communities is, therefore, central to ensuring sustainable food production. Benefits of natural (including semi-natural) habitat for wild bee abundance and diversity on farms are well documented. By contrast, few studies have examined toxicity of pesticides on wild bees, let alone effects of farm-level pesticide exposure on entire bee communities. Whether beneficial natural areas could mediate effects of harmful pesticides on wild bees is also unknown. Here, we assess the effect of conventional pesticide use on the wild bee community visiting apple ( Malus domestica ) within a gradient of percentage natural area in the landscape. Wild bee community abundance and species richness decreased linearly with increasing pesticide use in orchards one year after application; however, pesticide effects on wild bees were buffered by increasing proportion of natural habitat in the surrounding landscape. A significant contribution of fungicides to observed pesticide effects suggests deleterious properties of a class of pesticides that was, until recently, considered benign to bees. Our results demonstrate extended benefits of natural areas for wild pollinators and highlight the importance of considering the landscape context when weighing up the costs of pest management on crop pollination services.

There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.