A checklist of the bees (Hymenoptera: Apoidea) of Minnesota.

Research studies and conservation actions aimed at improving conditions for bees require a basic understanding of which species are present in a given region. The US state of Minnesota occupies a unique geographic position at the confluence of eastern deciduous forests, northern boreal forests, and western tallgrass prairie, which has led to a diverse and unique bee fauna. In recent years there have been multiple ongoing bee-focused inventory and research projects in Minnesota. Combined with the historic specimens housed in the University of Minnesota Insect Collection and other regional collections, these furnished a wealth of specimens available to form the basis of a statewide checklist. Here, we present the first comprehensive checklist of Minnesota bee species, documenting a total of 508 species in 45 genera. County-level occurrence data is included for each species, and further information on distribution and rarity is included for species of regional or national interest. Some species have their taxonomy clarified, with Perdita citrinella Graenicher, 1910 syn. nov. recognized as a junior synonym of Perdita perpallida Cockerell, 1901, P. bequaerti syn. nov. recognized as a junior synonym of P. pallidipennis Graenicher, 1910 stat. nov., Anthidiellum boreale (Robertson, 1902) stat. nov. recognized as a full species, and Anthidiellium beijingense Portman & Ascher nom. nov. is proposed for A. boreale Wu to resolve the homonymy with A. boreale (Robertson). We further include a list of species that may occur in Minnesota and highlight 11 species occurring in the state that are considered non-native. Recent collecting efforts, as well as increased taxonomic attention paid to Minnesota bees, have resulted in 66 species that have only been documented in the last 10 years. As a first step in determining native bees of conservation concern, we document 38 species that have not been detected in the state during the last 50 years and discuss their conservation status, along with other species for which evidence of decline exists. The checklist of Minnesota bees will continue to grow and change with additional surveys and research studies. In particular, recent surveys have continued to detect new bee species, and many bee groups are in need of taxonomic revision, with the most recent revisions for many genera occurring decades ago. Overall, this checklist strengthens our understanding of the bees of Minnesota and the broader region, informs conservation assessments, and establishes a baseline for faunal change.

The potential and realized foraging movements of bees are differentially determined by body size and sociality.

Reversing biodiversity declines requires a better understanding of organismal mobility, as movement processes dictate the scale at which species interact with the environment. Previous studies have demonstrated that species foraging ranges, and therefore, habitat use increases with body size. Yet, foraging ranges are also affected by other life-history traits, such as sociality, which influence the need of and ability to detect resources. We evaluated the effect of body size and sociality on potential and realized foraging ranges using a compiled dataset of 383 measurements for 81 bee species. Potential ranges were larger than realized ranges and increased more steeply with body size. Highly eusocial species had larger realized foraging ranges than primitively eusocial or solitary taxa. We contend that potential ranges describe species movement capabilities, whereas realized ranges depict how foraging movements result from interactions between species traits and environmental conditions. Furthermore, the complex communication strategies and large colony sizes in highly eusocial species may facilitate foraging over wider areas in response to resource depletion. Our findings should contribute to a greater understanding of landscape ecology and conservation, as traits that influence movement mediate species vulnerability to habitat loss and fragmentation.

A review of the Augochloropsis (Hymenoptera, Halictidae) and keys to the shiny green Halictinae of the midwestern United States.

Augochloropsis and other shiny green Halictinae have had various taxonomic issues and are often misidentified. One prevailing taxonomic issue is that Augochloropsismetallica (Fabricius) has two subspecies, that have long been recognized as morphologically distinct (Augochloropsismetallicametallica and Augochloropsismetallicafulgida (Smith), but the subspecies are inconsistently applied in the literature. Here, we review the Augochloropsis of the Midwest and further address the Augochloropsis species in the broader United States to resolve the outstanding taxonomic issues with the midwestern species. We provide identification keys and diagnoses for the genera and species of the shiny green Halictinae of the midwestern United States, which includes the genera Agapostemon, Augochlora, Augochlorella, and Augochloropsis. This work results in taxonomic changes to Augochloropsis. Augochloropsissumptuosa (Smith) is split into two species, with the name Augochloropsissumptuosa retained for the eastern form, and Augochloropsishumeralis (Patton), stat. nov., reinstated for the western form. Augochloropsismetallica is split into five species, with two of those species occurring in the midwestern United States: Augochloropsismetallica and Augochloropsisviridula (Smith), stat. nov. Examination of the holotype of Augochloropsisfulgida (Smith) revealed that it does not agree with the prevailing concept of Augochloropsismetallicafulgida; it is reinstated as Augochloropsisfulgida, stat. nov., but is currently known only from the holotype female from Florida. Augochloropsiscuprea (Smith), long considered to be a synonym of Augochloropsismetallica, is also distinct, and we are reinstating Augochloropsiscuprea, stat. nov., though the range of this species is unclear. We further recognize Augochloropsisfulvofimbriata (Friese), stat. nov., from South and Central America, as distinct. These changes result in a total of three Augochloropsis species in the Midwest and seven named species in the United States. We are aware of additional species from the southern and southwestern United States that are undescribed, and we highlight additional taxonomic work that remains to be done.

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.

A review of the challenges and opportunities for restoring animal-mediated pollination of native plants.

Ecological restoration is increasingly implemented to reverse habitat loss and concomitant declines in biological diversity. Typically, restoration success is evaluated by measuring the abundance and/or diversity of a single taxon. However, for a restoration to be successful and persistent, critical ecosystem functions such as animal-mediated pollination must be maintained. In this review, we focus on three aspects of pollination within ecological restorations. First, we address the need to measure pollination directly in restored habitats. Proxies such as pollinator abundance and richness do not always accurately assess pollination function. Pollen supplementation experiments, pollen deposition studies, and pollen transport networks are more robust methods for assessing pollination function within restorations. Second, we highlight how local-scale management and landscape-level factors may influence pollination within restorations. Local-scale management actions such as prescribed fire and removal of non-native species can have large impacts on pollinator communities and ultimately on pollination services. In addition, landscape context including proximity and connectivity to natural habitats may be an important factor for land managers and conservation practitioners to consider to maximize restoration success. Third, as climate change is predicted to be a primary driver of future loss in biodiversity, we discuss the potential effects climate change may have on animal-mediated pollination within restorations. An increased mechanistic understanding of how climate change affects pollination and incorporation of climate change predictions will help practitioners design stable, functioning restorations into the future.

Pollinator size and its consequences: Robust estimates of body size in pollinating insects.

Body size is an integral functional trait that underlies pollination-related ecological processes, yet it is often impractical to measure directly. Allometric scaling laws have been used to overcome this problem. However, most existing models rely upon small sample sizes, geographically restricted sampling and have limited applicability for non-bee taxa. Allometric models that consider biogeography, phylogenetic relatedness, and intraspecific variation are urgently required to ensure greater accuracy. We measured body size as dry weight and intertegular distance (ITD) of 391 bee species (4,035 specimens) and 103 hoverfly species (399 specimens) across four biogeographic regions: Australia, Europe, North America, and South America. We updated existing models within a Bayesian mixed-model framework to test the power of ITD to predict interspecific variation in pollinator dry weight in interaction with different co-variates: phylogeny or taxonomy, sexual dimorphism, and biogeographic region. In addition, we used ordinary least squares regression to assess intraspecific dry weight ~ ITD relationships for ten bees and five hoverfly species. Including co-variates led to more robust interspecific body size predictions for both bees and hoverflies relative to models with the ITD alone. In contrast, at the intraspecific level, our results demonstrate that the ITD is an inconsistent predictor of body size for bees and hoverflies. The use of allometric scaling laws to estimate body size is more suitable for interspecific comparative analyses than assessing intraspecific variation. Collectively, these models form the basis of the dynamic R package, "pollimetry," which provides a comprehensive resource for allometric pollination research worldwide.

Correction: The Allometry of Bee Proboscis Length and Its Uses in Ecology.

[This corrects the article DOI: 10.1371/journal.pone.0151482.].

Species turnover promotes the importance of bee diversity for crop pollination at regional scales.

Ecologists have shown through hundreds of experiments that ecological communities with more species produce higher levels of essential ecosystem functions such as biomass production, nutrient cycling, and pollination, but whether this finding holds in nature (that is, in large-scale and unmanipulated systems) is controversial. This knowledge gap is troubling because ecosystem services have been widely adopted as a justification for global biodiversity conservation. Here we show that, to provide crop pollination in natural systems, the number of bee species must increase by at least one order of magnitude compared with that in field experiments. This increase is driven by species turnover and its interaction with functional dominance, mechanisms that emerge only at large scales. Our results show that maintaining ecosystem services in nature requires many species, including relatively rare ones.

The Allometry of Bee Proboscis Length and Its Uses in Ecology.

Allometric relationships among morphological traits underlie important patterns in ecology. These relationships are often phylogenetically shared; thus quantifying allometric relationships may allow for estimating difficult-to-measure traits across species. One such trait, proboscis length in bees, is assumed to be important in structuring bee communities and plant-pollinator networks. However, it is difficult to measure and thus rarely included in ecological analyses. We measured intertegular distance (as a measure of body size) and proboscis length (glossa and prementum, both individually and combined) of 786 individual bees of 100 species across 5 of the 7 extant bee families (Hymenoptera: Apoidea: Anthophila). Using linear models and model selection, we determined which parameters provided the best estimate of proboscis length. We then used coefficients to estimate the relationship between intertegular distance and proboscis length, while also considering family. Using allometric equations with an estimation for a scaling coefficient between intertegular distance and proboscis length and coefficients for each family, we explain 91% of the variance in species-level means for bee proboscis length among bee species. However, within species, individual-level intertegular distance was a poor predictor of individual proboscis length. To make our findings easy to use, we created an R package that allows estimation of proboscis length for individual bee species by inputting only family and intertegular distance. The R package also calculates foraging distance and body mass based on previously published equations. Thus by considering both taxonomy and intertegular distance we enable accurate estimation of an ecologically and evolutionarily important trait.

Delivery of crop pollination services is an insufficient argument for wild pollinator conservation.

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.

Abundance of common species, not species richness, drives delivery of a real-world ecosystem service.

Biodiversity-ecosystem functioning experiments have established that species richness and composition are both important determinants of ecosystem function in an experimental context. Determining whether this result holds for real-world ecosystem services has remained elusive, however, largely due to the lack of analytical methods appropriate for large-scale, associational data. Here, we use a novel analytical approach, the Price equation, to partition the contribution to ecosystem services made by species richness, composition and abundance in four large-scale data sets on crop pollination by native bees. We found that abundance fluctuations of dominant species drove ecosystem service delivery, whereas richness changes were relatively unimportant because they primarily involved rare species that contributed little to function. Thus, the mechanism behind our results was the skewed species-abundance distribution. Our finding that a few common species, not species richness, drive ecosystem service delivery could have broad generality given the ubiquity of skewed species-abundance distributions in nature.

Causes of variation in wild bee responses to anthropogenic drivers.

Anthropogenic change can have large impacts on wild bees and the pollination services they provide. However, the overall pattern of wild bee response to drivers such as land-use change, pesticides, pathogens, and climate change has been one of variability in both the magnitude and directionality of responses. We argue that two causes contribute to this variation. First, different species exhibit differential responses to the same anthropogenic drivers. Second, these anthropogenic drivers vary in type and magnitude that will drive variation in bee responses. For this second issue, we focus on land-use change, the most well-studied driver. We conclude by discussing how understanding species-level responses and the magnitude of land-use change can make bee conservation more effective.

Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus).

Bacterial gut symbiont communities are critical for the health of many insect species. However, little is known about how microbial communities vary among host species or how they respond to anthropogenic disturbances. Bacterial communities that differ in richness or composition may vary in their ability to provide nutrients or defenses. We used deep sequencing to investigate gut microbiota of three species in the genus Bombus (bumble bees). Bombus are among the most economically and ecologically important non-managed pollinators. Some species have experienced dramatic declines, probably due to pathogens and land-use change. We examined variation within and across bee species and between semi-natural and conventional agricultural habitats. We categorized as 'core bacteria' any operational taxonomic units (OTUs) with closest hits to sequences previously found exclusively or primarily in the guts of honey bees and bumble bees (genera Apis and Bombus). Microbial community composition differed among bee species. Richness, defined as number of bacterial OTUs, was highest for B. bimaculatus and B. impatiens. For B. bimaculatus, this was due to high richness of non-core bacteria. We found little effect of habitat on microbial communities. Richness of non-core bacteria was negatively associated with bacterial abundance in individual bees, possibly due to deeper sampling of non-core bacteria in bees with low populations of core bacteria. Infection by the gut parasite Crithidia was negatively associated with abundance of the core bacterium Gilliamella and positively associated with richness of non-core bacteria. Our results indicate that Bombus species have distinctive gut communities, and community-level variation is associated with pathogen infection.

Response diversity to land use occurs but does not consistently stabilise ecosystem services provided by native pollinators.

More diverse biological communities may provide ecosystem services that are less variable over space or time. However, the mechanisms underlying this relationship are rarely investigated empirically in real-world ecosystems. Here, we investigate how a potentially important stabilising mechanism, response diversity, the differential response to environmental change among species, stabilises pollination services against land-use change. We measured crop pollination services provided by native bees across land-use gradients in three crop systems. We found that bee species responded differentially to increasing agricultural land cover in all three systems, demonstrating that response diversity occurs. Similarly, we found response diversity in pollination services in two of the systems. However, there was no evidence that response diversity, in general, stabilised ecosystem services. Our results suggest that either response diversity is not the primary stabilising mechanism in our system, or that new measures of response diversity are needed that better capture the stabilising effects it provides.

A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems.

Bees provide essential pollination services that are potentially affected both by local farm management and the surrounding landscape. To better understand these different factors, we modelled the relative effects of landscape composition (nesting and floral resources within foraging distances), landscape configuration (patch shape, interpatch connectivity and habitat aggregation) and farm management (organic vs. conventional and local-scale field diversity), and their interactions, on wild bee abundance and richness for 39 crop systems globally. Bee abundance and richness were higher in diversified and organic fields and in landscapes comprising more high-quality habitats; bee richness on conventional fields with low diversity benefited most from high-quality surrounding land cover. Landscape configuration effects were weak. Bee responses varied slightly by biome. Our synthesis reveals that pollinator persistence will depend on both the maintenance of high-quality habitats around farms and on local management practices that may offset impacts of intensive monoculture agriculture.

Wild pollinators enhance fruit set of crops regardless of honey bee abundance.

The diversity and abundance of wild insect pollinators have declined in many agricultural landscapes. Whether such declines reduce crop yields, or are mitigated by managed pollinators such as honey bees, is unclear. We found universally positive associations of fruit set with flower visitation by wild insects in 41 crop systems worldwide. In contrast, fruit set increased significantly with flower visitation by honey bees in only 14% of the systems surveyed. Overall, wild insects pollinated crops more effectively; an increase in wild insect visitation enhanced fruit set by twice as much as an equivalent increase in honey bee visitation. Visitation by wild insects and honey bees promoted fruit set independently, so pollination by managed honey bees supplemented, rather than substituted for, pollination by wild insects. Our results suggest that new practices for integrated management of both honey bees and diverse wild insect assemblages will enhance global crop yields.