Recent and future declines of a historically widespread pollinator linked to climate, land cover, and pesticides.

The acute decline in global biodiversity includes not only the loss of rare species, but also the rapid collapse of common species across many different taxa. The loss of pollinating insects is of particular concern because of the ecological and economic values these species provide. The western bumble bee (Bombus occidentalis) was once common in western North America, but this species has become increasingly rare through much of its range. To understand potential mechanisms driving these declines, we used Bayesian occupancy models to investigate the effects of climate and land cover from 1998 to 2020, pesticide use from 2008 to 2014, and projected expected occupancy under three future scenarios. Using 14,457 surveys across 2.8 million km2 in the western United States, we found strong negative relationships between increasing temperature and drought on occupancy and identified neonicotinoids as the pesticides of greatest negative influence across our study region. The mean predicted occupancy declined by 57% from 1998 to 2020, ranging from 15 to 83% declines across 16 ecoregions. Even under the most optimistic scenario, we found continued declines in nearly half of the ecoregions by the 2050s and mean declines of 93% under the most severe scenario across all ecoregions. This assessment underscores the tenuous future of B. occidentalis and demonstrates the scale of stressors likely contributing to rapid loss of related pollinator species throughout the globe. Scaled-up, international species-monitoring schemes and improved integration of data from formal surveys and community science will substantively improve the understanding of stressors and bumble bee population trends.

Genetic and Usurpation Data Support High Incidence of Bumble Bee Nest Invasion by Socially Parasitic Bumble Bee, Bombus insularis.

Cuckoo bumble bees (Psithyrus) (Lepeletier, 1832) (Hymenoptera: Apidae) are a unique lineage of bees that depend exclusively on a host bumble bee species to provide nesting material, nutritional resources, and labor to rear offspring. In this study, we document usurpation incidence and population genetic data of Bombus insularis (Smith, 1861) (Hymenoptera: Apidae), a bumble bee species in the Psithyrus subgenus, on field-deployed B. huntii colonies in northern Utah, United States. Within 12 d of deploying B. huntii Greene, 1860 (Hymenoptera: Apidae) colonies at two field sites, 13 of the 16 colonies contained at least one established B. insularis female. Although our results demonstrate that field-deployed bumble bee colonies are highly susceptible to B. insularis usurpation, applying a fabricated excluder to prevent the inquiline from invading a colony was 100% effective. Sibship analysis using microsatellite genotype data of 59 B. insularis females estimates that they originated from at least 49 unique colonies. Furthermore, sibship analysis found siblings distributed between the field sites that were 7.04 km apart. Our result suggests that B. insularis females have the capacity to disperse across the landscape in search of host colonies at distances of at least 3.52 km and up to 7.04 km. Our study underscores the detrimental impact B. insularis usurpation has on the host bumble bee colony. As B. insularis significantly impacts the success of bumble bee colonies, we briefly discuss how the utilization of excluders may be useful for commercial bumble bee colonies that are used to pollinate open field crops.

Osmia lignaria (Hymenoptera: Megachilidae) increase pollination of Washington sweet cherry and pear crops.

Apis mellifera Linnaeus (Hymenoptera: Apis), honey bees, are the most widely used managed crop pollinators. However, their high rental cost and uncertain availability for North American orchard crops have motivated growers to explore alternative pollination options. We examined whether adding solitary, spring-flying Osmia lignaria Say (Hymenoptera: Megachilidae), blue orchard bees, as co-pollinators with A. mellifera in Washington sweet cherry and pear orchards enhances fruit set and yield compared to the use of A. mellifera alone. We added managed O. lignaria to orchard sites where A. mellifera hives were already present. Fruit set, fruit yield, and O. lignaria reproduction at O. lignaria-supplemented sites were compared to nearby, paired sites pollinated only by A. mellifera (3 paired cherry and 3 paired pear sites). For both crops, the addition of O. lignaria significantly increased fruit set but did not yield at harvest. Microscopic inspection of pollen grains from O. lignaria nest cell provisions confirmed that O. lignaria primarily visited orchard flowers. Mean retention of O. lignaria in cherry orchards was slightly higher (65%) than O. lignaria retention reported in other orchard crops (30%-60%). However, retention in pear orchards was much lower (≤20%). These results show that supplementing hives with O. lignaria in Washington spring orchard crops can increase overall pollination, but that trees fail to bear developing fruit to maturity. The strategy of using co-pollinators, O. lignaria and A. mellifera, in US orchards may act as "pollination insurance" when A. mellifera hives are in low supply or when the weather is not amenable for A. mellifera flight during the bloom period.

Forest habitats and plant communities strongly predicts Megachilidae bee biodiversity.

Megachilidae is one of the United States' most diverse bee families, with 667 described species in 19 genera. Unlike other bee families, which are primarily ground nesters, most megachilid bees require biotic cavities for nesting (i.e., wood, pithy stems, etc.). For this group, the availability of woody-plant species may be as important as nectar/pollen resources in maintaining populations. We studied Megachilidae biodiversity in the continental United States. We confirmed that the highest species richness of Megachilidae was in the southwestern United States. We examined the relationship between species richness and climate, land cover, tree species richness, and flowering plant diversity. When examining environmental predictors across the conterminous United States, we found that forested habitats, but not tree diversity, strongly predicted Megachilidae richness. Additionally, Megachilidae richness was highest in areas with high temperature and low precipitation, however this was not linearly correlated and strongly positively correlated with flowering plant diversity. Our research suggests that the availability of nesting substrate (forested habitats), and not only flowering plants, is particularly important for these cavity-nesting species. Since trees and forested areas are particularly susceptible to climate change, including effects of drought, fire, and infestations, nesting substrates could become a potential limiting resource for Megachilidae populations.

Examination of Hivetop Incubator Efficacy for Emerging Osmia lignaria (Hymenoptera: Megachilidae) and the Impact on Apis mellifera (Hymenoptera: Apidae) Colonies.

Osmia lignaria Say is used in combination with Apis mellifera L. to pollinate U.S. orchard crops. The deployment of O. lignaria requires artificial warming to synchronize adult bee emergence with crop bloom. However, current methods for emerging bees are time consuming and inefficient; the Hivetop Incubator (HTI) invention creates a space atop an A. mellifera hive whose heat flows through the screened bottom of the HTI to incubate cocooned O. lignaria adults therein. In response to HTI heat, O. lignaria adults chew out of cocoons, find an exit hole, and fly away to nest in provided nesting sites and, thereby, pollinate a crop. Objectives for studies performed in Utah and Washington were to: 1) determine whether HTIs inhibit A. mellifera thermoregulation or colony growth, 2) compare O. lignaria emergence duration from an HTI with and without hive heat, and 3) assess whether O. lignaria females leave HTIs located at the orchard edge to nest throughout the orchard. We found no significant differences between the internal temperatures of A. mellifera colonies with and without HTIs and no impact on A. mellifera food storage or brood production. Osmia lignaria in hive-heated HTIs emerged 3× faster than bees in unheated HTIs. Heated HTIs were significantly cooler than hive temperatures but significantly warmer than HTIs atop empty hive boxes. Osmia lignaria nest distribution was not correlated to the location of HTIs at the orchard edge. Overall, HTIs were effective for timely, on-site emergence of O. lignaria for orchard pollination without negatively impacting A. mellifera colonies.

Blue orchard bee (Hymenoptera: Megachilidae) origin and orchard growing region affect female retention at artificial nest sites in cherry orchards.

The blue orchard bee, Osmia lignaria Say (Hymenoptera: Megachilidae), is a solitary, cavity-nesting species used for pollinating spring blooming crops. Commercial stocks are sourced from a few locations in the western United States but are sold across the country. However, the existence of local adaptations of these bees is unknown, such as the propensity to nest in nearby provided materials or to disperse broadly beyond release sites. In spring 2019, California- and Utah-sourced blue orchard bees were introduced into cherry orchards in both source and reciprocal states. Nest boxes were placed near (within 78 m) and far (500 m-1 km) from central bee release points. Paint-marked bees were released when floral resources were available. Observations of marked bees at nest boxes were used to evaluate female retention and dispersal pattern. Nesting bee counts in March-blooming California orchards revealed a significant difference in female retention by population source; over twice as many UT bees established nests than did CA bees. Few females were found at far nest sites. In May-blooming Utah orchards, counts of CA and UT bees were similar at near and far nest sites; neither female retention nor dispersal was significantly affected by bee origin. It is concerning that CA females were less likely to be retained in California orchards because the demand for commercial pollination is high for early-blooming California almond and cherry. Our results highlight the need to understand potential consequences of bee origin and their management on pollinator performance and reproduction in target crops.

A globally synthesised and flagged bee occurrence dataset and cleaning workflow.

Species occurrence data are foundational for research, conservation, and science communication, but the limited availability and accessibility of reliable data represents a major obstacle, particularly for insects, which face mounting pressures. We present BeeBDC, a new R package, and a global bee occurrence dataset to address this issue. We combined >18.3 million bee occurrence records from multiple public repositories (GBIF, SCAN, iDigBio, USGS, ALA) and smaller datasets, then standardised, flagged, deduplicated, and cleaned the data using the reproducible BeeBDC R-workflow. Specifically, we harmonised species names (following established global taxonomy), country names, and collection dates and, we added record-level flags for a series of potential quality issues. These data are provided in two formats, "cleaned" and "flagged-but-uncleaned". The BeeBDC package with online documentation provides end users the ability to modify filtering parameters to address their research questions. By publishing reproducible R workflows and globally cleaned datasets, we can increase the accessibility and reliability of downstream analyses. This workflow can be implemented for other taxa to support research and conservation.

Decreased bee emergence along an elevation gradient: Implications for climate change revealed by a transplant experiment.

Bees experience differences in thermal tolerance based on their geographical range; however, there are virtually no studies that examine how overwintering temperatures may influence immature survival rates. Here, we conducted a transplant experiment along an elevation gradient to test for climate-change effects on immature overwinter survival using movement along elevational gradient for a community of 26 cavity-nesting bee species in the family Megachilidae along the San Francisco Peaks, Arizona elevational gradient. In each of three years, we placed nest blocks at three elevations, to be colonized by native Megachilidae. Colonized blocks were then (1) moved to lower (warmer) elevations; (2) moved to higher (cooler) elevations; or (3) left in their natal habitat (no change in temperature). Because Megachilidae occupy high elevations with colder temperatures more than any other family of bees, we predicted that emergence would decrease in nest blocks moved to lower elevations, but that we would find no differences in emergence when nest blocks were moved to higher elevations. We found three major results: (1) Bee species moved to lower (warmer) habitats exhibited a 30% decrease in emergence compared with species moved within their natal habitat. (2) Habitat generalists were more likely than habitat specialists to emerge when moved up or down in elevation regardless of their natal life zones. (3) At our highest elevation treatment, emergence increased when blocks were moved to higher elevations, indicating that at least some Megachilidae species can survive at colder temperatures. Our results suggest that direct effects of warming temperatures will have negative impacts on the overall survival of Megachilidae. Additionally, above the tree line, low availability of wood-nesting resources is a probable limiting factor on bees moving up in elevation.

Variation in Plant-Pollinator Network Structure along the Elevational Gradient of the San Francisco Peaks, Arizona.

The structural patterns comprising bimodal pollination networks can help characterize plant-pollinator systems and the interactions that influence species distribution and diversity over time and space. We compare network organization of three plant-pollinator communities along the altitudinal gradient of the San Francisco Peaks in northern Arizona. We found that pollination networks become more nested, as well as exhibit lower overall network specialization, with increasing elevation. Greater weight of generalist pollinators at higher elevations of the San Francisco Peaks may result in plant-pollinator communities less vulnerable to future species loss due to changing climate or shifts in species distribution. We uncover the critical, more generalized pollinator species likely responsible for higher nestedness and stability at the higher elevation environment. The generalist species most important for network stability may be of the greatest interest for conservation efforts; preservation of the most important links in plant-pollinator networks may help secure the more specialized pollinators and maintain species redundancy in the face of ecological change, such as changing climate.

Adult body size measurement redundancies in Osmia lignaria and Megachile rotundata (Hymenoptera: Megachilidae).

Metrics to assess relative adult bee body size have included both mass and morphometrics, but these metrics may not equally or reliably estimate body size for all bee species and in all situations, due to bee age, diet, and/or environment. Understanding the relationships between different metrics and possible redundancies in the information they afford is important but not always known. Body size measurements provide valuable data for interpreting research outcomes for managed solitary bees, including Osmia lignaria Say and Megachile rotundata F. (Hymenoptera: Megachilidae). Applied studies of these important and readily available U.S. crop pollinators focus on refining commercial management practices, and basic empirical studies in various scientific disciplines (from genomics to ecology) employ them as model systems to study solitary bees. To examine common metrics of body size, we measured head capsule width (HCW), intertegular distance (ITD), and fresh and dry weights of newly emerged adults of both species. Using linear and exponential models, we determined relationships between these body size metrics. For M. rotundata, linear models best described relationships between ITD and all other metrics, and between HCW and fresh and dry weights. For O. lignaria, linear models best fit relationships between all metrics except for fresh weight with both ITD and HCW, which were fitted better with exponential models. For both species, model fits were strongest when males and females were pooled. Depending on the study question, knowing that only one metric may reliably measure body size can simplify evaluations of O. lignaria and M. rotundata responses to artificial or environmental variables.

Bee species checklist of the San Francisco Peaks, Arizona.

BACKGROUND: Here we present a checklist of the bee species found on the C. Hart Merriam elevation gradient along the San Francisco Peaks in northern Arizona. Elevational gradients can serve as natural proxies for climate change, replacing time with space as they span multiple vegetation zones over a short geographic distance. Describing the distribution of bee species along this elevation gradient will help predict how bee communities might respond to changing climate. To address this, we initiated an inventory associated with ecological studies on pollinators that documented bees on the San Francisco Peaks. Sample sites spanned six life zones (vegetation zones) on the San Francisco Peaks from 2009 to 2019. We also include occurrence data from other studies, gathered by querying the Symbiota Collection of Arthropods Network (SCAN) portal covering the San Francisco Peaks region (hereafter referred to as "the Peaks"). NEW INFORMATION: Our checklist reports 359 bee species and morphospecies spanning five families and 46 genera that have been collected in the Peaks region. Prior to our concerted sampling effort there were records for 155 bee species, yet there has not been a complete list of bee species inhabiting the Peaks published to date. Over a 10-year period, we documented an additional 204 bee species inhabiting the Peaks. Our study documents range expansions to northern Arizona for 15 species. The majority of these are range expansions from either southern Arizona, southern Utah, or the Rocky Mountain region of Colorado. Nine species are new records for Arizona, four of which are the southernmost record for that species. An additional 15 species are likely undescribed.

Environmental filtering of body size and darker coloration in pollinator communities indicate thermal restrictions on bees, but not flies, at high elevations.

BACKGROUND: Bees and flies are the two most dominant pollinator taxa in mountain environments of the Southwest USA. Communities of both taxa change dramatically along elevation gradients. We examined whether bee and fly traits would also change along elevation gradients and if so, do they change in a predictable way related to a decrease in temperature as elevation increases. METHODS: We used insect body size and darkness traits as proxies for energetic requirements and indicators of cold tolerance in order to assess patterns of bee and fly community trait differences along an elevation gradient. We examined 1,922 individuals of bees and flies sampled along an elevation gradient ranging from 2,400 meters to 3,200 meters and from 9.6 °C to 5.2 °C mean annual temperature. We examined bees and flies separately using community weighted means (site-level trait values weighted by species abundance) and estimates of environmental filtering (quantified as the inverse of the standardized range of trait values). RESULTS: Bees and flies exhibited two somewhat distinct patterns; (1) Community weighted mean body volume and darkness of bees increased sharply at the highest elevation, and the intensity of environmental filtering also increased with elevation. This was due to both a change among bee populations within a species as well as species replacement at the highest elevation. (2) Community weighted mean body volume and darkness of flies also increased moderately with increasing elevation, but did not exhibit patterns of significant environmental filtering. In fact, the intensity of environmental filtering as indicated by the range of fly body volume weakened with elevation. CONCLUSION: The increase in filter intensity at high elevations exhibited by bees suggests a significant limitation on the breadth of viable functional strategies for coping with extreme cold, at least within this regional species pool. Flies, on the other hand, do not appear to be limited by high elevations, indicating that the shift from bee to fly dominance at high elevations may be due, at least in part, to greater environmental constraints on bee adaptation to colder environments.

The transition from bee-to-fly dominated communities with increasing elevation and greater forest canopy cover.

Insect pollinator communities are thought to transition from bee-dominated communities at low elevations to fly-dominated communities at high elevations. We predicted that increased tree canopy cover and a subsequent decrease in meadows and flowering plants would limit bees but not flies at higher elevations. We tested and supported this prediction by examining changes in both abundance and species richness for 128 bee species and 96 fly species at key points along an elevational gradient in Northern Arizona represented by distinct vegetation life zones. In addition to an increase in fly species and abundance relative to bees with increasing elevation, there were changes in community structure). To better understand factors that might influence this transition we examined how tree canopy cover changed along the elevational gradient and how this influenced the change in insect pollinator communities. While bee communities were progressively divergent between forest and meadow habitats with increasing elevation and tree canopy cover, there was no significant pattern with flies between meadow and forest habitats. However, fly abundance did increase with increasing elevation relative to bees. Along a comparable elevational gradient on an adjacent mountain with no tree canopy cover (i.e., a fire burned mountain), the bee-to-fly transition did not occur; bees persisted as the dominant pollinator into the highest life zone. This suggests that tree canopy cover can in part explain the transition from bee-to fly-dominated communities. In conclusion, this is the first study in North America to document a bee-fly transition for both abundance and species richness and show that tree canopy cover may play a role in determining pollinator community composition, by restricting bees to open meadow habitats.

Assessment of North American arthropod collections: prospects and challenges for addressing biodiversity research.

Over 300 million arthropod specimens are housed in North American natural history collections. These collections represent a "vast hidden treasure trove" of biodiversity -95% of the specimen label data have yet to be transcribed for research, and less than 2% of the specimens have been imaged. Specimen labels contain crucial information to determine species distributions over time and are essential for understanding patterns of ecology and evolution, which will help assess the growing biodiversity crisis driven by global change impacts. Specimen images offer indispensable insight and data for analyses of traits, and ecological and phylogenetic patterns of biodiversity. Here, we review North American arthropod collections using two key metrics, specimen holdings and digitization efforts, to assess the potential for collections to provide needed biodiversity data. We include data from 223 arthropod collections in North America, with an emphasis on the United States. Our specific findings are as follows: (1) The majority of North American natural history collections (88%) and specimens (89%) are located in the United States. Canada has comparable holdings to the United States relative to its estimated biodiversity. Mexico has made the furthest progress in terms of digitization, but its specimen holdings should be increased to reflect the estimated higher Mexican arthropod diversity. The proportion of North American collections that has been digitized, and the number of digital records available per species, are both much lower for arthropods when compared to chordates and plants. (2) The National Science Foundation's decade-long ADBC program (Advancing Digitization of Biological Collections) has been transformational in promoting arthropod digitization. However, even if this program became permanent, at current rates, by the year 2050 only 38% of the existing arthropod specimens would be digitized, and less than 1% would have associated digital images. (3) The number of specimens in collections has increased by approximately 1% per year over the past 30 years. We propose that this rate of increase is insufficient to provide enough data to address biodiversity research needs, and that arthropod collections should aim to triple their rate of new specimen acquisition. (4) The collections we surveyed in the United States vary broadly in a number of indicators. Collectively, there is depth and breadth, with smaller collections providing regional depth and larger collections providing greater global coverage. (5) Increased coordination across museums is needed for digitization efforts to target taxa for research and conservation goals and address long-term data needs. Two key recommendations emerge: collections should significantly increase both their specimen holdings and their digitization efforts to empower continental and global biodiversity data pipelines, and stimulate downstream research.

LepNet: The Lepidoptera of North America Network.

The Lepidoptera of North America Network, or LepNet, is a digitization effort recently launched to mobilize biodiversity data from 3 million specimens of butterflies and moths in United States natural history collections (http://www.lep-net.org/). LepNet was initially conceived as a North American effort but the project seeks collaborations with museums and other organizations worldwide. The overall goal is to transform Lepidoptera specimen data into readily available digital formats to foster global research in taxonomy, ecology and evolutionary biology.