Range-wide genetic analysis of an endangered bumble bee (Bombus affinis, Hymenoptera: Apidae) reveals population structure, isolation by distance, and low colony abundance.

Declines in bumble bee species range and abundances are documented across multiple continents and have prompted the need for research to aid species recovery and conservation. The rusty patched bumble bee (Bombus affinis) is the first federally listed bumble bee species in North America. We conducted a range-wide population genetics study of B. affinis from across all extant conservation units to inform conservation efforts. To understand the species' vulnerability and help establish recovery targets, we examined population structure, patterns of genetic diversity, and population differentiation. Additionally, we conducted a site-level analysis of colony abundance to inform prioritizing areas for conservation, translocation, and other recovery actions. We find substantial evidence of population structuring along an east-to-west gradient. Putative populations show evidence of isolation by distance, high inbreeding coefficients, and a range-wide male diploidy rate of ~15%. Our results suggest the Appalachians represent a genetically distinct cluster with high levels of private alleles and substantial differentiation from the rest of the extant range. Site-level analyses suggest low colony abundance estimates for B. affinis compared to similar datasets of stable, co-occurring species. These results lend genetic support to trends from observational studies, suggesting that B. affinis has undergone a recent decline and exhibit substantial spatial structure. The low colony abundances observed here suggest caution in overinterpreting the stability of populations even where B. affinis is reliably detected interannually. These results help delineate informed management units, provide context for the potential risks of translocation programs, and help set clear recovery targets for this and other threatened bumble bee species.

Variation in North American bumble bee nest success and colony sizes under captive rearing conditions.

Of the 265 known bumble bee (Bombus) species, knowledge of colony lifecycle is derived from relatively few species. As interest in Bombus commercialization and conservation grows, it is becoming increasingly important to understand colony growth dynamics across a variety of species since variation exists in nest success, colony growth, and reproductive output. In this study, we reported successful nest initiation and establishment rates of colonies and generated a timeline of colony development for 15 western North American Bombus species, which were captively reared from wild-caught gynes from 2009 to 2019. Additionally, we assessed variation in colony size among 5 western North American Bombus species from 2015 to 2018. Nest initiation and establishment rates varied greatly among species, ranging from 5-76.1% and 0-54.6%, respectively. Bombus griseocollis had the highest rates of nest success across the 11-yr period, followed by B. occidentalis, B. vosnesenskii, and B. huntii. Furthermore, days to nest initiation and days to nest establishment varied among species, ranging from 8.4 to 27.7 days and 32.7 to 47 days. Colony size also differed significantly among species with B. huntii and B. vosnesenskii producing more worker/drone cells than B. griseocollis, B. occidentalis, and B. vancouverensis. Additionally, gyne production differed significantly among species with B. huntii colonies producing more gynes than B. vosnesenskii. Results from this study increase knowledge of systematic nesting biology for numerous western North American Bombus species under captive rearing conditions, which can further improve rearing techniques available to conservationists and researchers.

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.

Captive Rearing Success and Critical Thermal Maxima of Bombus griseocollis (Hymenoptera: Apidae): A Candidate for Commercialization?

Commercialized bumble bees (Bombus) are primary pollinators of several crops within open field and greenhouse settings. However, the common eastern bumble bee (Bombus impatiens Cresson, 1863) is the only species widely available for purchase in North America. As an eastern species, concerns have been expressed over their transportation outside of their native range. Therefore, there is a need to identify regionally appropriate candidates for commercial crop pollination services, especially in the western U.S.A. In this study, we evaluated the commercialization potential of brown-belted bumble bees (Bombus griseocollis De Geer, 1773), a broadly distributed species throughout the U.S.A., by assessing nest initiation and establishment rates of colonies produced from wild-caught gynes, creating a timeline of colony development, and identifying lab-reared workers' critical thermal maxima (CTMax) and lethal temperature (ecological death). From 2019 to 2021, 70.6% of the wild-caught B. griseocollis gynes produced brood in a laboratory setting. Of these successfully initiated nests, 74.8% successfully established a nest (produced a worker), providing guidance for future rearing efforts. Additionally, lab-reared workers produced from wild-caught B. griseocollis gynes had an average CTMax of 43.5°C and an average lethal temperature of 46.4°C, suggesting B. griseocollis can withstand temperatures well above those commonly found in open field and greenhouse settings. Overall, B. griseocollis should continue to be evaluated for commercial purposes throughout the U.S.A.

Ensemble Models Predict Invasive Bee Habitat Suitability Will Expand under Future Climate Scenarios in Hawai'i.

Climate change is predicted to increase the risk of biological invasions by increasing the availability of climatically suitable regions for invasive species. Endemic species on oceanic islands are particularly sensitive to the impact of invasive species due to increased competition for shared resources and disease spread. In our study, we used an ensemble of species distribution models (SDM) to predict habitat suitability for invasive bees under current and future climate scenarios in Hawai'i. SDMs projected on the invasive range were better predicted by georeferenced records from the invasive range in comparison to invasive SDMs predicted by records from the native range. SDMs estimated that climatically suitable regions for the eight invasive bees explored in this study will expand by ~934.8% (±3.4% SE). Hotspots for the invasive bees are predicted to expand toward higher elevation regions, although suitable habitat is expected to only progress up to 500 m in elevation in 2070. Given our results, it is unlikely that invasive bees will interact directly with endemic bees found at >500 m in elevation in the future. Management and conservation plans for endemic bees may be improved by understanding how climate change may exacerbate negative interactions between invasive and endemic bee species.

Neonicotinoid Pesticides Cause Mass Fatalities of Native Bumble Bees: A Case Study From Wilsonville, Oregon, United States.

In June of 2013 an application of dinotefuran on an ornamental planting of European linden trees (Tilia cordata Mill. [Malvales: Malvalceae]) in a shopping mall parking lot in Wilsonville, Oregon provoked the largest documented pesticide kill of bumble bees in North America. Based on geographic information systems and population genetic analysis, we estimate that between 45,830 and 107,470 bumble bees originating from between 289 and 596 colonies were killed during this event. Dinotefuran is a neonicotinoid that is highly effective in exterminating and/or harming target pest insects and non-target beneficial insects. Analysis to detect the concentration of pesticides in flowers that received foliar application revealed that the minimum reported dinotefuran concentration of a sampled T. cordata flower was 7.4 ppm, or in excess of 737% above the LC50 of the beneficial pollinator, the honey bee (Apis mellifera Linnaeus, 1758 [Hymenoptera: Apidae]). Furthermore, sampled Vosnesensky bumble bees (Bombus vosnesenskii Radoskowski, 1862 [Hymenoptera: Apidae]) were found to have an average dinotefuran concentration of 0.92 ppm at the time of death, which exceeds the maximum LC50 of A. mellifera (0.884 ppm). Our study underscores the lethal impact of the neonicotinoid pesticide dinotefuran on pollinating insect populations in a suburban environment. To our knowledge, the documentation and impact of pesticide kills on wild populations of beneficial insects has not been widely reported in the scientific literature. It is likely that the vast majority of mass pesticide kills of beneficial insects across other environments go unnoticed and unreported.

Reduction in the potential distribution of bumble bees (Apidae: Bombus) in Mesoamerica under different climate change scenarios: Conservation implications.

Bumble bees are an ecologically and economically important group of pollinating insects worldwide. Global climate change is predicted to affect bumble bee ecology including habitat suitability and geographic distribution. Our study aims to estimate the impact of projected climate change on 18 Mesoamerican bumble bee species. We used ecological niche modeling (ENM) using current and future climate emissions scenarios (representative concentration pathway 4.5, 6.0, and 8.5) and models (CCSM4, HadGEM2-AO, and MIROC-ESM-CHEM). Regardless of the scenario and model applied, our results suggest that all bumble bee species are predicted to undergo a reduction in their potential distribution and habitat suitability due to projected climate change. ENMs based on low emission scenarios predict a distribution loss ranging from 7% to 67% depending on the species for the year 2050. Furthermore, we discovered that the reduction of bumble bee geographic range shape will be more evident at the margins of their distribution. The reduction of suitable habitat is predicted to be accompanied by a 100-500 m upslope change in altitude and 1-581 km shift away from the current geographic centroid of a species' distribution. On average, protected natural areas in Mesoamerica cover ~14% of each species' current potential distribution, and this proportion is predicted to increase to ~23% in the high emission climate change scenarios. Our models predict that climate change will reduce Mesoamerican bumble bee habitat suitability, especially for rare species, by reducing their potential distribution ranges and suitability. The small proportion of current and future potential distribution falling in protected natural areas suggests that such areas will likely have marginal contribution to bumble bee habitat conservation. Our results have the capacity to inform stakeholders in designing effective landscape management for bumble bees, which may include developing restoration plans for montane pine oak forests habitats and native flowering plants.

Foraging Economics of the Hunt Bumble Bee, a Viable Pollinator for Commercial Agriculture.

Globally, there are only five bumble bee (Hymenoptera: Apidae, Bombus) species that have been successfully commercialized for agriculture. The Hunt bumble bee, Bombus huntii Green, 1860, has been recognized as a suitable pollinator of crops and has a broad distribution in western North America, making it a viable candidate for commercialization. In this study, our goal was to characterize the foraging dynamics of B. huntii female workers under open field conditions. To accomplish this goal, we monitored three B. huntii colonies over an 8-wk period in the summer of 2012 in northern Utah. Using marked bees, we studied the relationship between foraging duration/offloading and pollen/nonvisible pollen collection. In total, we observed 921 foraging events across all three colonies. Of our observations, 82% (n = 756) were foraging events that included both a departure and arrival time observation. Average duration of pollen and nonpollen (i.e., nectar) trips across foragers is 41.86 ± 5.65 min (±SE) and 32.18 ± 5.89 min, respectively. Workers spent a significantly longer time offloading pollen in the nest after a foraging trip relative to workers without pollen present on their corbicula. Pollen foraging rate increases over the course of the day, likely due to the time it takes to learn how to forage on a diverse array of flower morphologies. Our study provides data on how long it takes for B. huntii to forage in open field conditions and will be useful when comparing foraging rates in controlled crop systems.

Phylogeny and population genetic analyses reveals cryptic speciation in the Bombus fervidus species complex (Hymenoptera: Apidae).

Bumble bees (Bombus Latrielle) are significant pollinators of flowering plants due to their large body size, abundant setae, and generalist foraging strategies. However, shared setal coloration patterns among closely and distantly related bumble bee species makes identification notoriously difficult. The advent of molecular genetic techniques has increased our understanding of bumble bee evolution and taxonomy, and enables effective conservation policy and management. Individuals belonging to the North American Bombus fervidus species-complex (SC) are homogenous in body structure but exhibit significant body color phenotype variation across their geographic distribution. Given the uncertainty of the genealogical boundaries within the SC, some authors have synonymized all members of the B. fervidus SC within a single taxon, while others propose an alternative two taxa hypothesis. Operating under the phylogenetic species concept, our analysis supports the hypothesis that there are two independent lineages of bumble bees within the B. fervidus SC. With the current evidence, however, it is not possible to assign valid names to either of them, because both lineages include the color phenotypes found in the original species descriptions of B. fervidus and B. californicus. Cryptic speciation does not seem to be the product of Müllerian mimicry between the clades, because diverging coloration patterns are observed when the distribution of the clades overlaps. Furthermore, within each lineage there is evidence for strong population differentiation that is correlated with geographic distribution rather than color phenotype. In our study, we demonstrate the importance of obtaining a broad sample of multiple populations when conducting lower-level phylogenetic analyses. In addition to improving our knowledge of bumble bee diversification patterns, characterizing the evolutionary history of these pollinators provides the foundation needed to guide contemporary conservation assessments and management strategies.

Quaternary climate instability is correlated with patterns of population genetic variability in Bombus huntii.

Climate oscillations have left a significant impact on the patterns of genetic diversity observed in numerous taxa. In this study, we examine the effect of Quaternary climate instability on population genetic variability of a bumble bee pollinator species, Bombus huntii in western North America. Pleistocene and contemporary B. huntii habitat suitability (HS) was estimated with an environmental niche model (ENM) by associating 1,035 locality records with 10 bioclimatic variables. To estimate genetic variability, we genotyped 380 individuals from 33 localities at 13 microsatellite loci. Bayesian inference was used to examine population structure with and without a priori specification of geographic locality. We compared isolation by distance (IBD) and isolation by resistance (IBR) models to examine population differentiation within and among the Bayesian inferred genetic clusters. Furthermore, we tested for the effect of environmental niche stability (ENS) on population genetic diversity with linear regression. As predicted, high-latitude B. huntii habitats exhibit low ENS when compared to low-latitude habitats. Two major genetic clusters of B. huntii inhabit western North America: (a) a north genetic cluster predominantly distributed north of 28°N and (b) a south genetic cluster distributed south of 28°N. In the south genetic cluser, both IBD and IBR models are significant. However, in the north genetic cluster, IBD is significant but not IBR. Furthermore, the IBR models suggest that low-latitude montane populations are surrounded by habitat with low HS, possibly limiting dispersal, and ultimately gene flow between populations. Finally, we detected high genetic diversity across populations in regions that have been climatically unstable since the last glacial maximum (LGM), and low genetic diversity across populations in regions that have been climatically stable since the LGM. Understanding how species have responded to climate change has the potential to inform management and conservation decisions of both ecological and economic concerns.

Pheromone Lure and Trap Color Affects Bycatch in Agricultural Landscapes of Utah.

Aerial traps, using combinations of color and attractive lures, are a critical tool for detecting and managing insect pest populations. Yet, despite improvements in trap efficacy, collection of nontarget species ("bycatch") plagues many insect pest surveys. Bycatch can influence survey effectiveness by reducing the available space for target species and increasing trap screening time, especially in areas where thousands of insects are captured as bycatch in a given season. Additionally, bycatch may negatively impact local nontarget insect populations, including beneficial predators and pollinators. Here, we tested the effect of pheromone lures on bycatch rates of Coccinellidae (Coleoptera), Apoidea (Hymenoptera), and nontarget Lepidoptera. Multicolored (primarily yellow and white) bucket traps containing a pheromone lure for capturing one of three survey target species, Spodoptera litura (F.), S. littoralis (Boisduval), or Helicoverpa armigera (Hübner), were placed in alfalfa and corn fields, and compared to multicolored traps without a pheromone lure. All-green traps with and without H. armigera lures were employed in a parallel study investigating the effect of lure and trap color on bycatch. Over 2,600 Coccinellidae representing seven species, nearly 6,400 bees in 57 species, and >9,000 nontarget moths in 17 genera were captured across 180 traps and seven temporal sampling events. Significant effects of lure and color were observed for multiple taxa. In general, nontarget insects were attracted to the H. armigera lure and multicolored trap, but further studies of trap color and pheromone lure specificity are needed to better understand these interactions and to minimize nontarget captures.

Evidence for Bombus occidentalis (Hymenoptera: Apidae) Populations in the Olympic Peninsula, the Palouse Prairie, and Forests of Northern Idaho.

Since the mid-1990s, Bombus occidentalis (Green) has declined from being one of the most common to one of the rarest bumble bee species in the Pacific Northwest of the United States. Although its conservation status is unresolved, a petition to list this species as endangered or threatened was recently submitted to the U.S. Fish and Wildlife Service. To shed light on the conservation situation and inform the U.S. Fish and Wildlife Service decision, we report on the detection and abundance of B. occidentalis following bumble bee collection between 2012 and 2014 across the Pacific Northwest. Collection occurred from the San Juan Islands and Olympic peninsula east to northern Idaho and northeastern Oregon, excluding the arid region in central Washington. B. occidentalis was observed at 23 collection sites out of a total of 234. With the exception of three sites on the Olympic peninsula, all of these were in the southeastern portion of the collection range.

USBombus, a database of contemporary survey data for North American Bumble Bees (Hymenoptera, Apidae, Bombus) distributed in the United States.

BACKGROUND: Bumble bees (Hymenoptera: Apidae, Bombus) are pollinators of wild and economically important flowering plants. However, at least four bumble bee species have declined significantly in population abundance and geographic range relative to historic estimates, and one species is possibly extinct. While a wealth of historic data is now available for many of the North American species found to be in decline in online databases, systematic survey data of stable species is still not publically available. The availability of contemporary survey data is critically important for the future monitoring of wild bumble bee populations. Without such data, the ability to ascertain the conservation status of bumble bees in the United States will remain challenging. NEW INFORMATION: This paper describes USBombus, a large database that represents the outcomes of one of the largest standardized surveys of bumble bee pollinators (Hymenoptera, Apidae, Bombus) globally. The motivation to collect live bumble bees across the United States was to examine the decline and conservation status of Bombus affinis, B. occidentalis, B. pensylvanicus, and B. terricola. Prior to our national survey of bumble bees in the United States from 2007 to 2010, there have only been regional accounts of bumble bee abundance and richness. In addition to surveying declining bumble bees, we also collected and documented a diversity of co-occuring bumble bees. However we have not yet completely reported their distribution and diversity onto a public online platform. Now, for the first time, we report the geographic distribution of bumble bees reported to be in decline (Cameron et al. 2011), as well as bumble bees that appeared to be stable on a large geographic scale in the United States (not in decline). In this database we report a total of 17,930 adult occurrence records across 397 locations and 39 species of Bombus detected in our national survey. We summarize their abundance and distribution across the United States and association to different ecoregions. The geospatial coverage of the dataset extends across 41 of the 50 US states, and from 0 to 3500 m a.s.l. Authors and respective field crews spent a total of 512 hours surveying bumble bees from 2007 to 2010. The dataset was developed using SQL server 2008 r2. For each specimen, the following information is generally provided: species, name, sex, caste, temporal and geospatial details, Cartesian coordinates, data collector(s), and when available, host plants. This database has already proven useful for a variety of studies on bumble bee ecology and conservation. However it is not publicly available. Considering the value of pollinators in agriculture and wild ecosystems, this large database of bumble bees will likely prove useful for investigations of the effects of anthropogenic activities on pollinator community composition and conservation status.

Taxonomic utility of niche models in validating species concepts: A case study in Anthophora (Heliophila) (Hymenoptera: Apidae).

Taxonomy has far-reaching effects throughout biology, and incorrect taxonomy can be detrimental in many ways. Polymorphic species complexes, many of which exist in the bee genus Anthophora Latreille, lend themselves to such difficulties. This study employs environmental niche mapping (ENM) and traditional morphological analyses to investigate the validity of the subjective synonymy of Anthophora (Heliophila) curta Provancher with the senior synonym A. squammulosa Dours. Eleven of fifty morphological characters consistently differentiate the two putative species, with an additional five characters sometimes separating them. Additionally, based on over 1000 georeferenced museum specimens, the geographic ranges of the two taxa do not overlap. The two entities also react differently to the bioclimatic variables based on correlation analysis. We further tested the two-species hypothesis by constructing ENMs with informative bioclimatic variables associated with locality records. Their modelled distributions overlapped less than 1%, suggesting discrete environmental boundaries. The variables which contributed most to each species' model also differed. These differences are explored in relation to their habitats. The combined morphological and biogeographic analysis indicates that A. curta and A. squammulosa are distinct species. Based on the accumulated evidence the synonymy is formally rejected and A. curta is recognized as a valid species. Five additional taxa (A. bispinosa Cockerell, A. franciscana Cockerell, A. usticauda Cockerell, A. u. cinerior Cockerell, A. zamoranella Cockerell) are newly synonymized with A. squammulosa and Anthophora curta var. melanops Cockerell is newly synonymized with A. curta. Implications outside of taxonomy are discussed. 

Leafcutter bee nests and pupae from the Rancho La Brea Tar Pits of Southern California: implications for understanding the paleoenvironment of the Late Pleistocene.

The Rancho La Brea Tar Pits is the world's richest and most important Late Pleistocene fossil locality and best renowned for numerous fossil mammals and birds excavated over the past century. Less researched are insects, even though these specimens frequently serve as the most valuable paleoenvironemental indicators due to their narrow climate restrictions and life cycles. Our goal was to examine fossil material that included insect-plant associations, and thus an even higher potential for significant paleoenviromental data. Micro-CT scans of two exceptionally preserved leafcutter bee nest cells from the Rancho La Brea Tar Pits in Los Angeles, California reveal intact pupae dated between ∼23,000-40,000 radiocarbon years BP. Here identified as best matched to Megachile (Litomegachile) gentilis Cresson (Hymenoptera: Megachilidae) based on environmental niche models as well as morphometrics, the nest cells (LACMRLP 388E) document rare preservation and life-stage. The result of complex plant-insect interactions, they offer new insights into the environment of the Late Pleistocene in southern California. The remarkable preservation of the nest cells suggests they were assembled and nested in the ground where they were excavated. The four different types of dicotyledonous leaves used to construct the cells were likely collected in close proximity to the nest and infer a wooded or riparian habitat with sufficient pollen sources for larval provisions. LACMRLP 388E is the first record of fossil Megachile Latreille cells with pupae. Consequently, it provides a pre-modern age location for a Nearctic group, whose phylogenetic relationships and biogeographic history remain poorly understood. Megachile gentilis appears to respond to climate change as it has expanded its distribution across elevation gradients over time as estimated by habitat suitability comparisons between low and high elevations; it currently inhabits mesic habitats which occurred at a lower elevation during the Last Glacial Maximum ∼21,000 years ago. Nevertheless, the broad ecological niche of M. gentilis appears to have remained stable.

Patterns of widespread decline in North American bumble bees.

Bumble bees (Bombus) are vitally important pollinators of wild plants and agricultural crops worldwide. Fragmentary observations, however, have suggested population declines in several North American species. Despite rising concern over these observations in the United States, highlighted in a recent National Academy of Sciences report, a national assessment of the geographic scope and possible causal factors of bumble bee decline is lacking. Here, we report results of a 3-y interdisciplinary study of changing distributions, population genetic structure, and levels of pathogen infection in bumble bee populations across the United States. We compare current and historical distributions of eight species, compiling a database of >73,000 museum records for comparison with data from intensive nationwide surveys of >16,000 specimens. We show that the relative abundances of four species have declined by up to 96% and that their surveyed geographic ranges have contracted by 23-87%, some within the last 20 y. We also show that declining populations have significantly higher infection levels of the microsporidian pathogen Nosema bombi and lower genetic diversity compared with co-occurring populations of the stable (nondeclining) species. Higher pathogen prevalence and reduced genetic diversity are, thus, realistic predictors of these alarming patterns of decline in North America, although cause and effect remain uncertain.