A century of wild bee sampling: historical data and neural network analysis reveal ecological traits associated with species loss.

We analysed the wild bee community sampled from 1921 to 2018 at a nature preserve in southern Michigan, USA, to study long-term community shifts in a protected area. During an intensive survey in 1972 and 1973, Francis C. Evans detected 135 bee species. In the most recent intensive surveys conducted in 2017 and 2018, we recorded 90 species. Only 58 species were recorded in both sampling periods, indicating a significant shift in the bee community. We found that the bee community diversity, species richness and evenness were all lower in recent samples. Additionally, 64% of the more common species exhibited a more than 30% decline in relative abundance. Neural network analysis of species traits revealed that extirpation from the reserve was most likely for oligolectic ground-nesting bees and kleptoparasitic bees, whereas polylectic cavity-nesting bees were more likely to persist. Having longer phenological ranges also increased the chance of persistence in polylectic species. Further analysis suggests a climate response as bees in the contemporary sampling period had a more southerly overall distribution compared to the historic community. Results exhibit the utility of both long-term data and machine learning in disentangling complex indicators of bee population trajectories.

Large ecosystem-scale effects of restoration fail to mitigate impacts of land-use legacies in longleaf pine savannas.

Ecological restoration is a global priority, with potential to reverse biodiversity declines and promote ecosystem functioning. Yet, successful restoration is challenged by lingering legacies of past land-use activities, which are pervasive on lands available for restoration. Although legacies can persist for centuries following cessation of human land uses such as agriculture, we currently lack understanding of how land-use legacies affect entire ecosystems, how they influence restoration outcomes, or whether restoration can mitigate legacy effects. Using a large-scale experiment, we evaluated how restoration by tree thinning and land-use legacies from prior cultivation and subsequent conversion to pine plantations affect fire-suppressed longleaf pine savannas. We evaluated 45 ecological properties across four categories: 1) abiotic attributes, 2) organism abundances, 3) species diversity, and 4) species interactions. The effects of restoration and land-use legacies were pervasive, shaping all categories of properties, with restoration effects roughly twice the magnitude of legacy effects. Restoration effects were of comparable magnitude in savannas with and without a history of intensive human land use; however, restoration did not mitigate numerous legacy effects present prior to restoration. As a result, savannas with a history of intensive human land use supported altered properties, especially related to soils, even after restoration. The signature of past human land-use activities can be remarkably persistent in the face of intensive restoration, influencing the outcome of restoration across diverse ecological properties. Understanding and mitigating land-use legacies will maximize the potential to restore degraded ecosystems.

Global patterns in bumble bee pollen collection show phylogenetic conservation of diet.

Bumble bees (Bombus) are a group of eusocial bees with a strongly generalised feeding pattern, collecting pollen from many different botanical families. Though predominantly generalists, some bumble bee species seem to have restricted dietary choices. It is unclear whether restricted diets in bumble bees are inherent or a function of local conditions due to a lack of data for many species across different regions. The objective of this study was to determine whether bumble bee species displayed specific patterns of pollen collection, and whether patterns were influenced by phylogenetic relatedness or tongue length, a trait known to be associated with structuring floral visitation. Bumble bee pollen collection patterns were quantified from 4,132 pollen loads taken from 58 bumble bee species, representing 24% of the pollen-collecting diversity of this genus. Phylogenetic trait mapping showed a conserved pattern of dietary dissimilarity across species, but not for dietary breadth. Dietary dissimilarity was driven by collection of Fabaceae, with the most similar species collecting around 50%-60% of their diet from this botanical family. The proportion of the diet collected from Fabaceae also showed a conserved phylogenetic signal. Greater collection of Fabaceae was associated with longer tongue lengths, with shorter tongued species focusing on alternative botanical families. However, this result was largely driven by phylogenetic relatedness, not tongue length per se. These results demonstrate that, though generalists, bumble bees are still subject to dietary restrictions that constrain their foraging choices. These dietary constraints have implications for their persistence should their core resources decline in abundance.

Mismatched outcomes for biodiversity and ecosystem services: testing the responses of crop pollinators and wild bee biodiversity to habitat enhancement.

Supporting ecosystem services and conserving biodiversity may be compatible goals, but there is concern that service-focused interventions mostly benefit a few common species. We use a spatially replicated, multiyear experiment in four agricultural settings to test if enhancing habitat adjacent to crops increases wild bee diversity and abundance on and off crops. We found that enhanced field edges harbored more taxonomically and functionally abundant, diverse, and compositionally different bee communities compared to control edges. Enhancements did not increase the abundance or diversity of bees visiting crops, indicating that the supply of pollination services was unchanged following enhancement. We find that actions to promote crop pollination improve multiple dimensions of biodiversity, underscoring their conservation value, but these benefits may not be spilling over to crops. More work is needed to identify the conditions that promote effective co-management of biodiversity and ecosystem services.

Bee phenology is predicted by climatic variation and functional traits.

Climate change is shifting the environmental cues that determine the phenology of interacting species. Plant-pollinator systems may be susceptible to temporal mismatch if bees and flowering plants differ in their phenological responses to warming temperatures. While the cues that trigger flowering are well-understood, little is known about what determines bee phenology. Using generalised additive models, we analyzed time-series data representing 67 bee species collected over 9 years in the Colorado Rocky Mountains to perform the first community-wide quantification of the drivers of bee phenology. Bee emergence was sensitive to climatic variation, advancing with earlier snowmelt timing, whereas later phenophases were best explained by functional traits including overwintering stage and nest location. Comparison of these findings to a long-term flower study showed that bee phenology is less sensitive than flower phenology to climatic variation, indicating potential for reduced synchrony of flowers and pollinators under climate change.

Feeding specialization and longer generation time are associated with relatively larger brains in bees.

Despite their miniature brains, insects exhibit substantial variation in brain size. Although the functional significance of this variation is increasingly recognized, research on whether differences in insect brain sizes are mainly the result of constraints or selective pressures has hardly been performed. Here, we address this gap by combining prospective and retrospective phylogenetic-based analyses of brain size for a major insect group, bees (superfamily Apoidea). Using a brain dataset of 93 species from North America and Europe, we found that body size was the single best predictor of brain size in bees. However, the analyses also revealed that substantial variation in brain size remained even when adjusting for body size. We consequently asked whether such variation in relative brain size might be explained by adaptive hypotheses. We found that ecologically specialized species with single generations have larger brains-relative to their body size-than generalist or multi-generation species, but we did not find an effect of sociality on relative brain size. Phylogenetic reconstruction further supported the existence of different adaptive optima for relative brain size in lineages differing in feeding specialization and reproductive strategy. Our findings shed new light on the evolution of the insect brain, highlighting the importance of ecological pressures over social factors and suggesting that these pressures are different from those previously found to influence brain evolution in other taxa.

Flower traits associated with the visitation patterns of bees.

Plant-pollinator interactions are partially driven by the expression of plant traits that signal and attract bees to the nutritional resources within flowers. Although multiple physical and chemical floral traits are known to influence the visitation patterns of bees, how distinct bee groups vary in their responses to floral traits has yet to be elucidated. In this study, we used a common garden experiment to test for morphological floral traits associated with pollen quantity at the plant species level, and examined how the visitation patterns of taxonomically and functionally distinct bee groups are related to flower trait characteristics of 39 wildflower species. We also determined how floral traits influence the structure of wild bee communities visiting plants and whether this varies among geographic localities. Our results suggest that floral area is the primary morphological floral trait related to bee visitation of several distinct bee groups, but that wild bee families and functionally distinct bee groups have unique responses to floral trait expression. The composition of the wild bee communities visiting different plants was most strongly associated with variability in floral area, flower height, and the quantity of pollen retained in flowers. Our results inform wildflower habitat management for bees by demonstrating that the visitation patterns of distinct bee taxa can be predicted by floral traits, and highlight that variability in these traits should be considered when selecting plants to support pollinators.

Specialist foragers in forest bee communities are small, social or emerge early.

Individual pollinators that specialize on one plant species within a foraging bout transfer more conspecific and less heterospecific pollen, positively affecting plant reproduction. However, we know much less about pollinator specialization at the scale of a foraging bout compared to specialization by pollinator species. In this study, we measured the diversity of pollen carried by individual bees foraging in forest plant communities in the mid-Atlantic United States. We found that individuals frequently carried low-diversity pollen loads, suggesting that specialization at the scale of the foraging bout is common. Individuals of solitary bee species carried higher diversity pollen loads than did individuals of social bee species; the latter have been better studied with respect to foraging bout specialization, but account for a small minority of the world's bee species. Bee body size was positively correlated with pollen load diversity, and individuals of polylectic (but not oligolectic) species carried increasingly diverse pollen loads as the season progressed, likely reflecting an increase in the diversity of flowers in bloom. Furthermore, the seasonal increase in pollen load diversity was stronger for bees visiting trees and shrubs than for bees visiting herbaceous plants. Overall, our results showed that both plant and pollinator species' traits as well as community-level patterns of flowering phenology are likely to be important determinants of individual-level interactions in plant-pollinator communities.

Modeling the status, trends, and impacts of wild bee abundance in the United States.

Wild bees are highly valuable pollinators. Along with managed honey bees, they provide a critical ecosystem service by ensuring stable pollination to agriculture and wild plant communities. Increasing concern about the welfare of both wild and managed pollinators, however, has prompted recent calls for national evaluation and action. Here, for the first time to our knowledge, we assess the status and trends of wild bees and their potential impacts on pollination services across the coterminous United States. We use a spatial habitat model, national land-cover data, and carefully quantified expert knowledge to estimate wild bee abundance and associated uncertainty. Between 2008 and 2013, modeled bee abundance declined across 23% of US land area. This decline was generally associated with conversion of natural habitats to row crops. We identify 139 counties where low bee abundances correspond to large areas of pollinator-dependent crops. These areas of mismatch between supply (wild bee abundance) and demand (cultivated area) for pollination comprise 39% of the pollinator-dependent crop area in the United States. Further, we find that the crops most highly dependent on pollinators tend to experience more severe mismatches between declining supply and increasing demand. These trends, should they continue, may increase costs for US farmers and may even destabilize crop production over time. National assessments such as this can help focus both scientific and political efforts to understand and sustain wild bees. As new information becomes available, repeated assessments can update findings, revise priorities, and track progress toward sustainable management of our nation's pollinators.

Forest bees are replaced in agricultural and urban landscapes by native species with different phenologies and life-history traits.

Anthropogenic landscapes are associated with biodiversity loss and large shifts in species composition and traits. These changes predict the identities of winners and losers of future global change, and also reveal which environmental variables drive a taxon's response to land use change. We explored how the biodiversity of native bee species changes across forested, agricultural, and urban landscapes. We collected bee community data from 36 sites across a 75,000 km2 region, and analyzed bee abundance, species richness, composition, and life-history traits. Season-long bee abundance and richness were not detectably different between natural and anthropogenic landscapes, but community phenologies differed strongly, with an early spring peak followed by decline in forests, and a more extended summer season in agricultural and urban habitats. Bee community composition differed significantly between all three land use types, as did phylogenetic composition. Anthropogenic land use had negative effects on the persistence of several life-history strategies, including early spring flight season and brood parasitism, which may indicate adaptation to conditions in forest habitat. Overall, anthropogenic communities are not diminished subsets of contemporary natural communities. Rather, forest species do not persist in anthropogenic habitats, but are replaced by different native species and phylogenetic lineages preadapted to open habitats. Characterizing compositional and functional differences is crucial for understanding land use as a global change driver across large regional scales.

DNA barcoding a nightmare taxon: assessing barcode index numbers and barcode gaps for sweat bees.

There is an ongoing campaign to DNA barcode the world's >20 000 bee species. Recent revisions of Lasioglossum (Dialictus) (Hymenoptera: Halictidae) for Canada and the eastern United States were completed using integrative taxonomy. DNA barcode data from 110 species of L. (Dialictus) are examined for their value in identification and discovering additional taxonomic diversity. Specimen identification success was estimated using the best close match method. Error rates were 20% relative to current taxonomic understanding. Barcode Index Numbers (BINs) assigned using Refined Single Linkage Analysis (RESL) and barcode gaps using the Automatic Barcode Gap Discovery (ABGD) method were also assessed. RESL was incongruent for 44.5% of species, although some cryptic diversity may exist. Forty-three of 110 species were part of merged BINs with multiple species. The barcode gap is non-existent for the data set as a whole and ABGD showed levels of discordance similar to the RESL. The viridatum species-group is particularly problematic, so that DNA barcodes alone would be misleading for species delimitation and specimen identification. Character-based methods using fixed nucleotide substitutions could improve specimen identification success in some cases. The use of DNA barcoding for species discovery for standard taxonomic practice in the absence of a well-defined barcode gap is discussed.

The relative importance of pollinator abundance and species richness for the temporal variance of pollination services.

The relationship between biodiversity and the stability of ecosystem function is a fundamental question in community ecology, and hundreds of experiments have shown a positive relationship between species richness and the stability of ecosystem function. However, these experiments have rarely accounted for common ecological patterns, most notably skewed species abundance distributions and non-random extinction risks, making it difficult to know whether experimental results can be scaled up to larger, less manipulated systems. In contrast with the prolific body of experimental research, few studies have examined how species richness affects the stability of ecosystem services at more realistic, landscape scales. The paucity of these studies is due in part to a lack of analytical methods that are suitable for the correlative structure of ecological data. A recently developed method, based on the Price equation from evolutionary biology, helps resolve this knowledge gap by partitioning the effect of biodiversity into three components: richness, composition, and abundance. Here, we build on previous work and present the first derivation of the Price equation suitable for analyzing temporal variance of ecosystem services. We applied our new derivation to understand the temporal variance of crop pollination services in two study systems (watermelon and blueberry) in the mid-Atlantic United States. In both systems, but especially in the watermelon system, the stronger driver of temporal variance of ecosystem services was fluctuations in the abundance of common bee species, which were present at nearly all sites regardless of species richness. In contrast, temporal variance of ecosystem services was less affected by differences in species richness, because lost and gained species were rare. Thus, the findings from our more realistic landscapes differ qualitatively from the findings of biodiversity-stability experiments.

Historical changes in northeastern US bee pollinators related to shared ecological traits.

Pollinators such as bees are essential to the functioning of terrestrial ecosystems. However, despite concerns about a global pollinator crisis, long-term data on the status of bee species are limited. We present a long-term study of relative rates of change for an entire regional bee fauna in the northeastern United States, based on >30,000 museum records representing 438 species. Over a 140-y period, aggregate native species richness weakly decreased, but richness declines were significant only for the genus Bombus. Of 187 native species analyzed individually, only three declined steeply, all of these in the genus Bombus. However, there were large shifts in community composition, as indicated by 56% of species showing significant changes in relative abundance over time. Traits associated with a declining relative abundance include small dietary and phenological breadth and large body size. In addition, species with lower latitudinal range boundaries are increasing in relative abundance, a finding that may represent a response to climate change. We show that despite marked increases in human population density and large changes in anthropogenic land use, aggregate native species richness declines were modest outside of the genus Bombus. At the same time, we find that certain ecological traits are associated with declines in relative abundance. These results should help target conservation efforts focused on maintaining native bee abundance and diversity and therefore the important ecosystems services that they provide.

Negative effects of pesticides on wild bee communities can be buffered by landscape context.

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.

A problematic species complex of Lasioglossum subgeneric diagnostics in North America (Hymenoptera: Halictidae).

A problematic species complex within Lasioglossum subgenus Sphecodogastra with unusual metallic reflections on the mesosoma is described from North America. Three new species in this complex are described and illustrated: Lasioglossum (Sphecodogastra) iridescens sp. nov., Lasioglossum (Sphecodogastra) dilisena sp. nov., and Lasioglossum (Sphecodogastra) silveirai sp. nov. Our study addresses the challenge of diagnosing Lasioglossum subgenera within North America. We present an updated key for the North American Lasioglossum subgenera.

Spatiotemporal variability and foraging behavior of bee visitors to a rare long-lived iteroparous forb, Silene spaldingii (Caryophyllaceae).

Silene spaldingii S Watson is a rare long-lived forb (Caryophyllaceae) found primarily in open native grasslands of the Inland Pacific Northwest and is putatively pollinated by one key bumble bee pollinator, Bombus fervidus (Fabricius). However, populations of bumble bees and their visitation patterns can vary dramatically, and some species are in decline including B. fervidus. Understanding the role of co-pollinators such as sweat bees (Halictidae) could be crucial as the plight of rare plants and pollinators intensifies. We collected data across three seasons (2015-2017) on the Bombus-S. spaldingii pollination system, focusing on three Key Conservation Areas in the Channeled Scablands of eastern Washington. Bee visitors to S. spaldingii were monitored and the pool-of-pollinators was surveyed with blue vane traps. Nine species of bees were observed foraging on the plant, while 2211 bees comprised of five families, 22 genera and 81 taxa were captured in blue vane traps, meaning only 11.1% of species in the pollinator pool visited S. spaldingii. Halictus tripartitus Cockerell, a sweat bee, was a common visitor to the plant, but this was the first record of visitation for several other species, including Lasioglossum buccale (Pérez) which has never before been recorded in the Americas. These sweat bees appear to vector S. spaldingii pollen, suggesting they are co-pollinators of the plant. Weather and patch characteristics affected visitation patterns and the pool-of-pollinators. We conclude that sweat bees are likely co-pollinators of S. spaldingii and that they could become increasingly important if B. fervidus populations continue to decline.

Oxytocin Receptor Single-Nucleotide Polymorphisms Are Related to Maternal-Infant Co-Occupation and Infant Sensory Processing.

BACKGROUND: Caregiver-infant reciprocity is related to infant/toddler development and health. However, there is a dearth of research on reciprocity variables like co-occupation and developmental variables such as infant/toddler sensory processing/preferences, and it is important to understand the biopsychosocial mediators of these relations. These include novel genetic markers like maternal oxytocin receptor single-nucleotide polymorphisms (OXTR SNPs). Therefore, this study examined whether mothers carrying risk alleles for three OXTR SNPs displayed different co-occupational behaviors with their infants and whether their infants/toddlers showed different sensory processing/preferences. METHODS: Data from the Infant Development and Healthy Outcomes in Mothers Study included prenatal saliva samples assayed for OXTR SNPs, 6-month postnatal behavioral observations coded for maternal-infant co-occupations (reciprocal emotionality, physicality, and intentionality), and 10-, 14-, and 18-month postnatal, maternal-reported Infant/Toddler Sensory Profiles (classified as within or outside the majority range for low registration, sensory seeking, sensory sensitivity, and sensory avoiding). RESULTS: Mothers with rs53576 risk allele A engaged in more frequent reciprocal emotionality, while those with rs2254298 risk allele A engaged in less frequent reciprocal emotionality but more frequent reciprocal intentionality. Mothers with rs53576 risk allele A had infants with 11 times greater odds of being outside of the majority range for sensation avoiding at 10 months old. CONCLUSIONS: The results converge with the literature supporting links between OXTR SNPs, caregiver reciprocity, and infant/toddler development but extend the findings to relatively novel constructs (caregiver-infant co-occupations and infant/toddler sensory processing/preferences).

Biodiversity ensures plant-pollinator phenological synchrony against climate change.

Climate change has the potential to alter the phenological synchrony between interacting mutualists, such as plants and their pollinators. However, high levels of biodiversity might buffer the negative effects of species-specific phenological shifts and maintain synchrony at the community level, as predicted by the biodiversity insurance hypothesis. Here, we explore how biodiversity might enhance and stabilise phenological synchrony between a valuable crop, apple and its native pollinators. We combine 46 years of data on apple flowering phenology with historical records of bee pollinators over the same period. When the key apple pollinators are considered altogether, we found extensive synchrony between bee activity and apple peak bloom due to complementarity among bee species' activity periods, and also a stable trend over time due to differential responses to warming climate among bee species. A simulation model confirms that high biodiversity levels can ensure plant-pollinator phenological synchrony and thus pollination function.

Revision and reclassification of Lasioglossum (Evylaeus), L. (Hemihalictus) and L. (Sphecodogastra) in eastern North America (Hymenoptera: Apoidea: Halictidae).

The black species of weak-veined Lasioglossum (or Hemihalictus series) in eastern North America are revised to clarify their taxonomy and nomenclature and to facilitate identification. A subgeneric classification based upon available phylogenetic data is applied. Lasioglossum (Sphecodogastra) is applied more broadly than any previous usage to include many species typically classified as L. (Evylaeus). The subgenus L. (Evylaeus) is retained but applied narrowly in agreement with phylogenetic results. Lasioglossum (Hemihalictus) has historically been considered monotypic but is here applied to many species of L. (Dialictus) sensu lato (equivalent to the carinaless L. (Evylaeus) of some authors). Usage of L. (Dialictus) is restricted primarily to species with metallic integument. Additional subgeneric synonymies for extralimital taxa are formalized and discussed. Descriptions are provided for each species with a synonymic list, diagnosis, and notes on taxonomy and biology. The recently revised Onagraceae-specialist species of L. (Sphecodogastra) are given abbreviated treatments. Notes on available DNA barcode data are given, with diagnostic characters supplied for closely related spe-cies. One new species is described: L. (Sphecodogastra) seillean Gibbs and Packer and the males of L. fedorense (Crawford) and L. pectinatum (Robertson) are described for the first time. The following three new synonymies are proposed: Lasioglossum (Hemihalictus) sopinci (Crawford), senior subjective synonym of Evylaeus bradleyi Mitchell; Lasioglosum (Hemihalictus) macoupinense (Robertson), senior subjective synonym of Halictus divergens Lovell; and Lasioglossum (Hemihalictus) inconditum (Cockerell), senior subjective synonym of Halictus tracyi Cockerell. Lasioglossum inconditum is here considered to be distinct from the Palaearctic species L. rufitarse (Zetterstedt). A lectotype is designat-ed for Halictus quebecensis Crawford. We present the first record of L. lustrans (Cockerell) and L. swenki (Crawford) in Canada and the first record of L. lusorium (Cresson) east of the Mississippi River. Updated keys to species are provided for the fauna of eastern North America.

Socioeconomic resources moderate the relationship between maternal prenatal obsessive-compulsive symptoms and infant negative affectivity.

Perinatal maternal depression, anxiety, and stress are associated with poor infant outcomes. However, no known study has investigated the effects of perinatal maternal obsessive-compulsive symptomatology on infant outcomes while considering important situational factors such as socioeconomic resources. Therefore, we investigated the effects of prenatal and postnatal obsessive-compulsive symptomatology on infant behavioral reactivity, beyond the effects of postnatal depressive symptomatology, at 6 months of age. It was expected that socioeconomic resources would moderate this relationship. We recruited 125 pregnant women from a Health Professional Shortage Area for mental health and primary care in the Midwest United States and interviewed them at approximately 34 weeks gestation and again at 6 months postnatally. They were administered questionnaires at both time points measuring obsessive-compulsive and depressive symptoms. Infant behavioral reactivity was gathered during 6-month follow-up through behavioral observation coding and maternal-report modalities. Maternal-reported infant negative affectivity at 6 months was related to greater severity of maternal postnatal depressive symptomatology, and socioeconomic resources moderated the relationship between maternal prenatal obsessive-compulsive symptoms and maternal-reported infant negative affectivity. However, neither of these relations was statistically significant when infant reactivity was quantified using behavioral observations.