Fine-scale monitoring and mapping of biodiversity and ecosystem services reveals multiple synergies and few tradeoffs in urban green space management.

Urban watersheds can play a critical role in supporting biodiversity and ecosystem services in a rapidly changing world. However, managing for multiple environmental and social objectives in urban landscapes is challenging, especially if the optimization of one ecosystem service conflicts with another. Urban ecology research has frequently been limited to a few indicators - typically either biodiversity or ecosystem service indices - making tradeoffs and synergies difficult to assess. Through a recently established watershed-scale monitoring network in Central Texas, we address this gap by evaluating biodiversity (flora and fauna), habitat quality, and ecosystem service indices of urban green spaces across the watershed. Our results reveal substantial heterogeneity in biodiversity and ecosystem service levels and multiple synergies (stacked benefits or "win-wins"). For example, we found that carbon sequestration positively correlated with tree species richness and the proportion of native trees in a green space, indicating that biodiversity goals for increased tree diversity can also provide carbon sequestration benefits. We also documented correlations between green spaces with greater riparian forest cover and lower particulate matter (PM2.5) concentrations and cooler temperatures. In addition, we found that bee and wasp species richness was positively correlated with carbon sequestration and human visitation rates, meaning that urban green spaces can optimize carbon sequestration goals without losing pollinator habitat or access opportunities for city residents. Overall, our results indicate that many aspects of habitat quality, biodiversity, and ecosystem services can be simultaneously supported in urban green spaces. We conclude that urban design and management can optimize nature-based solutions and strategies to have distinct positive impacts on both people and nature.

The Native Bees of Texas: Evaluating the Benefits of a Public Engagement Course.

Declines in native bee communities due to forces of global change have become an increasing public concern. Despite this heightened interest, there are few publicly available courses on native bees, and little understanding of how participants might benefit from such courses. In October of 2018 and 2019, we taught the 'Native Bees of Texas' course to the public at The University of Texas at Austin Lady Bird Johnson Wildflower Center botanical gardens in an active learning environment with slide-based presentations, printed photo-illustrated resources, and direct insect observations. In this study, we evaluated course efficacy and learning outcomes with a pre/post-course test, a survey, and open-ended feedback, focused on quality improvement findings. Overall, participants' test scores increased significantly, from 60% to 87% correct answers in 2018 and from 64% to 87% in 2019, with greater post-course differences in ecological knowledge than in identification skills. Post-course, the mean of participants' bee knowledge self-ratings was 4.56 on a five-point scale. The mean of participants' ratings of the degree to which they attained the course learning objectives was 4.43 on a five-point scale. Assessment results provided evidence that the course enriched participants' knowledge of native bee ecology and conservation and gave participants a basic foundation in bee identification. This highlights the utility of systematic course evaluations in public engagement efforts related to biodiversity conservation.

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.

Seasonal variation of a plant-pollinator network in the Brazilian Cerrado: Implications for community structure and robustness.

Seasonal variation in the availability of floral hosts or pollinators is a key factor influencing diversity in plant-pollinator communities. In seasonally dry Neotropical habitats, where month-long periods of extreme drought are followed by a long rainy season, flowering is often synchronized with the beginning of precipitation, when environmental conditions are most beneficial for plant reproduction. In the Brazilian Cerrado, a seasonally dry ecosystem considered one of the world's biodiversity hotspots for angiosperms, plants with shallow root systems flower predominantly during the rainy season. Foraging activity in social bees however, the major pollinators in this biome, is not restricted to any particular season because a constant supply of resources is necessary to sustain their perennial colonies. Despite the Cerrado's importance as a center of plant diversity, the influence of its extreme cycles of drought and precipitation on the dynamics and stability of plant-pollinator communities is not well understood. We sampled plant-pollinator interactions of a Cerrado community weekly for one year and used network analyses to characterize intra-annual seasonal variation in community structure. We also compared seasonal differences in community robustness to species loss by simulating extinctions of plants and pollinators. We find that the community shrinks significantly in size during the dry season, becoming more vulnerable to disturbance due to the smaller pool of floral hosts available to pollinators during this period. Major changes in plant species composition but not in pollinators has led to high levels of turnover in plant-pollinator associations across seasons, indicated by in interaction dissimilarity (<3% of shared interactions). Aseasonal pollinators, which mainly include social bees and some solitary specialized bees, functioned as keystone species, maintaining robustness during periods of drastic changes in climatic conditions.

Landscape context differentially drives diet breadth for two key pollinator species.

An animal's diet contributes to its survival and reproduction. Variation in diet can alter the structure of community-level consumer-resource networks, with implications for ecological function. However, much remains unknown about the underlying drivers of diet breadth. Here we use a network approach to understand how consumer diet changes in response to local and landscape context and how these patterns compare between closely-related consumer species. We conducted field surveys to build 36 quantitative plant-pollinator networks using observation-based and pollen-based records of visitation across the gulf-coast cotton growing region of Texas, US. We focused on two key cotton pollinator species in the region: the social European honey bee, Apis mellifera, and the solitary native long-horned bee, Melissodes tepaneca. We demonstrate that diet breadth is highly context-dependent. Specifically, local factors better explain patterns of diet than regional factors for both species, but A. mellifera and M. tepaneca respond to local factors with contrasting patterns. Despite being collected directly from cotton blooms, both species exhibit significant preferences for non-cotton pollen, indicating a propensity to spend substantial effort foraging on remnant vegetation despite the rarity of these patches in the intensely managed cotton agroecosystem. Overall, our results demonstrate that diet is highly context- and species-dependent and thus an understanding of both factors is key for evaluating the conservation of important cotton pollinators.

Multi-scalar drivers of biodiversity: local management mediates wild bee community response to regional urbanization.

It is critical to understand the specific drivers of biodiversity across multiple spatial scales, especially within rapidly urbanizing areas, given the distinct management recommendations that may result at each scale. However, drivers of biodiversity patterns and interactions between drivers are often only measured and modeled at a single scale. In this study, we assessed bee community composition at three time periods in 20 grassland and 20 agriculture sites located across two major metroplexes. We examined how local environmental variables and surrounding landscape composition impact bee abundance, richness, and evenness, including comparisons between groups with different nesting strategies and body sizes. We collected nearly 13,000 specimens and identified 172 species. We found that levels of regional land use differentially impacted bee abundance and diversity depending on local habitat management. Specifically, within agriculture sites, bee richness was greater with increasing landscape-level seminatural habitat, while in grassland sites, bee richness was similar across landscapes regardless of seminatural habitat cover. Bee evenness at both site types declined with increasing landscape-level habitat heterogeneity, due to an increase of rare species at the grassland sites, but not in the agricultural sites, further indicating that diversity is driven by the interaction of local habitat quality and landscape-level habitat composition. We additionally found that agriculture sites supported higher abundances, but not richness, of small-bodied and below-ground nesting bees, while grassland sites supported higher abundances of aboveground nesting bees, and higher richness of large-bodied species. Increased levels of local bare ground were significantly related to multiple metrics of bee diversity, including greater belowground nesting bee abundance and richness. Local floral richness was also significantly related to increases of overall bee abundance, as well as the abundance and richness of small bees. Overall, we suggest that local land managers can support bee abundance and diversity by conserving areas of bare soil and promoting native floral diversity, the latter especially critical in highly urban agricultural spaces. Our results provide the first documentation of significant interactions between local habitat management and landscape composition impacting insect communities in urban systems, indicating that bee conservation practices depend critically on land use interactions across multiple spatial scales.

Flowers and Wild Megachilid Bees Share Microbes.

Transmission pathways have fundamental influence on microbial symbiont persistence and evolution. For example, the core gut microbiome of honey bees is transmitted socially and via hive surfaces, but some non-core bacteria associated with honey bees are also found on flowers, and these bacteria may therefore be transmitted indirectly between bees via flowers. Here, we test whether multiple flower and wild megachilid bee species share microbes, which would suggest that flowers may act as hubs of microbial transmission. We sampled the microbiomes of flowers (either bagged to exclude bees or open to allow bee visitation), adults, and larvae of seven megachilid bee species and their pollen provisions. We found a Lactobacillus operational taxonomic unit (OTU) in all samples but in the highest relative and absolute abundances in adult and larval bee guts and pollen provisions. The presence of the same bacterial types in open and bagged flowers, pollen provisions, and bees supports the hypothesis that flowers act as hubs of transmission of these bacteria between bees. The presence of bee-associated bacteria in flowers that have not been visited by bees suggests that these bacteria may also be transmitted to flowers via plant surfaces, the air, or minute insect vectors such as thrips. Phylogenetic analyses of nearly full-length 16S rRNA gene sequences indicated that the Lactobacillus OTU dominating in flower- and megachilid-associated microbiomes is monophyletic, and we propose the name Lactobacillus micheneri sp. nov. for this bacterium.

Taxonomic revision of Perdita subgenus Heteroperdita Timberlake (Hymenoptera: Andrenidae), with descriptions of two ant-like males.

Perdita subgenus Heteroperdita Timberlake, a distinctive subgenus of 22 species from the southwestern United States and adjacent Mexico, all specialists on Tiquilia (Boraginaceae), is revised. Nine new species are described: Perdita (Heteroperdita) desdemona Portman, sp. n., P. (H.) exusta Portman & Griswold, sp. n., P. (H.) hippolyta Portman & Griswold, sp. n. (male previously incorrectly described as P. pilonotata Timberlake), P. (H.) hooki Portman & Neff, sp. n., P. (H.) nuttalliae Portman, sp. n., P. (H.) prodigiosa Portman & Griswold, sp. n., P. (H.) sycorax Portman, sp. n., P. (H.) titania Portman & Griswold, sp. n., and P. (H.) yanegai Portman, sp. n. The following sexes are associated and described for the first time: the male of P. (H.) frontalis Timberlake, 1968, the female of P. (H.) optiva Timberlake, 1954, and the true male of P. (H.) pilonotata Timberlake, 1980. Perdita (H.) fasciatella Timberlake, 1980 is proposed as a junior synonym of P. (H.) sexfasciata Timberlake, 1954. A neotype is designated for P. (H.) pilonotata Timberlake, 1980. Two species in particular, P. prodigiosa and P. pilonotata, are sexually dimorphic with distinctive ant-like males. Information is presented on floral relationships, phenology, and geographic distribution. Identification keys for males and females are provided.

Phylogeny of the Callandrena subgenus of Andrena (Hymenoptera: Andrenidae) based on mitochondrial and nuclear DNA data: polyphyly and convergent evolution.

We propose a phylogenetic hypothesis of relationships within Callandrena, a North American subgenus of the bee genus Andrena, based on both mitochondrial and nuclear DNA sequences. Our data included 695 aligned base pairs comprising parts of the mitochondrial genes cytochrome oxidase subunits I and II and the intervening tRNA-leucine and 767 aligned base pairs of the F2 copy of the nuclear gene elongation factor-1alpha. We also suggest a preliminary hypothesis of relationships of the North American subgenera in the genus. Our analyses included 54 species of Callandrena, 42 species of Andrena representing 24 additional subgenera, and 11 outgroup species in the family Andrenidae. Parsimony analyses of each marker separately suggested that Callandrena was polyphyletic, with a combined analysis suggesting that there were at least two phylogenetically independent clades of bees with similar morphological features. Maximum likelihood and Bayesian analyses supported this conclusion, as did the non-parametric bootstrapping SOWH test. Convergence in morphological characters was likely due to their common use of members of Asteraceae as pollen hosts.

NESTMATE RELATEDNESS IN A COMMUNAL BEE, PERDITA TEXANA (HYMENOPTERA: ANDRENIDAE), BASED ON DNA FINGERPRINTING.

Perdita texana is a facultatively communal bee species with up to 28 females per nest. We used multilocus DNA fingerprinting to test the hypothesis that nestmates are more closely related to each other than are nonnestmates. The mean band sharing proportion among pairwise nestmate comparisons did not differ significantly from the mean among nonnestmate comparisons [P = 0.787 (df = 484)]. Although mean band sharing proportions did not differ among nestmates and nonnestmates, some nestmates show very high band sharing proportions (in excess of the upper 95% confidence limit for the nonnestmate mean). These individuals almost certainly are related, probably as half-sib sisters, however, they comprise a very small percentage of the nestmate populations. Our results indicate that kin selection is unlikely to play an important role in the evolution and maintenance of communal nesting. Communal societies most likely arise because of the mutualistic benefits of cooperative nesting, including accelerated nest founding and improved nest defense.