Changing bee and hoverfly pollinator assemblages along an urban-rural gradient

Background

The potential for reduced pollination ecosystem service due to global declines of bees and other pollinators is cause for considerable concern. Habitat degradation, destruction and fragmentation due to agricultural intensification have historically been the main causes of this pollinator decline. However, despite increasing and accelerating levels of global urbanization, very little research has investigated the effects of urbanization on pollinator assemblages. We assessed changes in the diversity, abundance and species composition of bee and hoverfly pollinator assemblages in urban, suburban, and rural sites across a UK city.

Methodology/Principal Findings

Bees and hoverflies were trapped and netted at 24 sites of similar habitat character (churchyards and cemeteries) that varied in position along a gradient of urbanization. Local habitat quality (altitude, shelter from wind, diversity and abundance of flowers), and the broader-scale degree of urbanization (e.g. percentage of built landscape and gardens within 100 m, 250 m, 500 m, 1 km, and 2.5 km of the site) were assessed for each study site. The diversity and abundance of pollinators were both significantly negatively associated with higher levels of urbanization. Assemblage composition changed along the urbanization gradient with some species positively associated with urban and suburban land-use, but more species negatively so. Pollinator assemblages were positively affected by good site habitat quality, in particular the availability of flowering plants.

Conclusions/Significance

Our results show that urban areas can support diverse pollinator assemblages, but that this capacity is strongly affected by local habitat quality. Nonetheless, in both urban and suburban areas of the city the assemblages had fewer individuals and lower diversity than similar rural habitats. The unique development histories of different urban areas, and the difficulty of assessing mobile pollinator assemblages in just part of their range, mean that complementary studies in different cities and urban habitats are required to discover if these findings are more widely applicable.     

Decreasing Abundance,Increasing Diversity and Changing Structure of the Wild Bee Community (Hymenoptera: Anthophila) along an Urbanization Gradient

Background

Wild bees are important pollinators that have declined in diversity and abundance during the last decades. Habitat destruction and fragmentation associated with urbanization are reported as part of the main causes of this decline. Urbanization involves dramatic changes of the landscape, increasing the proportion of impervious surface while decreasing that of green areas. Few studies have investigated the effects of urbanization on bee communities. We assessed changes in the abundance, species richness, and composition of wild bee community along an urbanization gradient.

Methodology/Principal Findings

Over two years and on a monthly basis, bees were sampled with colored pan traps and insect nets at 24 sites located along an urbanization gradient. Landscape structure within three different radii was measured at each study site. We captured 291 wild bee species. The abundance of wild bees was negatively correlated with the proportion of impervious surface, while species richness reached a maximum at an intermediate (50%) proportion of impervious surface. The structure of the community changed along the urbanization gradient with more parasitic species in sites with an intermediate proportion of impervious surface. There were also greater numbers of cavity-nesting species and long-tongued species in sites with intermediate or higher proportion of impervious surface. However, urbanization had no effect on the occurrence of species depending on their social behavior or body size.

Conclusions/Significance

We found nearly a third of the wild bee fauna known from France in our study sites. Indeed, urban areas supported a diverse bee community, but sites with an intermediate level of urbanization were the most speciose ones, including greater proportion of parasitic species. The presence of a diverse array of bee species even in the most urbanized area makes these pollinators worthy of being a flagship group to raise the awareness of urban citizens about biodiversity.     

Ecological meta‐networks integrate spatial and temporal dynamics of plant–bumble bee interactions

Bumble bees can forage on a large number of wild plants and crops. The survival of a colony depends on the availability of suitable food resources within foraging range and throughout their forage season. We studied the spatial and temporal use of floral resources by bumble bees in a set of 30 local plant communities and used these data to model colony survival under different combinations of patch size and bumble bee flight distance. Floral resources vary spatially and temporally at the landscape level, and bumble bees track these resources across the landscape during the season. The simulation model showed that different patterns of resources availability could affect the survival and distribution of bumble bee nests across the landscape. This model can be used to generate hypotheses explaining bumble bee richness and abundance that can be tested in real landscapes. Integrating the spatial and temporal dynamics of the flower resources used by bumble bees provides a new perspective that can be used to inform bumble bee conservation, particularly in the context of their widespread decline in recent decades.     

Bumble bee abundance and richness improves honey bee pollination behaviour in sweet cherry

Pollination service in agricultural crops increases significantly with pollinator diversity and wild pollinator abundance. Differences in the foraging behaviour of pollinating insects are one of the reasons why pollinator diversity and abundance enhances crop pollination. Here, we focused on the foraging behaviour of honey bees and bumble bees in sweet cherry orchards. In addition, we studied the influence of bee diversity and abundance on the foraging behaviour of honey bees and bumble bees. Honey bees were found to visit fewer flowers than bumble bees. Bumble bees also showed a higher probability of changing trees between rows than honey bees. Both visitation rate and probability of row changes of honey bees increased with bumble bee diversity and with bumble bee abundance. We also found that the probability of row changes of honey bees increased with increasing bumble bee abundance. These effects of bumble bee richness and abundance on the pollination behaviour of honey bees can improve the pollination performance of honey bees in crops that depend on cross pollination. Our results highlight the higher pollination performance of bumble bees and the facilitative effect of wild pollinators to crop pollination.     

The Abundance and Pollen Foraging Behaviour of Bumble Bees in Relation to Population Size of Whortleberry (Vaccinium uliginosum)

Habitat fragmentation can have severe effects on plant pollinator interactions, for example changing the foraging behaviour of pollinators. To date, the impact of plant population size on pollen collection by pollinators has not yet been investigated. From 2008 to 2010, we monitored nine bumble bee species (Bombus campestris, Bombus hortorum s.l., Bombus hypnorum, Bombus lapidarius, Bombus pascuorum, Bombus pratorum, Bombus soroensis, Bombus terrestris s.l., Bombus vestalis s.l.) on Vaccinium uliginosum (Ericaceae) in up to nine populations in Belgium ranging in size from 80 m² to over 3.1 ha. Bumble bee abundance declined with decreasing plant population size, and especially the proportion of individuals of large bumble bee species diminished in smaller populations. The most remarkable and novel observation was that bumble bees seemed to switch foraging behaviour according to population size: while they collected both pollen and nectar in large populations, they largely neglected pollen collection in small populations. This pattern was due to large bumble bee species, which seem thus to be more likely to suffer from pollen shortages in smaller habitat fragments. Comparing pollen loads of bumble bees we found that fidelity to V. uliginosum pollen did not depend on plant population size but rather on the extent shrub cover and/or openness of the site. Bumble bees collected pollen only from three plant species (V. uliginosum, Sorbus aucuparia and Cytisus scoparius). We also did not discover any pollination limitation of V. uliginosum in small populations. We conclude that habitat fragmentation might not immediately threaten the pollination of V. uliginosum, nevertheless, it provides important nectar and pollen resources for bumble bees and declining populations of this plant could have negative effects for its pollinators. The finding that large bumble bee species abandon pollen collection when plant populations become small is of interest when considering plant and bumble bee conservation.     

Monitoring the conservation status of bumble bee populations across an elevation gradient in the Front Range of Colorado

Bumble bees are important pollinators of native flowers and crop plants. Consequently, declines in bumble bee populations in many regions around the globe are cause for concern. We monitored abundance of 22 bumble bee species at multiple elevations over 5 years in Boulder County, Colorado. While no declines in abundance of any species were apparent over the course of the study, such a finding does not preclude prior declines in abundance. This study provides current baseline abundance data that can be used for future monitoring projects.     

A contemporary survey of bumble bee diversity across the state of California

Bumble bees (genus Bombus) are important pollinators with more than 260 species found worldwide, many of which are in decline. Twenty‐five species occur in California with the highest species abundance and diversity found in coastal, northern, and montane regions. No recent studies have examined California bumble bee diversity across large spatial scales nor explored contemporary community composition patterns across the state. To fill these gaps, we collected 1740 bumble bee individuals, representing 17 species from 17 sites (~100 bees per site) in California, using an assemblage monitoring framework. This framework is intended to provide an accurate estimate of relative abundance of more common species without negatively impacting populations through overcollection. Our sites were distributed across six ecoregions, with an emphasis on those that historically hosted high bumble bee diversity. We compared bumble bee composition among these sites to provide a snapshot of California bumble bee biodiversity in a single year. Overall, the assemblage monitoring framework that we employed successfully captured estimated relative abundance of species for most sites, but not all. This shortcoming suggests that bumble bee biodiversity monitoring in California might require multiple monitoring approaches, including greater depth of sampling in some regions, given the variable patterns in bumble bee abundance and richness throughout the state. Our study sheds light on the current status of bumble bee diversity in California, identifies some areas where greater sampling effort and conservation action should be focused in the future, and performs the first assessment of an assembly monitoring framework for bumble bee communities in the state.     

Activity and abundance of bumble bees near Crested Butte,Colorado: diel,seasonal, and elevation effects

1. We revisited bumble bee survey data collected by Pyke in 1974 (Pyke, Ecology, 63 , 555–573, 1982) to evaluate seasonal changes in abundances of bumble bees and their floral resources, diel patterns of bumble bee activity, and elevation effects on plant and bumble bee phenology. 2. Bumble bee abundance increased during summer as spring queens founded colonies that produced workers, followed by males and autumn queens. The number of plant species visited by bumble bees increased to a peak in midsummer, then declined. 3. The number of bumble bees recorded per person‐hour peaked later than the number of flowering plant species used by the bees. Few autumn queens were observed. 4. Despite species differences in emergence times of spring queens, there were no apparent phenological differences among species in worker abundances. 5. Because flowering commences later at higher elevation, abundances of workers and males are also shifted later; therefore elevational comparisons must be seasonally adjusted. 6. These analyses provide basic information about important pollinating insects, and permit future investigations of elevational shifts over time to be properly adjusted for phenological and elevation effects in survey data.     

Reduced abundance and earlier collection of bumble bee workers under intensive cultivation of a mass‐flowering prairie crop

One of the most commonly seeded crops in Canada is canola, a cultivar of oilseed rape (Brassica napus). As a mass‐flowering crop grown intensively throughout the Canadian Prairies, canola has the potential to influence pollinator success across tens of thousands of square kilometers of cropland. Bumble bees (Bombus sp.) are efficient pollinators of many types of native and crop plants. We measured the influence of this mass‐flowering crop on the abundance and phenology of bumble bees, and on another species of social bee (a sweat bee; Halictus rubicundus), by continuously deploying traps at different levels of canola cultivation intensity, spanning the start and end of canola bloom. Queen bumble bees were more abundant in areas with more canola cover, indicating that this crop is attractive to queens. However, bumble bee workers were significantly fewer in these locations later in the season, suggesting reduced colony success. The median collection dates of workers of three bumble bee species were earlier near canola fields, suggesting a dynamic response of colonies to the increased floral resources. Different species experienced this shift to different extents. The sweat bee was not affected by canola cultivation intensity. Our findings suggest that mass‐flowering crops such as canola are attractive to bumble bee queens and therefore may lead to higher rates of colony establishment, but also that colonies established near this crop may be less successful. We propose that the effect on bumble bees can be mitigated by spacing the crop more evenly with respect to alternate floral resources.     

Floral resources,body size,and surrounding landscape influence bee community assemblages in oak‐savannah fragments

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Spillover of trap-nesting bees and wasps in an urban–rural interface

A mismatch of resource availability in certain periods can lead to spillover of insects between habitats, resulting in temporal differences in insect diversity. Urban gardens are important anthropogenic habitats but it is unknown whether, when and why spillover of beneficial insects occurs between gardens and agricultural habitats. We used trap nests for Hymenoptera to monthly monitor bee and wasp abundance and species richness in 12 gardens and 12 rapeseed fields. Half of the gardens and rapeseed fields were located in the urban–rural interface and bordered each other (a garden paired with a rapeseed field) and the other half were isolated in the rural landscape (isolated rapeseed fields) and in the urban city centre (isolated gardens). In general, gardens in the urban–rural interface comprised the highest richness of bees and wasps. The abundance of bees but not of wasps was highest in paired habitats and peaked at full rapeseed blooming, indicating that mass-flowering rapeseed offers foraging resources for bees nesting in adjacent gardens. Thus, bees nest and increase their populations in both areas, benefiting from the mass-flowering resource in the agricultural habitat as well as the nesting resources from gardens, suggesting spillover of bees but not of wasps between paired gardens and rapeseed fields. Our study highlights the value of gardens in the urban–rural interface for the biodiversity of functionally important insects. Implementing urban gardening and small-scale agriculture in cities and suburban habitats can promote local pollinator populations and benefit adjacent croplands.     

Floral resource pulse decreases bumble bee foraging trip duration in central Wisconsin agroecosystem

1. Resource pulses, narrow periods of high resource availability, can elicit strong behavioural responses across diverse taxa. Mass‐flowering agricultural crops are an example of a resource pulse that insect pollinators exploit. However, the underlying mechanism behind changes in pollinator behaviour associated with mass‐flowering crops is still relatively unexplored. 2. The present study quantified the behavioural response of bumble bees, an important wild pollinator, to commercial cranberry bloom, an important mass‐flowering crop in Wisconsin, U.S.A. Over a 2‐year period, foraging trip duration was measured using radio frequency identification at 14 farms situated across landscape contexts, ranging from high to low natural area (woodland amount). Using transect surveys, floral resource abundance at a landscape scale was estimated. 3. It was found that bumble bees were highly sensitive to temporal changes in landscape‐level resource abundance associated with the onset of cranberry bloom, during which they decreased foraging trip duration by 22% and increased the number of foraging trips during bloom by 24% on average relative to the period before and after bloom. This phenomenon was consistent across colonies, individual bees, and landscape contexts, despite a higher abundance of flowers in low woodland landscapes. Bumble bee colonies growing in low‐ and high‐woodland landscapes exhibited a similar performance. 4. As mass‐flowering crops are probably a factor influencing bumble bee foraging behaviour in agricultural regions, investigations should continue into how variable resource landscapes, particularly those offering resource pulses, affect wild pollinators and the pollination services they provide.     

The bee fauna of large parks in downtown Paris,France

In recent years, a growing number of studies have focused on the potential interest of urban green areas for supporting biodiversity. Private gardens, urban parks or green roofs may support relatively high densities of diverse wild bees. Knowledge is lacking regarding bee assemblages in Paris, the French capital, and one of the most densely populated part of France. In this context, we here provide a first assessment of the taxonomic and functional composition of bee assemblages in three urban parks in downtown Paris. Bees were sampled with a set of three coloured pan traps per park. Fifteen 24-hour sessions were performed from April to July 2011. We captured 425 specimens from 44 species representing five families and 11 genera. The assemblage was dominated by Halictidae (15 species representing 70.1% of total abundance), especially the eusocial species Lasioglossum morio that made 25.2% of total abundance. From a functional point of view, there were only two species of parasitic bees that made 1.2% of total abundance. Most non-parasitic species were polylectic and below-ground nesting. This study highlights the importance of preserving and managing urban parks and other green areas to promote the conservation of wild bees and ultimately the functionality of pollination service in urban ecosystems.     

Population genetics of wild and managed pollinators: implications for crop pollination and the genetic integrity of wild bees

Loss of habitat and chemical use associated with agriculture can cause population declines of wild pollinators. Less is known about the evolutionary consequences of interactions between species used in commercial agriculture and wild pollinators. Given population declines of many wild bee species, it is crucial to understand if commercial queens become established in natural areas, if wild bees visit agricultural fields and have the potential to interact with commercial bees, and if gene flow occurs between commercial and wild bees. We drew on a long-term data set that documents commercial bumble bee (Bombus impatiens) use in New England, and we conducted genetic analyses of foraging B. impatiens from areas with varying intensities of commercial bee use. In agricultural areas with a history of commercial bee use we also sampled bees directly from commercial hives. We found significant genetic differences among foraging B. impatiens and B. impatiens sampled directly from hives (average pairwise F′_ST = 0.14), but not among samples of foraging bees from natural areas (average F′_ST among foraging bees?=?0.002). Furthermore, Bayesian analysis of population structure revealed that foraging bees caught in areas with a history of commercial bee use grouped with samples from natural areas. These results document an agricultural setting where there was no widespread introgression of alleles from commercial bumble bees to wild bumble bees, commercial bumble bees did not become established in natural areas, and wild bees were providing pollination services to crops.     

High-altitude multi-taskers: bumble bee food plant use broadens along an altitudinal productivity gradient

We use an extensive historical data set on bumble bee host choice collected almost 50 years ago by L. W. Macior (Melanderia 15:1–59, 1974) to examine how resource partitioning by bumble bees varies over a 2,700-m altitudinal gradient at four hierarchical scales: individual, colony, species and community. Bumble bee behavior, resource overlap between castes, and plant-bumble bee networks change with altitude in accordance with tightening temporal constraints on flowering and colony growth in alpine habitats. Individual bees were more likely to collect pollen from multiple sources at high altitude. Between-caste foraging niche overlap increased with altitude. Similarly, alpine forager networks were more highly nested than either subalpine or montane networks due to increased asymmetric specialization. However, interspecific resource partitioning showed a more complex spatial pattern with low niche overlap at intermediate altitude (subalpine) compared to montane (disturbed) and alpine (unproductive) sites. Results suggest that spatial variation in interspecific resource partitioning is driven by a shift in the behavior of long-tongued bumble bees. Long-tongued bumble bees specialized in the subalpine but generalized in montane and alpine zones. Our reanalysis of Macior’s data shows that bumble bee behavior varies substantially with altitude influencing plant-bumble bee interaction networks. Results imply that pollination services to alpine host plants will change dramatically as subalpine species with unique foraging strategies move upward under global warming.     

Garden and Landscape-Scale Correlates of Moths of Differing Conservation Status: Significant Effects of Urbanization and Habitat Diversity

Moths are abundant and ubiquitous in vegetated terrestrial environments and are pollinators, important herbivores of wild plants, and food for birds, bats and rodents. In recent years, many once abundant and widespread species have shown sharp declines that have been cited by some as indicative of a widespread insect biodiversity crisis. Likely causes of these declines include agricultural intensification, light pollution, climate change, and urbanization; however, the real underlying cause(s) is still open to conjecture. We used data collected from the citizen science Garden Moth Scheme (GMS) to explore the spatial association between the abundance of 195 widespread British species of moth, and garden habitat and landscape features, to see if spatial habitat and landscape associations varied for species of differing conservation status. We found that associations with habitat and landscape composition were species-specific, but that there were consistent trends in species richness and total moth abundance. Gardens with more diverse and extensive microhabitats were associated with higher species richness and moth abundance; gardens near to the coast were associated with higher richness and moth abundance; and gardens in more urbanized locations were associated with lower species richness and moth abundance. The same trends were also found for species classified as increasing, declining and vulnerable under IUCN (World Conservation Union) criteria. However, vulnerable species were more strongly negatively affected by urbanization than increasing species. Two hypotheses are proposed to explain this observation: (1) that the underlying factors causing declines in vulnerable species (e.g., possibilities include fragmentation, habitat deterioration, agrochemical pollution) across Britain are the same in urban areas, but that these deleterious effects are more intense in urban areas; and/or (2) that urban areas can act as ecological traps for some vulnerable species of moth, the light drawing them in from the surrounding landscape into sub-optimal urban habitats.     

Molecular tools and bumble bees: revealing hidden details of ecology and evolution in a model system

Bumble bees are a longstanding model system for studies on behaviour, ecology and evolution, due to their well‐studied social lifestyle, invaluable role as wild and managed pollinators, and ubiquity and diversity across temperate ecosystems. Yet despite their importance, many aspects of bumble bee biology have remained enigmatic until the rise of the genetic and, more recently, genomic eras. Here, we review and synthesize new insights into the ecology, evolution and behaviour of bumble bees that have been gained using modern genetic and genomic techniques. Special emphasis is placed on four areas of bumble bee biology: the evolution of eusociality in this group, population‐level processes, large‐scale evolutionary relationships and patterns, and immunity and resistance to pesticides. We close with a prospective on the future of bumble bee genomics research, as this rapidly advancing field has the potential to further revolutionize our understanding of bumble bees, particularly in regard to adaptation and resilience. Worldwide, many bumble bee populations are in decline. As such, throughout the review, connections are drawn between new molecular insights into bumble bees and our understanding of the causal factors involved in their decline. Ongoing and potential applications to bumble bee management and conservation are also included to demonstrate how genetics‐ and genomics‐enabled research aids in the preservation of this threatened group.     

Are all urban green spaces a favourable habitat for pollinator communities? Bees,butterflies and hoverflies in different urban green areas

1. Urban ecosystems create suitable habitats for many plant and animal species, including pollinators. However, heterogenic habitats in city centres and suburban areas have various effects on pollinators due to variations in the composition of vegetation and in landscape management by humans. 2. This study compared the abundance and species richness of three main groups of pollinators – wild bees, butterflies, and hoverflies – in Poznań, western Poland, and in three different types of urban green areas – urban grasslands, urban parks, and green infrastructure in housing estates. 3. The total abundance of pollinators was higher in urban grasslands than in housing estates and urban parks. Species composition of pollinator communities differed between the three habitat types. 4. The study results showed that species richness and abundance of butterflies varied between habitat types, whereas no such differences were found in the case of wild bees and hoverflies. Cover of green area, vegetation structure, and plant height were important for the pollinator community; however, these variables had different effects depending on habitat type. 5. These findings revealed that not all urban green areas are equally valuable in terms of local biodiversity. High‐quality urban habitats such as urban grasslands are capable of supporting rich and abundant populations of pollinators. Therefore, it is important to protect high‐value urban green areas and simultaneously strive to improve intensively managed urban habitats through effective planning and new management practices.     

Foraging habitats and floral resource use by colonies of long- and short-tongued bumble bee species in an agricultural landscape with kabocha squash fields

Bumble bees pollinate and forage on flowers of crop and wild plants in agricultural landscapes. These interactions may depend on landscape patterns and bumble bee traits. We studied the abundance, colony density, and foraging range in long-tongued Bombus diversus Smith and short-tongued B. hypocrita Pérez, and evaluated their visits to flowers of wild plants and cultivated kabocha squash (Cucurbita maxima Duchesne). In forests in a farmland, B. hypocrita workers were trapped more frequently in the canopy. Full-sibs determined by nuclear microsatellite genotypes among workers collected in the farmland showed higher colony density and a larger foraging radius in B. hypocrita (30.8 km^?2 and 848 m) than in B. diversus (8.3 km^?2 and 723 m), respectively. Regarding wild plants, workers more frequently visited shallow flowers in B. hypocrita and deep flowers in B. diversus. These results suggest that bumble bees with different traits forage on different wild flowers in different habitats. Squash flowers were visited by both bumble bee species at similar frequency in the latter period of colony growth when males and new queens appeared. Composition of full-sib workers visiting squash and wild flowers did not depend on the number of collected workers of individual colonies, indicating that foraging on squash flowers was not associated with colony growth. Thus, growth and reproduction of bumble bee colonies may be supported by various wild plants and cultivated squash, respectively.     

Floral visitors in urban gardens and natural areas: Diversity and interaction networks in a neotropical urban landscape

Because cities concentrate 50% of the world’s population, and are experiencing a re-emergence of urban agriculture, we investigated the influences of urban agriculture and surrounding natural areas on floral visitors (bees, wasps, butterflies and flies) and plant species in San Cristóbal de Las Casas, Mexico.Throughout the frost, dry and rainy seasons of 2015, we sampled floral visitors in nine urban gardens and nine natural areas. We found 210 floral visitor species: 78% pollinators, 18% predators, and 4% florivores. Rarefaction curves showed that natural areas harbor significantly more floral visitor species (148) than home gardens (132). However, the differences in species composition between habitats and seasons highlight the need to view natural areas and home gardens as complementary habitats with which floral visitors interact in varying ways, during successive seasons, to meet different needs. Furthermore, mean species richness of floral visitors was influenced mainly by seasonality, and increased as seasons progressed from the dry, frost season to the rainy season. Nonetheless, some taxa were influenced by both season and habitat type. Floral visitor abundance was influenced by both habitat type and season, with home gardens showing higher abundance across seasons. Moreover, interaction networks for each season were more asymmetric in natural areas than in home gardens. Urban cover in the surrounding landscape influenced in a quadratic way the species number of floral visitors, but not their abundance. Thus, our results are evidence that natural areas surrounding cities and urban agriculture contribute to floral visitor communities and their networks.