Using physiology to better support wild bee conservation.

There is accumulating evidence that wild bees are experiencing a decline in terms of species diversity, abundance or distribution, which leads to major concerns about the sustainability of both pollination services and intrinsic biodiversity. There is therefore an urgent need to better understand the drivers of their decline, as well as design conservation strategies. In this context, the current approach consists of linking observed occurrence and distribution data of species to environmental features. While useful, a highly complementary approach would be the use of new biological metrics that can link individual bee responses to environmental alteration with population-level responses, which could communicate the actual bee sensitivity to environmental changes and act as early warning signals of bee population decline or sustainability. We discuss here through several examples how the measurement of bee physiological traits or performance can play this role not only in better assessing the impact of anthropogenic pressures on bees, but also in guiding conservation practices with the help of the documentation of species' physiological needs. Last but not least, because physiological changes generally occur well in advance of demographic changes, we argue that physiological traits can help in predicting and anticipating future population trends, which would represent a more proactive approach to conservation. In conclusion, we believe that future efforts to combine physiological, ecological and population-level knowledge will provide meaningful contributions to wild bee conservation-based research.

Nile blue as reporter dye in salt aggregation based-colorimetric aptasensors for peptide, small molecule and metal ion detection.

Herein, we report a novel approach for the design of a colorimetric aptasensor, relying on a Dye Salt Aggregation-based Colorimetric Oligonucleotide assay (DYSACO assay). This method is based on the use of an intercalating agent, Nile Blue (NB), whose aggregation capacities (and thus modification of its absorption spectrum) are drastically amplified by adding salts to the working solution. The presence of an aptamer could protect NB from such aggregation process due to its intercalation into double-stranded DNA and/or interaction with nucleobases. In response to the addition of the specific ligand, the competition between NB and the target for binding to the aptamer occurs, resulting in an increase in the dye salt aggregation and then in the blue-to-blank color change of the solution. The proof-of-principle was demonstrated by employing the anti-l-tyrosinamide aptamer and the assay was successfully applied to the trace enantiomer detection, allowing the detection of an enantiomeric impurity down to approximately 2% in a non-racemic sample. Through a reversed mechanism based on the increased capture of NB by DNA upon analyte binding, the sensing platform was further demonstrated for the Hg(II) detection. Water samples of different origin were spiked with Hg(II) analyte at final range concentrations comprised between (0.5-15 µM). An excellent overall recovery of 122 ± 14%; 105 ± 14%; 99 ± 9%; was respectively obtained from river, tap and mineral water, suggesting that the sensor can be used under real sample conditions. The assay was also shown to work for sensing the ochratoxin A and d-arginine vasopressin compounds, revealing its simplicity and generalizability potentialities.

A large-scale dataset reveals taxonomic and functional specificities of wild bee communities in urban habitats of Western Europe.

Wild bees are declining, mainly due to the expansion of urban habitats that have led to land-use changes. Effects of urbanization on wild bee communities are still unclear, as shown by contrasting reports on their species and functional diversities in urban habitats. To address this current controversy, we built a large dataset, merging 16 surveys carried out in 3 countries of Western Europe during the past decades, and tested whether urbanization influences local wild bee taxonomic and functional community composition. These surveys encompassed a range of urbanization levels, that were quantified using two complementary metrics: the proportion of impervious surfaces and the human population density. Urban expansion, when measured as a proportion of impervious surfaces, but not as human population density, was significantly and negatively correlated with wild bee community species richness. Taxonomic dissimilarity of the bee community was independent of both urbanization metrics. However, occurrence rates of functional traits revealed significant differences between lightly and highly urbanized communities, for both urbanization metrics. With higher human population density, probabilities of occurrence of above-ground nesters, generalist and small species increased. With higher soil sealing, probabilities of occurrence of above-ground nesters, generalists and social bees increased as well. Overall, these results, based on a large European dataset, suggest that urbanization can have negative impacts on wild bee diversity. They further identify some traits favored in urban environments, showing that several wild bee species can thrive in cities.

Pesticide risk assessment in honeybees: Toward the use of behavioral and reproductive performances as assessment endpoints.

The growing gap between new evidence of pesticide toxicity in honeybees and conventional toxicological assays recommended by regulatory test guidelines emphasizes the need to complement current lethal endpoints with sublethal endpoints. In this context, behavioral and reproductive performances have received growing interest since the 2000s, likely due to their ecological relevance and/or the emergence of new technologies. We review the biological interests and methodological measurements of these predominantly studied endpoints and discuss their possible use in the pesticide risk assessment procedure based on their standardization level, simplicity and ecological relevance. It appears that homing flights and reproduction have great potential for pesticide risk assessment, mainly due to their ecological relevance. If exploratory research studies in ecotoxicology have paved the way toward a better understanding of pesticide toxicity in honeybees, the next objective will then be to translate the most relevant behavioral and reproductive endpoints into regulatory test methods. This will require more comparative studies and improving their ecological relevance. This latter goal may be facilitated by the use of population dynamics models for scaling up the consequences of adverse behavioral and reproductive effects from individuals to colonies.

Possible Spillover of Pathogens between Bee Communities Foraging on the Same Floral Resource.

Viruses are known to contribute to bee population decline. Possible spillover is suspected from the co-occurrence of viruses in wild bees and honey bees. In order to study the risk of virus transmission between wild and managed bee species sharing the same floral resource, we tried to maximize the possible cross-infections using Phacelia tanacetifolia, which is highly attractive to honey bees and a broad range of wild bee species. Virus prevalence was compared over two years in Southern France. A total of 1137 wild bees from 29 wild bee species (based on COI barcoding) and 920 honey bees (Apis mellifera) were checked for the seven most common honey bee RNA viruses. Halictid bees were the most abundant. Co-infections were frequent, and Sacbrood virus (SBV), Black queen cell virus (BQCV), Acute bee paralysis virus (ABPV) and Israeli acute paralysis virus (IAPV) were widespread in the hymenopteran pollinator community. Conversely, Deformed wing virus (DWV) was detected at low levels in wild bees, whereas it was highly prevalent in honey bees (78.3% of the samples). Both wild bee and honey bee virus isolates were sequenced to look for possible host-specificity or geographical structuring. ABPV phylogeny suggested a specific cluster for Eucera bees, while isolates of DWV from bumble bees (Bombus spp.) clustered together with honey bee isolates, suggesting a possible spillover.

Measuring ontogenetic shifts in central-place foragers: A case study with honeybees.

Measuring time-activity budgets over the complete individual life span is now possible for many animals with the recent advances of life-long individual monitoring devices. Although analyses of changes in the patterns of time-activity budgets have revealed ontogenetic shifts in birds or mammals, no such technique has been applied to date on insects. We tested an automated breakpoint-based procedure to detect, assess and quantify shifts in the temporal pattern of the flight activities in honeybees. We assumed that the learning and foraging stages of honeybees will differ in several respects, to detect the age at onset of foraging (AOF). Using an extensive dataset covering the life-long monitoring of 1,167 individuals, we compared the AOF outputs with the more conventional approaches based on arbitrary thresholds. We further evaluated the robustness of the different methods comparing the foraging time-activity budget allocations between the presumed foragers and confirmed foragers. We revealed a clear-cut learning-foraging ontogenetic shift that differs in duration, frequency and time of occurrence of flights. Although AOF appeared to be highly plastic among bees, the breakpoint-based procedure seems better capable to detect it than arbitrary threshold-based methods that are unable to deal with inter-individual variation. We developed the aof r-package including a broad range of examples with both simulated and empirical datasets to illustrate the simplicity of use of the procedure. This simple procedure is generic enough to be derived from any individual life-long monitoring devices recording the time-activity budgets, and could propose new ecological applications of bio-logging to detect ontogenetic shifts in the behaviour of central-place foragers.

Neonicotinoid-induced mortality risk for bees foraging on oilseed rape nectar persists despite EU moratorium.

The implication of neonicotinoids in bee declines led in 2013 to an EU moratorium on three neonicotinoids in bee-attractive crops. However, neonicotinoids are frequently detected in wild flowers or untreated crops suggesting that neonicotinoids applied to cereals can spread into the environment and harm bees. Therefore, we quantified neonicotinoid residues in nectar from winter-sown oilseed rape in western France collected within the five years under the EU moratorium. We detected all three restricted neonicotinoids. Imidacloprid was detected in all years with no clear declining trend but a strong inter- and intra-annual variation and maximum concentrations exceeding reported concentrations in treated crops. No relation to non-organic winter-sown cereals was identified even though these were the only crops treated with imidacloprid, but residue levels depended on soil type and increased with rainfall. Simulating acute and chronic mortality suggests a considerable risk for nectar foraging bees. We conclude that persistent imidacloprid soil residues diffuse on a large scale in the environment and substantially contaminate a major mass-flowering crop. Despite the limitations of case-studies and risk simulations, our findings provide additional support to the recent extension of the moratorium to a permanent ban in all outdoor crops.

Toward the protection of bees and pollination under global change: present and future perspectives in a challenging applied science.

Over the past 30 years (1987-2016), bibliometric data have shown a drastic change in the scientific investigation of threats to bee populations. Bee research efforts committed to studying bioagressors of honeybees (mainly Varroa sp.) were predominant, but now appear to be shifting from bioagressors to global change in the published literature. This rise of global change science reveals prevailing topics, for current and future years: climate change, landscape alteration, agricultural intensification and invasive species. We argue that with increased investment in applied research and development, the scientific, beekeeping and agricultural communities will be able to find management strategies for productive agrosystems and enhanced resilience of pollination and beekeeping. This implies the need for restoring and improving food resources and shelters of bees by ecological intensification of diversified farming systems, and also reconciling sustainable beekeeping with wild pollinator conservation.

FragSAD: A database of diversity and species abundance distributions from habitat fragments.

Habitat destruction is the single greatest anthropogenic threat to biodiversity. Decades of research on this issue have led to the accumulation of hundreds of data sets comparing species assemblages in larger, intact, habitats to smaller, more fragmented, habitats. Despite this, little synthesis or consensus has been achieved, primarily because of non-standardized sampling methodology and analyses of notoriously scale-dependent response variables (i.e., species richness). To be able to compare and contrast the results of habitat fragmentation on species' assemblages, it is necessary to have the underlying data on species abundances and sampling intensity, so that standardization can be achieved. To accomplish this, we systematically searched the literature for studies where abundances of species in assemblages (of any taxa) were sampled from many habitat patches that varied in size. From these, we extracted data from several studies, and contacted authors of studies where appropriate data were collected but not published, giving us 117 studies that compared species assemblages among habitat fragments that varied in area. Less than one-half (41) of studies came from tropical forests of Central and South America, but there were many studies from temperate forests and grasslands from all continents except Antarctica. Fifty-four of the studies were on invertebrates (mostly insects), but there were several studies on plants (15), birds (16), mammals (19), and reptiles and amphibians (13). We also collected qualitative information on the length of time since fragmentation. With data on total and relative abundances (and identities) of species, sampling effort, and affiliated meta-data about the study sites, these data can be used to more definitively test hypotheses about the role of habitat fragmentation in altering patterns of biodiversity. There are no copyright restrictions. Please cite this data paper and the associated Dryad data set if the data are used in publications.

Hazard of a neonicotinoid insecticide on the homing flight of the honeybee depends on climatic conditions and Varroa infestation.

The paradigm for all toxicological bioassays in the risk assessment of pesticide registration reflects the principle that experimental conditions should be controlled to avoid any other factors that may affect the endpoint measures. As honeybee colonies can be frequently exposed to bio-aggressors in real conditions, often concomitantly with pesticides, co-exposure to pesticide/bio-aggressors is becoming a concern for regulatory authorities. We investigated the effects of the neonicotinoid insecticide thiamethoxam on the homing performances of foragers emerging from colonies differentiated by health status (infestation with Varroa destructor mites, microsporidian parasite Nosema spp. and Deformed Wing Virus). We designed a homing test that has been recently identified to fill a regulatory gap in the field evaluations of sublethal doses of pesticides before their registration. We also assessed the effect of temperature as an environmental factor. Our results showed that the Varroa mite exacerbates homing failure (HF) caused by the insecticide, whereas high temperatures reduce insecticide-induced HF. Through an analytical Effective Dose (ED) approach, predictive modeling results showed that, for instance, ED level of an uninfested colony, can be divided by 3.3 when the colony is infested by 5 Varroa mites per 100 bees and at a temperature of 24 °C. Our results suggest that the health status of honeybee colonies and climatic context should be targeted for a thorough risk assessment.

Controlling the impact of the managed honeybee on wild bees in protected areas.

In recent years, conservation biologists have raised awareness about the risk of ecological interference between massively introduced managed honeybees and the native wild bee fauna in protected natural areas. In this study, we surveyed wild bees and quantified their nectar and pollen foraging success in a rosemary Mediterranean scrubland in southern France, under different conditions of apiary size and proximity. We found that high-density beekeeping triggers foraging competition which depresses not only the occurrence (-55%) and nectar foraging success (-50%) of local wild bees but also nectar (-44%) and pollen (-36%) harvesting by the honeybees themselves. Overall, those competition effects spanned distances of 600-1.100 m around apiaries, i.e. covering 1.1-3.8km2 areas. Regardless the considered competition criterion, setting distance thresholds among apiaries appeared more tractable than setting colony density thresholds for beekeeping regulation. Moreover, the intraspecific competition among the honeybees has practical implications for beekeepers. It shows that the local carrying capacity has been exceeded and raises concerns for honey yields and colony sustainability. It also offers an effective ecological criterion for pragmatic decision-making whenever conservation practitioners envision progressively reducing beekeeping in protected areas. Although specific to the studied area, the recommendations provided here may help raise consciousness about the threat high-density beekeeping may pose to local nature conservation initiatives, especially in areas with sensitive or endangered plant or bee species such as small oceanic islands with high levels of endemism.

A 'Landscape physiology' approach for assessing bee health highlights the benefits of floral landscape enrichment and semi-natural habitats.

Understanding how anthropogenic landscape alteration affects populations of ecologically- and economically-important insect pollinators has never been more pressing. In this context, the assessment of landscape quality typically relies on spatial distribution studies, but, whether habitat-restoration techniques actually improve the health of targeted pollinator populations remains obscure. This gap could be filled by a comprehensive understanding of how gradients of landscape quality influence pollinator physiology. We therefore used this approach for honey bees (Apis mellifera) to test whether landscape patterns can shape bee health. We focused on the pre-wintering period since abnormally high winter colony losses have often been observed. By exposing colonies to different landscapes, enriched in melliferous catch crops and surrounded by semi-natural habitats, we found that bee physiology (i.e. fat body mass and level of vitellogenin) was significantly improved by the presence of flowering catch crops. Catch crop presence was associated with a significant increase in pollen diet diversity. The influence of semi-natural habitats on bee health was even stronger. Vitellogenin level was in turn significantly linked to higher overwintering survival. Therefore, our experimental study, combining landscape ecology and bee physiology, offers an exciting proof-of-concept for directly identifying stressful or suitable landscapes and promoting efficient pollinator conservation.

Small molecule aptamer assays based on fluorescence anisotropy signal-enhancer oligonucleotides.

Herein, we design novel fluorescence anisotropy (FA) aptamer sensing platforms dedicated to small molecule detection. The assay strategy relied on enhanced fluctuations of segmental motion dynamics of the aptamer tracer mediated by an unlabelled, partially complementary oligonucleotide. The signal-enhancer oligonucleotide (SEO) essentially served as a free probe fraction revealer. By targeting specific regions of the signalling functional nucleic acid, the SEO binding to the unbound aptamer triggered perturbations of both the internal DNA flexibility and the localized dye environment upon the free probe to duplex structure transition. This potentiating effect determined increased FA variations between the duplex and target bound states of the aptameric probe. FA assay responses were obtained with both pre-structured (adenosine) and unstructured (tyrosinamide) aptamers and with dyes of different photochemical properties (fluorescein and texas red). The multiplexed analysis ability was further demonstrated through the simultaneous multicolour detection of the two small targets. The FA method appears to be especially simple, sensitive and widely applicable.

A Locomotor Deficit Induced by Sublethal Doses of Pyrethroid and Neonicotinoid Insecticides in the Honeybee Apis mellifera.

The toxicity of pesticides used in agriculture towards non-targeted organisms and especially pollinators has recently drawn the attention from a broad scientific community. Increased honeybee mortality observed worldwide certainly contributes to this interest. The potential role of several neurotoxic insecticides in triggering or potentiating honeybee mortality was considered, in particular phenylpyrazoles and neonicotinoids, given that they are widely used and highly toxic for insects. Along with their ability to kill insects at lethal doses, they can compromise survival at sublethal doses by producing subtle deleterious effects. In this study, we compared the bee's locomotor ability, which is crucial for many tasks within the hive (e.g. cleaning brood cells, feeding larvae…), before and after an acute sublethal exposure to one insecticide belonging to the two insecticide classes, fipronil and thiamethoxam. Additionally, we examined the locomotor ability after exposure to pyrethroids, an older chemical insecticide class still widely used and known to be highly toxic to bees as well. Our study focused on young bees (day 1 after emergence) since (i) few studies are available on locomotion at this stage and (ii) in recent years, pesticides have been reported to accumulate in different hive matrices, where young bees undergo their early development. At sublethal doses (SLD48h, i.e. causing no mortality at 48 h), three pyrethroids, namely cypermethrin (2.5 ng/bee), tetramethrin (70 ng/bee), tau-fluvalinate (33 ng/bee) and the neonicotinoid thiamethoxam (3.8 ng/bee) caused a locomotor deficit in honeybees. While the SLD48h of fipronil (a phenylpyrazole, 0.5 ng/bee) had no measurable effect on locomotion, we observed high mortality several days after exposure, an effect that was not observed with the other insecticides. Although locomotor deficits observed in the sublethal range of pyrethroids and thiamethoxam would suggest deleterious effects in the field, the case of fipronil demonstrates that toxicity evaluation requires information on multiple endpoints (e.g. long term survival) to fully address pesticides risks for honeybees. Pyrethroid-induced locomotor deficits are discussed in light of recent advances regarding their mode of action on honeybee ion channels and current structure-function studies.

Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees.

European governments have banned the use of three common neonicotinoid pesticides due to insufficiently identified risks to bees. This policy decision is controversial given the absence of clear consistency between toxicity assessments of those substances in the laboratory and in the field. Although laboratory trials report deleterious effects in honeybees at trace levels, field surveys reveal no decrease in the performance of honeybee colonies in the vicinity of treated fields. Here we provide the missing link, showing that individual honeybees near thiamethoxam-treated fields do indeed disappear at a faster rate, but the impact of this is buffered by the colonies' demographic regulation response. Although we could ascertain the exposure pathway of thiamethoxam residues from treated flowers to honeybee dietary nectar, we uncovered an unexpected pervasive co-occurrence of similar concentrations of imidacloprid, another neonicotinoid normally restricted to non-entomophilous crops in the study country. Thus, its origin and transfer pathways through the succession of annual crops need be elucidated to conveniently appraise the risks of combined neonicotinoid exposures. This study reconciles the conflicting laboratory and field toxicity assessments of neonicotinoids on honeybees and further highlights the difficulty in actually detecting non-intentional effects on the field through conventional risk assessment methods.

Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds.

In intensive farmland habitats, pollination of wild flowers and crops may be threatened by the widespread decline of pollinators. The honey bee decline, in particular, appears to result from the combination of multiple stresses, including diseases, pathogens, and pesticides. The reduction of semi-natural habitats is also suspected to entail floral resource scarcity for bees. Yet, the seasonal dynamics and composition of the honey bee diet remains poorly documented to date. In this study, we studied the seasonal contribution of mass-flowering crops (rapeseed and sunflower) vs. other floral resources, as well as the influence of nutritional quality and landscape composition on pollen diet composition over five consecutive years. From April to October, the mass of pollen and nectar collected by honey bees followed a bimodal seasonal trend, marked by a two-month period of low food supply between the two oilseed crop mass-flowerings (ending in May for rapeseed and July for sunflower). Bees collected nectar mainly from crops while pollen came from a wide diversity of herbaceous and woody plant species in semi-natural habitats or from weeds in crops. Weed species constituted the bulk of the honey bee diet between the mass flowering crop periods (up to 40%) and are therefore suspected to play a critical role at this time period. The pollen diet composition was related to the nutritional value of the collected pollen and by the local landscape composition. Our study highlights (1) a food supply depletion period of both pollen and nectar resources during late spring, contemporaneously with the demographic peak of honey bee populations, (2) a high botanical richness of pollen diet, mostly proceeding from trees and weeds, and (3) a pollen diet composition influenced by the local landscape composition. Our results therefore support the Agri-Environmental Schemes intended to promote honey bees and beekeeping sustainability through the enhancement of flower availability in agricultural landscapes.

Delivery of crop pollination services is an insufficient argument for wild pollinator conservation.

There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.

Species undersampling in tropical bat surveys: effects on emerging biodiversity patterns.

Undersampling is commonplace in biodiversity surveys of species-rich tropical assemblages in which rare taxa abound, with possible repercussions for our ability to implement surveys and monitoring programmes in a cost-effective way. We investigated the consequences of information loss due to species undersampling (missing subsets of species from the full species pool) in tropical bat surveys for the emerging patterns of species richness (SR) and compositional variation across sites. For 27 bat assemblage data sets from across the tropics, we used correlations between original data sets and subsets with different numbers of species deleted either at random, or according to their rarity in the assemblage, to assess to what extent patterns in SR and composition in data subsets are congruent with those in the initial data set. We then examined to what degree high sample representativeness (r ≥ 0·8) was influenced by biogeographic region, sampling method, sampling effort or structural assemblage characteristics. For SR, correlations between random subsets and original data sets were strong (r ≥ 0·8) with moderate (ca. 20%) species loss. Bias associated with information loss was greater for species composition; on average ca. 90% of species in random subsets had to be retained to adequately capture among-site variation. For nonrandom subsets, removing only the rarest species (on average c. 10% of the full data set) yielded strong correlations (r > 0·95) for both SR and composition. Eliminating greater proportions of rare species resulted in weaker correlations and large variation in the magnitude of observed correlations among data sets. Species subsets that comprised ca. 85% of the original set can be considered reliable surrogates, capable of adequately revealing patterns of SR and temporal or spatial turnover in many tropical bat assemblages. Our analyses thus demonstrate the potential as well as limitations for reducing survey effort and streamlining sampling protocols, and consequently for increasing the cost-effectiveness in tropical bat surveys or monitoring programmes. The dependence of the performance of species subsets on structural assemblage characteristics (total assemblage abundance, proportion of rare species), however, underscores the importance of adaptive monitoring schemes and of establishing surrogate performance on a site by site basis based on pilot surveys.

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.