Müllerian mimicry among bees and wasps: a review of current knowledge and future avenues of research.

Many bees and stinging wasps, or aculeates, exhibit striking colour patterns or conspicuous coloration, such as black and yellow stripes. Such coloration is often interpreted as an aposematic signal advertising aculeate defences: the venomous sting. Aposematism can lead to Müllerian mimicry, the convergence of signals among different species unpalatable to predators. Müllerian mimicry has been extensively studied, notably on Neotropical butterflies and poison frogs. However, although a very high number of aculeate species harbour putative aposematic signals, aculeates are under-represented in mimicry studies. Here, we review the literature on mimicry rings that include bee and stinging wasp species. We report over a hundred described mimicry rings, involving a thousand species that belong to 19 aculeate families. These mimicry rings are found all throughout the world. Most importantly, we identify remaining knowledge gaps and unanswered questions related to the study of Müllerian mimicry in aculeates. Some of these questions are specific to aculeate models, such as the impact of sociality and of sexual dimorphism in defence levels on mimicry dynamics. Our review shows that aculeates may be one of the most diverse groups of organisms engaging in Müllerian mimicry and that the diversity of aculeate Müllerian mimetic interactions is currently under-explored. Thus, aculeates represent a new and major model system to study the evolution of Müllerian mimicry. Finally, aculeates are important pollinators and the global decline of pollinating insects raises considerable concern. In this context, a better understanding of the impact of Müllerian mimicry on aculeate communities may help design strategies for pollinator conservation, thereby providing future directions for evolutionary research.

Native and exotic plants play different roles in urban pollination networks across seasons.

Urban areas often host exotic plant species, whether managed or spontaneous. These plants are suspected of affecting pollinator diversity and the structure of pollination networks. However, in dense cityscapes, exotic plants also provide additional flower resources during periods of scarcity, and the consequences for the seasonal dynamics of networks still need to be investigated. For two consecutive years, we monitored monthly plant-pollinator networks in 12 green spaces in Paris, France. We focused on seasonal variations in the availability and attractiveness of flower resources, comparing native and exotic plants at both the species and community levels. We also considered their respective contributions to network properties over time (specialization and nestedness). Exotic plants provided more abundant and diverse flower resources than native plants, especially from late summer on. However, native plants received more visits and attracted more pollinator species at the community level; and during certain times of the year at the species level as well. Exotic plants were involved in more generalist interactions, increasingly so over the seasons. In addition, they contributed more to network nestedness than native plants. These results show that exotic plants are major components of plant-pollinator interactions in a dense urban landscape, even though they are less attractive than natives. They constitute a core of generalist interactions that increase nestedness and can participate in the overall stability of the network. However, most exotic species were seldom visited by insects. Pollinator communities may benefit from including more native species when managing urban green spaces.

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.

Keeping Up with Insect Pollinators in Paris.

There is growing interest in urban pollinator communities, although they may be subject to biotic homogenization in densely artificial landscapes. Paris (France) is one of the densest cities in the world, yet over the years many insect pollinator species have been reported there. We conducted in-depth surveys of Parisian green spaces for two years, in order to improve our knowledge of these assemblages. We explored several types of green spaces, monitoring pollinators throughout their activity season. We listed 118 species of wild bees and 37 species of hoverflies, updating pre-existing lists with 32 additional species. Bee assemblages showed functional diversity with 18.5% parasitic species and 17.7% oligolectic species. We also found several bee and hoverfly species under special conservation status. Over the study period, we observed seasonal succession of species, with diversified phenological niches. The greatest taxonomic and functional diversity was found in green spaces combining several habitats with ecological management. Despite its very dense urbanism, Paris is home to diverse pollinator communities. As a result, nearly half of the wild bee species of the wider Ile-de-France administrative region can be found within the city. This highlights the need to also consider dense urban environments in insect pollinator conservation strategies.

Using Matching Traits to Study the Impacts of Land-Use Intensification on Plant-Pollinator Interactions in European Grasslands: A Review.

Permanent grasslands are suitable habitats for many plant and animal species, among which are pollinating insects that provide a wide range of ecosystem services. A global crisis in pollination ecosystem service has been highlighted in recent decades, partly the result of land-use intensification. At the grassland scale, however, the underlying mechanisms of land-use intensification that affect plant-pollinator interactions and pollination remain understudied. In this review, we first synthesise the literature to provide new insights into the relationships between land-use intensification and pollination by using matching community and interaction traits. We then identify knowledge gaps and summarise how land-use intensification of grassland influences floral traits that may in turn be associated with modifications to pollinator matching traits. Last, we summarise how these modifications may affect pollination function on permanent grasslands. Overall, land-use intensification may lead to a shift in flower colour, a decrease in mean nectar tube depth and a decrease in reward production and pollen quality at the community level. This, in turn, may generate a decrease in pollinator mouthparts length and body size, that may favour pollinators that require a low amount of floral reward. We found no study citing the effect of land-use intensification on volatile organic compounds emitted by flowers despite the importance of these molecules in pollinator community composition. Overall, our review highlighted major knowledge gaps about the effects of land-use intensification on plant-pollinator interactions, and suggests that land-use intensification could favour plants with generalised floral traits that adversely affect pollination.

Seasonal Variations of Pollinator Assemblages among Urban and Rural Habitats: A Comparative Approach Using a Standardized Plant Community.

Even though urban green spaces may host a relatively high diversity of wild bees, urban environments impact the pollinator taxonomic and functional diversity in a way that is still misunderstood. Here, we provide an assessment of the taxonomic and functional composition of pollinator assemblages and their response to urbanization in the Paris region (France). We performed a spring-to-fall survey of insect pollinators in green spaces embedded in a dense urban matrix and in rural grasslands, using a plant setup standardized across sites and throughout the seasons. We compared pollinator species composition and the occurrence of bee functional traits over the two habitats. There was no difference in species richness between habitats, though urban assemblages were dominated by very abundant generalist species and displayed a lower evenness. They also included fewer brood parasitic, solitary or ground-nesting bees. Overall, bees tended to be larger in the city than in the semi-natural grasslands, and this trait exhibited seasonal variations. The urban environment filters out some life history traits of insect pollinators and alters their seasonal patterns, likely as a result of the fragmentation and scarcity of feeding and nesting resources. This could have repercussions on pollination networks and the efficiency of the pollination function.

Broader phenology of pollinator activity and higher plant reproductive success in an urban habitat compared to a rural one.

Urban habitat characteristics create environmental filtering of pollinator communities. They also impact pollinating insect phenology through the presence of an urban heat island and the year-round availability of floral resources provided by ornamental plants.Here, we monitored the phenology and composition of pollinating insect communities visiting replicates of an experimental plant assemblage comprising two species, with contrasting floral traits: Sinapis alba and Lotus corniculatus, whose flowering periods were artificially extended. Plant assemblage replicates were set up over two consecutive years in two different habitats: rural and densely urbanized, within the same biogeographical region (Ile-de-France region, France).The phenology of pollination activity, recorded from the beginning (early March) to the end (early November) of the season, differed between these two habitats. Several pollinator morphogroups (small wild bees, bumblebees, honeybees) were significantly more active on our plant sets in the urban habitat compared to the rural one, especially in early spring and autumn. This resulted in different overall reproductive success of the plant assemblage between the two habitats. Over the course of the season, reproductive success of S. alba was always significantly higher in the urban habitat, while reproductive success of L. corniculatus was significantly higher in the urban habitat only during early flowering.These findings suggest different phenological adaptations to the urban habitat for different groups of pollinators. Overall, results indicate that the broadened activity period of pollinating insects recorded in the urban environment could enhance the pollination function and the reproductive success of plant communities in cities.

Below-ground competition alters attractiveness of an insect-pollinated plant to pollinators.

Competitive interactions between plants can affect patterns of allocation to reproductive structures through modulation of resource availability. As floral traits involved in plant attractiveness to pollinators can be sensitive to these resources, competition with any neighbouring species may influence the attractiveness of insect-pollinated plants. While pollination research has primarily focused on above-ground interactions, this study aims at investigating if the presence of a competitor plant can modulate neighbouring insect-pollinated plant attractiveness to pollinators and resulting fecundity, especially through below-ground competitive interactions for soil resources. We set up a plot experiment in which we grew an insect-pollinated plant, Sinapis alba (Brassicaceae), in a mixture dominated by a wind-pollinated plant, Holcus lanatus (Poaceae). Individuals of S. alba were either subjected to or isolated from (with buried tubes in the soil) below-ground competition. Across the flowering season, floral traits involved in attractiveness of S. alba and pollinator visitation were followed at the plot and plant level to investigate different scales of attractiveness. At the end of the experiment, seeds were harvested to assess plant fecundity. Competition had a significant negative effect on plot and plant floral display size as well as flower size while nectar traits were not affected. When plants of S. alba were in competition, the time to first visit was altered: the proportion of plots that received a visit was smaller for a given time; in other words, it took more time for a given proportion of plots to be visited and some plots were even never visited. Moreover, pollinators made fewer visits per plots. The proportion of viable seeds produced by S. alba in competition was lower and probably linked to the competition itself rather than changes in pollinator visitation. This study suggests that competitive interactions between plants can modulate pollination interactions even when competing plant species are not insect-pollinated.

Wild pollinator activity negatively related to honey bee colony densities in urban context.

As pollinator decline is increasingly reported in natural and agricultural environments, cities are perceived as shelters for pollinators because of low pesticide exposure and high floral diversity throughout the year. This has led to the development of environmental policies supporting pollinators in urban areas. However, policies are often restricted to the promotion of honey bee colony installations, which resulted in a strong increase in apiary numbers in cities. Recently, competition for floral resources between wild pollinators and honey bees has been highlighted in semi-natural contexts, but whether urban beekeeping could impact wild pollinators remains unknown. Here, we show that in the city of Paris (France), wild pollinator visitation rates are negatively correlated to honey bee colony densities present in the surrounding landscape (500m -slope = -0.614; p = 0.001 -and 1000m -slope = -0.489; p = 0.005). Regarding the morphological groups of wild pollinators, large solitary bee and beetle visitation rates were negatively affected by honey bee colony densities within a 500m buffer (slope = -0.425, p = 0.007 and slope = - 0.671, p = 0.002, respectively) and bumblebee visitation rates were negatively affected by honey bee colony density within a 1000m buffer (slope = - 0.451, p = 0.012). Further, lower interaction evenness in plant-pollinator networks was observed with high honey bee colony density within a 1000m buffer (slope = -0.487, p = 0.008). Finally, honey bees tended to focus their foraging activity on managed rather than wild plant species (student t-test, p = 0.001) whereas wild pollinators equally visited managed and wild species. We advocate responsible practices mitigating the introduction of high density of honey bee colonies in urban environments. Further studies are however needed to deepen our knowledge about the potential negative interactions between wild and domesticated pollinators.

Buzz in Paris: flower production and plant-pollinator interactions in plants from contrasted urban and rural origins.

Urbanisation, associated with habitat fragmentation, affects pollinator communities and insect foraging behaviour. These biotic changes are likely to select for modified traits in insect-pollinated plants from urban populations compared to rural populations. To test this hypothesis, we conducted an experiment involving four plant species commonly found in both urban and rural landscapes of the Île-de-France region (France): Cymbalaria muralis, Geranium robertianum, Geum urbanum and Prunella vulgaris. The four species were grown in four urban and four rural experimental sites in 2015. For each species and each experimental site, plants were grown from seeds collected in five urban and five rural locations. During flowering, we observed flower production and insect-flower interactions during 14 weeks and tested for the effects of experimental site location and plant origin on flower production and on the number of floral visits. The study species had various flower morphology and hence were visited by different floral visitors. The effect of experimental sites and seed origin also varied among study species. We found that (1) insect visits on P. vulgaris were more frequent in rural than in urban sites; (2) for C. muralis, the slope relating the number of pollinator visits to the number of flowers per individual was steeper in urban versus rural sites, suggesting a greater benefit in allocating resources to flower production in urban conditions; (3) as a likely consequence, C. muralis tended to produce more flowers in plants from urban versus rural origin.

The proportion of impervious surfaces at the landscape scale structures wild bee assemblages in a densely populated region.

Given the predicted expansion of cities throughout the world, understanding the effect of urbanization on bee fauna is a major issue for the conservation of bees. The aim of this study was to understand how urbanization affects wild bee assemblages along a gradient of impervious surfaces and to determine the influence of landscape composition and floral resource availability on these assemblages. We chose 12 sites with a proportion of impervious surfaces (soil covered by parking, roads, and buildings) ranging from 0.06% to 64.31% within a 500 m radius. We collected using pan trapping and estimated the landscape composition of the sites within a 500 m radius and the species richness of plant assemblages within a 200 m radius. We collected 1104 bees from 74 species. The proportion of impervious surfaces at the landscape scale had a negative effect on wild bee abundance and species richness, whereas local flower composition had no effect. Ground-nesting bees were particularly sensitive to the urbanization gradient. This study provides new evidences of the impact of urbanization on bee assemblages and the proportion of impervious surfaces at the landscape scale emerged as a key factor that drives those assemblages.

Competition with wind-pollinated plant species alters floral traits of insect-pollinated plant species.

Plant traits related to attractiveness to pollinators (e.g. flowers and nectar) can be sensitive to abiotic or biotic conditions. Soil nutrient availability, as well as interactions among insect-pollinated plants species, can induce changes in flower and nectar production. However, further investigations are needed to determine the impact of interactions between insect-pollinated species and abiotically pollinated species on such floral traits, especially floral rewards. We carried out a pot experiment in which three insect-pollinated plant species were grown in binary mixtures with four wind-pollinated plant species, differing in their competitive ability. Along the flowering period, we measured floral traits of the insect-pollinated species involved in attractiveness to pollinators (i.e. floral display size, flower size, daily and total 1) flower production, 2) nectar volume, 3) amount of sucrose allocated to nectar). Final plant biomass was measured to quantify competitive interactions. For two out of three insect-pollinated species, we found that the presence of a wind-pollinated species can negatively impact floral traits involved in attractiveness to pollinators. This effect was stronger with wind-pollinated species that induced stronger competitive interactions. These results stress the importance of studying the whole plant community (and not just the insect-pollinated plant community) when working on plant-pollinator interactions.

Plant pollinator networks along a gradient of urbanisation.

BACKGROUND: Habitat loss is one of the principal causes of the current pollinator decline. With agricultural intensification, increasing urbanisation is among the main drivers of habitat loss. Consequently studies focusing on pollinator community structure along urbanisation gradients have increased in recent years. However, few studies have investigated how urbanisation affects plant-pollinator interaction networks. Here we assessed modifications of plant-pollinator interactions along an urbanisation gradient based on the study of their morphological relationships. METHODOLOGY/PRINCIPAL FINDINGS: Along an urbanisation gradient comprising four types of landscape contexts (semi-natural, agricultural, suburban, urban), we set up experimental plant communities containing two plant functional groups differing in their morphological traits ("open flowers" and "tubular flowers"). Insect visitations on these communities were recorded to build plant-pollinator networks. A total of 17 857 interactions were recorded between experimental plant communities and flower-visitors. The number of interactions performed by flower-visitors was significantly lower in urban landscape context than in semi-natural and agricultural ones. In particular, insects such as Syrphidae and solitary bees that mostly visited the open flower functional group were significantly impacted by urbanisation, which was not the case for bumblebees. Urbanisation also impacted the generalism of flower-visitors and we detected higher interaction evenness in urban landscape context than in agricultural and suburban ones. Finally, in urban context, these modifications lowered the potential reproductive success of the open flowers functional group. CONCLUSIONS/SIGNIFICANCE: Our findings show that open flower plant species and their specific flower-visitors are especially sensitive to increasing urbanisation. These results provide new clues to improve conservation measures within urbanised areas in favour of specialist flower-visitors. To complete this functional approach, studies using networks resolved to the species level along urbanised gradients would be required.

Association of highly and weakly mycorrhizal seedlings can promote the extra- and intraradical development of a common mycorrhizal network.

Arbuscular mycorrhizal fungi (AMF) are key determinants of plant interactions in ecosystems. Through their effects on competition, they are regulators of the structure of communities. Conversely, the composition of plant assemblages may also influence the AMF colonization dynamics of plant species. Here, we tested under in vitro culture conditions the effects of Medicago truncatula, a highly mycorrhizal plant species, and Silene vulgaris, a weakly mycorrhizal plant species, grown single (monospecies treatments) or in combination (bispecies treatment) on the colonization dynamics of the AMF Rhizophagus irregularis MUCL 43194. The seedlings were placed in a pre-established hyphal network developing from a mature M. truncatula mycorrhizal donor plant. Extraradical mycelium (ERM) and root colonization parameters as well as root morphology were measured over a period of 12 days. An increased ERM length, total root colonization and proportion of arbuscules were noted in the bispecies treatment. Conversely, the bispecies treatment seemed to have no effect on root growth. This study also demonstrated the suitability of the in vitro culture system for studying the interactions between AMF and host plants grown as mono- and bispecies combinations.

Conspecifics as informers and competitors: an experimental study in foraging bumble-bees.

Conspecifics are usually considered competitors negatively affecting food intake rates. However, their presence can also inform about resource quality by providing inadvertent social information. Few studies have investigated whether foragers perceive conspecifics as informers or competitors. Here, we experimentally tested whether variation in the density of demonstrators ('none', 'low' and 'high'), whose location indicated flower profitability, affected decision-making of bumble-bees Bombus terrestris. Bumble-bees foraged on either 'simple' (two colours) or 'complex' (four colours) artificial floral communities. We found that conspecifics at low density may be used as sources of information in first flower choices, whereas they appeared as competitors over the whole foraging sequence. Low conspecific densities improved foragers' first-visit success rate in the simple environment, and decreased time to first landing, especially in the complex environment. High conspecific densities did not affect these behavioural parameters, but reduced flower constancy in both floral communities, which may alter the efficiency of pollinating visits. These results suggest that the balance of the costs and benefits of conspecific presence varies with foraging experience, floral community and density. Spatio-temporal scales could thus be an important determinant of social information use. This behavioural flexibility should allow bumble-bees to better exploit their environment.

Are insect pollinators more generalist than insect herbivores?

Recent community-level studies have acknowledged that generalist species are more widespread than previously thought and highlighted their preponderant impact on community functioning and evolution. It is suggested that the type of interaction, trophic versus mutualistic, should affect species generalization level; however, no direct comparison has been made yet. Here, we performed such a comparison using 44 plant-insect networks describing either pollination or herbivory communities. Our analysis shows that the type of interaction does indeed have an impact on various aspects of species generalism, from the distribution of generalism in the community to the phylogenetic diversity of the plants with which a given insect species interacts. However, the amplitude of the observed differences depends on the aspect of species generalism studied. While the non-quantitative and quantitative measures of generalism suggest that pollinators interact with more plant species and more evenly than herbivores, phylogenetic measures clearly show that herbivores interact with plant species far more closely related to each other than pollinators. This comparative approach offers a promising perspective to better understand the functioning and evolution of multispecies assemblages by pointing out some fundamental singularities of communities depending on the type of interaction considered.

Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities.

Pollination is exclusively or mainly animal mediated for 70% to 90% of angiosperm species. Thus, pollinators provide an essential ecosystem service to humankind. However, the impact of human-induced biodiversity loss on the functioning of plant-pollinator interactions has not been tested experimentally. To understand how plant communities respond to diversity changes in their pollinating fauna, we manipulated the functional diversity of both plants and pollinators under natural conditions. Increasing the functional diversity of both plants and pollinators led to the recruitment of more diverse plant communities. After two years the plant communities pollinated by the most functionally diverse pollinator assemblage contained about 50% more plant species than did plant communities pollinated by less-diverse pollinator assemblages. Moreover, the positive effect of functional diversity was explained by a complementarity between functional groups of pollinators and plants. Thus, the functional diversity of pollination networks may be critical to ecosystem sustainability.

Limited seed dispersal and microspatial population structure of an agamospermous grass of West African savannahs, Hyparrhenia diplandra (Poaceae).

We studied the microspatial population structure of the perennial tussock grass, Hyparrhenia diplandra (Poaceae), a facultative agamospermous species of West African savannahs. The microspatial population structure of H. diplandra was investigated by choosing two 100-m(2); quadrats at random from which all individuals were mapped. The genotype of every individual was determined using two highly polymorphic microsatellite loci. A chloroplast locus was also used to investigate the role of seed dispersal on the genetic structure of populations. The genetic diversity index (0.85) was high for a clonal species. Significant genetic differentiation over short distances was detected by F statistics, and spatial autocorrelation analyses within both quadrats showed significant isolation-by-distance patterns, both with the cytoplasmic locus and the nuclear loci. Some clones formed large patches (up to 5 m in diameter) whereas others were more scattered. However, the genetic differentiation between quadrats was much higher when studied with the cytoplasmic locus than with the nuclear loci, indicating that gene flow via pollen, but not seeds, may frequently occur between quadrats. The maintenance of genetic diversity in this facultative agamospermous species most likely results from several factors, such as low seed dispersal ability, nonnegligible gene flow through pollen, and selective pressures induced by regularly occurring fires in this ecosystem.