Pollinator-plant interactions as basis for entomovectoring

Pollinator-plant interactions as basis for entomovectoringPollinator declines and pollination deficits are aggravated by climate change, pesticide load on agricultural environments, and other factors.  Can we secure food production if these trends continue? Basic knowledge about pollinator behaviour and ecology are accumulating, but also need to be taken in use. Arthropod-Plant Interactions has published an impressive collection of cutting edge science to increase our understanding of plant-pollinator interactions. 

In this Virtual Special Issue curated by Ingeborg Menzler-Hokkanen, Arthropod-Plant Interactions Managing Editor, we wish to highlight these advances, in particular as a basis for entomovectoring, i.e. using insects to vector beneficial organisms (usually biocontrol agents for crop protection) to flowers, or sometimes other plant parts such as leaves1,2. Basic research on entomovectoring is very scattered, and we wish to encourage further research to engage in exploiting this powerful technology for the dual purpose of safe, targeted biological crop protection, and improved pollination at the same time. The articles curated in this Virtual Special Issue have been divided into five topics: 

  • Flower visitation dynamics
  • Night pollination
  • External factors affecting plant-pollinator interactions
  • Bee foraging and flower handling behaviour
  • Vision and learning in bees

We hope you enjoy reading this virtual issue.

Acknowledgement: The support provided by the Institut Francais de Finlande, the Embassy of France in Finland, the French Ministry of Higher Education, Research and Innovation and the Finnish Society of Science and Letters is acknowledged in organising and co-financing an international workshop on entomovectoring. Our thanks to the Maupertuis Programme. This Virtual Special Issue lays the foundation to the entomovectoring workshop.
1 Hokkanen HMT & Menzler-Hokkanen I. (2007). Use of honeybees in the biological control of plant diseases. Entomol Res 37 (Suppl. 1), A62-A63.
2 Menzler-Hokkanen I, Hokkanen HMT (2017). Entomovectoring: an agroecological practice of using bees for biocontrol. In: Wezel, A. (Ed.), Agroecological Practices for Sustainable Agriculture. World Scientific Publishing Europe, London. pp. 183-199.

Flower visitation dynamics

Flower visitation dynamics
8 articles

Visitor or vector? The extent of rove beetle (Coleoptera: Staphylinidae) pollination and floral interactions

Thomas D. J. Sayers, Martin J. Steinbauer & Rebecca E. Miller     |     Review Paper     |     Published: 16 April 2019

Abstract: Beetles (Coleoptera) are a diverse group of overlooked pollinators, considered particularly important in tropical ecosystems. The role of the most diverse beetle family, Staphylinidae, as pollinators is generally considered minor, yet their relationships with plants are mostly unknown. Although often referred to as opportunistic visitors, it is arguable that the true extent of rove beetle pollination is underestimated given their frequency of visitation to flowers. This review comprehensively analysed the plant–pollinator or visitor interactions of the Staphylinidae and uncovered 108 well-described staphylinid–flower interactions across 27 seed plant families. Of these interactions, Staphylinidae were considered either potential or conclusive pollinators for 56 plant species, having either a primary or secondary role in pollination. Conversely, Staphylinidae were visitors to 40 plant species with a negligible role in pollination. For the remaining 12 interactions and additional anecdotal reports, the role of staphylinids as pollinators was unresolved. Staphylinid–flower interactions were most prevalent in the monocots and magnoliids (families: Araceae, Annonaceae, Arecaceae, and Magnoliaceae) involving predominantly generalist pollination systems, and interactions were limited to six staphylinid subfamilies (Omaliinae, Tachyporinae, Aleocharinae, Oxytelinae, Paederinae, and Staphylininae). Trends in the involvement of staphylinid subfamilies with particular plant lineages were identified, associated with differences in insect habit and floral rewards. Overall this review indicates that the role of Staphylinidae as pollinators, and Coleoptera as a whole, is underestimated. Caution, however, must be given to inferring the role of staphylinids in pollination because rove beetles commonly function as inadvertent secondary pollinators or antagonists there to fulfil other ecological roles.

How many species of arthropods visit flowers?

Carl W. Wardhaugh     |     Review Paper     |     Published: 30 September 2015

Abstract: The majority of living plant species are pollinated by insects, and this interaction is thought to have played a major role in driving the diversification of modern angiosperms. But while flower–insect interactions have been well studied from the perspective of plants in the form of pollination biology, few studies have been carried out from an entomological perspective, where flowers are resources to exploit. As a consequence, it remains unknown how many insect species actually utilise floral resources, especially since many flower-visitors do not carry out pollination and may therefore be widely ignored in pollination studies. In this review, I attempt to present an overview of the taxonomic range of flower-visiting invertebrates and estimate the proportion of described species that regularly utilise flowers. The flower-visiting habit has likely evolved independently hundreds of times across more than a dozen modern invertebrate orders. I speculate, based on reviewing the literature and discussions with experts, that ~30 % of arthropod species (>350,000 described species) may regularly utilise flowers to feed, find a mate, or acquire other resources. When extrapolated to the estimated global diversity of the phylum Arthropoda, perhaps more than a million species regularly visit flowers. However, generating more accurate estimates will require much more work from the perspective of flower-visiting insects, including the often-ignored species that do not pollinate host plants. In particular, sampling techniques in addition to traditional observation protocols should be encouraged to ensure that all flower-visitors are recorded. Greater efforts to identify flower-visiting species beyond the level of order or family will also enhance our understanding of flower-visitor diversity.

Insights from measuring pollen deposition: quantifying the pre-eminence of bees as flower visitors and effective pollinators

P. G. Willmer, H. Cunnold, G. Ballantyne     |     Original Paper     |     Open Access     |     Published: 06 May 2017

Abstract: Using our accumulated datasets from Kenyan savanna, Mediterranean garigue, UK gardens and heathland, involving 76 plants from 30 families, we present detailed data to quantify the superiority of bees as pollinators of most flowering plants when compared with other flower visitors. Bees provided the majority of visits to study species at all sites, and 33 of the 76 plants received more than 90% of their visits from bees. Furthermore, pollen deposition onto stigmas from single-visit events (SVD, a measure of pollination effectiveness) was significantly higher for bees than non-bees at all the four sites where a major proportion of the flora was sampled. Solitary bees, and also bumblebees in temperate habitats, were the best potential pollinators for most plants in this respect, and significantly out-performed honeybees. Only a few plants were well served by bombyliid flies, and fewer again by larger hoverflies, butterflies, or solitary wasps. Bees also achieved better matches of their visit timing to peak pollen availability (measured indirectly as peak SVD), and made much shorter visits to flowers than did non-bees, permitting a substantially greater visit frequency. Additionally, they deposited significantly lower levels of potentially deleterious heterospecific pollen on stigmas in heathland and Mediterranean garigue, though not in the UK garden with densely clustered high-diversity flowering, or in the Kenyan savanna site with particularly dispersed flowering patches and some specialist non-bee flowers. Our data provide a novel and quantified characterisation of the specific advantages of bees as flower visitors, and underline the need to conserve diverse bee communities.

Extreme host range in an insular bee supports the super-generalist hypothesis with implications for both weed invasion and crop pollination

Jenna T. Draper, Tenn Haigh, Orkun Atakan, Danielle T. Limgenco, Tia Kearney, Lochlan Taylor, Jessica Wong, Elise Kalderovskis, Marika Tuiwawa, Olivia K. Davies, Mark I. Stevens & Michael P. Schwarz     |     Original Paper     |    
Published: 20 January 2021

Abstract: Super-generalism is a pollinator trait where species obtain floral resources from a very wide range of plant species. Theoretical and empirical studies suggest that on islands with low pollinator diversity, such pollinators should evolve to exploit a very wide range of floral morphologies. Super-generalism has implications not only for securing pollination network stability, but also for the invasibility of potential weeds that require specialist pollinators in their original ranges. Here we expand earlier studies on bees in Fiji to include a wider range of bee-plant interactions for bees that have been recently introduced into Fiji as well as the endemic Fijian halictine bee, Homalictus fijiensis. Our data show that the endemic Fijian bee has a much wider range of floral hosts than introduced bees, and this extends to pollen larceny of solanoid plant species that are usually buzz pollinated. Importantly, solanoid plants were not visited by introduced bee species, including the honeybee Apis mellifera, which is usually regarded as a super-generalist. Our findings are important because they add critical support to the hypothesis that super-generalism evolves in insular ecosystems with low pollinator diversity and that this may make such ecosystems vulnerable to invasion by exotic weeds. However, insular super-generalists may also have potential to stabilize plant-pollinator networks and may also be effective pollinators for exotic crop species, and this needs to be further explored in agricultural settings.

Pollen specialists are more endangered than non-specialised bees even though they collect pollen on flowers of non-endangered plants

Petr Bogusch, Eliška Bláhová & Jakub Horák     |     Original Paper     |     Published: 21 October 2020

Abstract: Non-parasitic bees differ in the degree of their taxonomic specialisation for pollen collection to feed their brood. Surveys of published data on pollen specialisation by bees of central Europe showed that about two-thirds of species are pollen generalists (polylectic) while the remainder only collect pollen of one family, genus or species (monolectic and oligolectic). Proportions of monolectic and oligolectic species among bee families and genera in central Europe varies widely, from the entirely pollen-specialised but small family Melittidae, to the mostly polylectic Halictidae and Apidae. The Asteraceae plant family attracts the most monolectic and oligolectic species, followed by Fabaceae, Brassicaceae and Campanulaceae. Several plant families in central Europe host only a single bee species. Of the species included in the Red List of bees of Czechia, oligoleges are proportionally more strongly represented than polyleges. Most of these red-listed oligoleges are associated with specific and regionally endangered habitats, i.e. steppes or wetlands. Most of the bees are more limited by the presence of their habitat or nesting site than by the host plant, although this fact is not simple to evaluate due to the incomplete data on the floral relations and distribution of bee species.

How long to stay on a plant: the response of bumblebees to encountered nectar levels

Hans Dreisig     |     Original Paper      |      Published: 27 December 2011

Abstract: This field study shows that the number of flowers visited per bee per plant (Anchusa officinalis) increases with the instantaneous nectar level at the plant. Observations during the season showed that a bee visits more flowers per plant of given nectar level, the lower the overall mean nectar level in the study area. These results agree with predictions from a model based on the ‘marginal value theorem’, but with assumptions and constraints adapted for nectar-foraging bees. It suggests that bumblebees assess the nectar level at a plant by sampling one or a few flowers, which is possible because within-plant nectar volumes are correlated. The bees compare encountered gains to an optimal plant switching threshold equal to the overall mean nectar level and leave an unrewarding plant as soon as possible, but continue to visit the flowers on a rewarding plant. However, the bees leave before having visited all flowers due to a searching constraint. The bees’ response to plant nectar levels results in systematic flower visitation, because visitation to recently depleted flowers is reduced, which reduces the variation of the inter-visit time per flower. Systematic flower visitation implies that the overall mean encountered gain per flower is higher than the overall mean standing crop, as predicted by a model of systematic foraging. However, the sampling and searching constraints on the bees’ response to plant nectar levels increase the variation of the inter-visit time per flower, and thereby limit the degree of systematic flower visitation and the effect on the mean encountered gain.

Taste perception in honeybees: just a taste of honey?

Gabriela de Brito Sanchez, João Ramalho Ortigão-Farias, Monique Gauthier, Fanglin Liu, Martin Giurfa     |     
Original Paper     |     Published: 08 August 2007

Abstract: The advent of the genomic era has opened new doors to understand the fundamental organization of living organisms and has therefore promoted a fertile field of comparative research that intends to identify similarities and differences between related and unrelated species at the genomic level. One of the organisms whose genome has been recently decoded is that of the honeybee Apis mellifera, enabling a direct comparison with another well-studied insect, the fruit fly Drosophila melanogaster. It was reported that the honeybee has only ten gustatory receptors and thus a very poor taste perception compared to Drosophila, which presents 68 gustatory receptors, and the mosquito Anopheles gambiae, which presents 76 gustatory receptors. In this forum article, we discuss the implications of these findings taking into account previous and new discoveries on honeybee gustation based on behavioral and neurobiological studies by several authors and us. We conclude that the world of taste of a honeybee might not be as poor as proposed and that further studies should integrate molecular, neurobiological, behavioral and ecological approaches to better characterize taste perception in bees.

Positive effects of the pollinators Osmia cornuta (Megachilidae) and Lucilia sericata (Calliphoridae) on strawberry quality 

John David Herrmann, Henriette Beye, Christel de la Broise, Hollyn Hartlep & Tim Diekötter     |     Original Paper     |     Published: 03 September 2018

Abstract: In the last decades, the fraction of crops requiring biotic pollination has increased dramatically. While wind- and self-pollination is possible for some of these crops, insect pollination generally increases yields and quality of produce. Especially pollinator communities with varying traits often show additive, positive effects on crop pollination. The aim of this study was to investigate the effect of two pollinator species with contrasting life history traits, the European orchard bee, Osmia cornuta, and the green bottle fly, Luciana sericata, on fruit quality, namely size, weight, shape, and color of fruits of the garden strawberry, Fragaria × ananassa We hypothesized that (1) pollination by both species individually results in higher strawberry quality compared to wind- and self-pollination, and (2) combining both species for pollination leads to higher strawberry quality due to higher functional diversity. To test these hypotheses, we used 40 mesh cages, each containing six strawberry plants. Flowering strawberry plants were either exposed to four O. cornuta individuals, four L. sericata individuals, two individuals of each species, or no pollinators (control) for one week. Fruit weight was only significantly higher than the control treatment when strawberry plants were exposed to bees. Fruit deformation, however, significantly decreased with all three pollinator treatments. Strawberry quality in cages with a combination of bees and flies was not superior to strawberry quality in cages with bees alone. Our results highlight the importance of insect pollination for strawberry quality but increased functional diversity of pollinators did not lead to additive pollination effects.

Night pollination

Night pollination
4 articles

Nocturnal bees exploit but do not pollinate flowers of a common bat-pollinated tree

Fernanda Figueiredo de Araujo, Priscila de Cássia Souza Araújo, Estefane Siqueira, Isabel Alves-dos-Santos, Reisla Oliveira, Stefan Dötterl & Clemens Schlindwein     |     Original Paper     |     Published: 22 September 2020

Abstract: Some species of bees restrict foraging to the twilight period before sunrise or after sunset. Among the plants sought by these nocturnal bees are species described as chiropterophilous, such as Caryocar brasiliense. The flowers of this species open in the evening and provide resources until dawn. We determined the pattern of flower visitation by nocturnal bees and their role in pollination and fruit set of C. brasiliense and evaluated its importance as floral resource for nocturnal bees. We analyzed the pollen composition of cell provisions of nocturnal bees of Ptiloglossa (Colletidae) and compared its scent with floral scent compounds of C. brasiliense. Moreover, we conducted a pollinator exclusion experiment to determine the contribution of nocturnal bees to its fruit set. Disregarding bats, Ptiloglossa latecalcarata and two species of Megalopta (Halictidae) were consistent nectar and pollen gathering visitors, along with some social diurnal bees. The visitor exclusion experiment revealed that bee visits do not result in fruit set, which only occurs through visits by bats. The flowers supply a significant amount of pollen for nocturnal bees, as demonstrated through pollen analysis of brood cells and scopa loads. This interaction, therefore, is only beneficial to the commensalist bees. The scent collected from brood cells was dominated by hexanoic acid and 1-hexanol and differed strongly from the floral scent of C. brasiliense. These results substantiate that bat-pollinated flowers are an important part of the food niche of nocturnal bees, which implies that they are sensorially equipped to recognize floral traits shaped by bats.

Effect of diurnal vs. nocturnal pollinators and flower position on the reproductive success of Echium simplex

Julia Jaca, Manuel Nogales & Anna Traveset     |     Original Paper     |     Published: 27 March 2020

Abstract: Nocturnal pollination plays an important role in sexual plant reproduction but has been overlooked, partially because of intrinsic difficulties in field experimentation. Even less attention has received the effect of within-inflorescence spatial position (distal or proximal) on nocturnal pollinators of columnar plants, despite numerous studies examining the relationship between such position and reproductive success. Woody endemic Echium simplex possesses large erect inflorescences bearing thousands of flowers which are visited by a wide array of diurnal and nocturnal animals. In this study, we identified nocturnal visitors and compared their pollination effectiveness with that of diurnal pollinators in different inflorescence sections by means of selective exclosures in NE Tenerife (Canary Islands). Nocturnal visitors included at least ten morphospecies of moths (such as Paradrina rebeli and Eupithecia sp.), two coleopteran species (mainly Alloxantha sp.), neuropterans (Chrysoperla carnea), dictyopterans (Phyllodromica brullei), dermapterans (Guanchia sp.) and julidans (Ommatoiulus moreletii). In general, plants excluded from pollinators set less fruits than open-pollination (control) plants which set fruits homogeneously across sections. Diurnally pollinated plants set more fruit in their upper parts whereas nocturnally pollinated plants set fruit in both upper and bottom sections. We conclude that although the frequency and diversity of diurnal pollinators is far higher than that of nocturnal pollinators, both exhibit different foraging behaviour that generates complementary effects on the reproductive success of E. simplex.

Pollination of Machaerium opacum (Fabaceae) by nocturnal and diurnal bees

Estefane Siqueira, Reisla Oliveira, Stefan Dötterl, Guaraci Duran Cordeiro, Isabel Alves-dos-Santos, Theo Mota & Clemens Schlindwein     |     Original Paper     |     Published: 29 June 2018

Abstract: With plants whose flowers open at night and stay open during the day, nocturnal pollinators may exploit floral resources before diurnal competitors. Moths, bats, and beetles are the most familiar nocturnal pollinators, whereas nocturnal bees as pollinators remain poorly understood. The common Cerrado tree Machaerium opacum (Fabaceae) has white and strongly scented melittophilous flowers, which first open at the night and remain open during the day and, thus, have the potential to be visited by both nocturnal and diurnal bees. We asked: (1) what is the plant’s breeding system? (2) when during the night do the flowers open? (3) what are the visual and olfactory floral cues? and (4) which nocturnal/diurnal bees visit and pollinate the flowers? We show that M. opacum is self-incompatible. Its flowers open synchronously at 03:30 h, produce nectar exclusively at night, and have an explosive mechanism of pollen presentation. The flowers have pure white petals, release strong scents during anthesis, and are pollinated by nocturnal and diurnal bees. We recorded four nocturnal and 17 diurnal species as flower visitors, with females of nocturnal species of Ptiloglossa (Colletidae) being the most abundant. After an initial pollen-releasing visit, only a minor amount of pollen remains in a flower. Several floral traits favor visits by nocturnal bees: (1) night-time flower opening, (2) nectar production at night, (3) almost complete pollen release during the first flower visit, and (4) pure white petals and strong odor production prior to sunrise, facilitating visual and olfactory detection of flowers when light is dim.

Solitary and social bees as pollinators of Wahlenbergia (Campanulaceae): single-visit effectiveness, overnight sheltering and responses to flower colour

Megan R. Welsford, Steven D. Johnson     |     Original Paper     |     Published: 01 July 2011

Abstract: Solitary bees often form specialised mutualisms with particular plant species, while honeybees are considered to be relatively opportunistic foragers. Thus, it may be expected that solitary bees are more effective pollinators than honeybees when foraging on the same floral resource. To test this, we studied two Wahlenbergia species (Campanulaceae) in South Africa that are visited by both social honeybees and solitary bees, and which are shown here to be genetically self-incompatible and thus reliant on pollinator visits for seed production. Contrary to expectation, the solitary bee Lipotriches sp. (Halictidae) and social bee Apis mellifera (Apidae), which were the two most frequent visitors to flowers of the study species, were equally effective pollinators in terms of the consequences of single visits for fruit and seed set. Both bee species preferentially visited female phase flowers, which contain more nectar than male phase flowers. Male solitary bees of several genera frequently shelter overnight in flowers of both Wahlenbergia species, but temporal exclusion experiments showed that this behaviour makes little contribution to either seed production or pollen dispersal (estimated using a dye particle analogue). Manipulation of flower colour using a sunscreen that removed UV reflectance strongly reduced visits by both bee groups, while neither group responded to Wahlenbergia floral odour cues in choice tests. This study indicates that while flowers of Wahlenbergia cuspidata and W. krebsii are pollinated exclusively by bees, they are not under strong selection to specialise for pollination by any particular group of bees.

External factors affecting plant-pollinator interactionsExternal factors affecting plant-pollinator interactions
8 articles

The effects of rainfall on plant–pollinator interactions

David A. Lawson & Sean A. Rands     |     Review Paper     |     Open Access     |     Published: 21 February 2019

Abstract: As global surface temperatures rise, global precipitation rates are predicted to increase. These localised increases in rainfall patterns may significantly affect plant–pollinator interactions in multiple ways. Detrimental effects to plant–pollinator interactions could have significant ecological and economic consequences, and so it is important to understand the effects that rain has on these mutualisms. Increased rainfall has the potential for population-level effects but there also wide scope for individual-level effects, which have received surprisingly little attention. Changes in rainfall patterns could alter the timings of phenological phases while also increasing the likelihood of pollen degradation and nectar dilution, each having detrimental effects to the fitness of the plant, the pollinator or both parties. Pollinators could also be affected through mechanical and energetic constraints, along with disruption of foraging patterns and disruption to sensory signals. In this review, we demonstrate that there are clear gaps in our knowledge of these events, the exploration of which should open new areas of debate surrounding the effects of climate change on biological systems.

Understanding how changing soil nitrogen affects plant–pollinator interactions

Thomas I. David, Jonathan Storkey & Carly J. Stevens     |     Review Paper     |     Open Access     |     Published: 23 August 2019

Abstract: Many pollinating insects, across taxa and regions, have declined during the twentieth century. Amongst the drivers of these trends, soil eutrophication and acidification caused by nitrogen (N) have not been broadly researched. Anthropogenic influences have greatly increased the global deposition of N to soils during the past century; this is increasingly recognised as a threat to global biodiversity. The fundamental role of soil in plant growth and health means that alterations to soil conditions will likely have consequences for plant–pollinator interactions. Soil N can be a substantial driver of the species structure of botanical communities, often reducing species richness due to quick growth of competitive grasses. Floral traits, relevant to pollinators, such as phenology, morphology, and nectar and pollen production and quality can also be affected by soil N. We currently lack sufficient research to determine if and how pollinators will be impacted by these changes. This review collates the research and evidence of how soil N affects botanical species composition and relevant floral traits, and discusses how pollinating insects and plant–pollinator interactions might be impacted. We conclude by identifying the key knowledge gaps in this subject; the lack of research that includes the pollinators into studies of how N additions affect botanical traits, poor understanding of inter-specific variation in botanical responses to N, synthesis of botanical traits to form a comprehensive understanding, and the inclusion of other abiotic and biotic drivers into studies.

Changes in plant community structure and decrease in floral resource availability lead to a high temporal β-diversity of plant–bee interactions

Leandro Hachuy-Filho, Caio S. Ballarin & Felipe W. Amorim     |     Original article     |     Published: 23 July 2020

Abstract: Biological communities are subject to spatiotemporal variations in community structure, i.e., species composition, richness, and abundance. Plant–pollinator interactions are affected by species composition and abundance, so that rapid changes in plant community structure can lead to critical impacts on plant–pollinator interactions at the community level. The extent of these impacts depends on how plants respond to different kinds of stressors, such as the disturbance caused by invading species. In this research, we conducted a before-and-after study to evaluate the potential effects of an invasive fast-growing alien grass species on the structure of a plant–pollinator interaction network. We described the changes in community structure and plant–pollinator interactions over two sampling periods, through the temporal β-diversity of plant and bee species, plant–bee interactions, and plant functional traits. Our results showed that changes in plant community composition (especially the plants in the network core) and decrease in plant species richness, as well as in floral resources availability impacted plant–pollinator interactions of a grassland community after the growth of a fast-growing alien grass species. These changes were accompanied by a decrease in plant–bee interaction diversity, and a high β-diversity of species interactions mainly due to interaction rewiring. However, we found no effect on the functional diversity of flowers. In conclusion, our study showed that a short-term change in plant species composition and floral resource abundance impacted plant–bee interactions, which markedly changed network structure and dynamics.

Transient dehydration of pollen carried by hot bees impedes fertilization

Sarah A. Corbet, Fei-Fei Chen, Fang-Fang Chang & Shuang-Quan Huang     |     Original Paper     |     Published: 05 November 2019

Abstract: In the intense solar radiation of an alpine climate, small black bees often experience extremely high thoracic temperatures when they are foraging on flowers, but flies forage at lower temperatures. To explore the hypothesis that seed set could be depressed by transient dehydration of pollen at the high temperatures reached by hot bees foraging in sunshine, we compared the effectiveness of single visits by different pollinators to a bowl-shaped flower Potentilla lancinata in alpine meadows, SW China. The ratio of seed set to pollen transferred in individual flowers was monitored over 2 years, indicating that pollen deposited on stigmas by halictid bees produced lower seed set than pollen carried by flies. Scopal pollen applied to stigmas by hand gave good seed set, but in germination tests it burst more frequently than pollen from anthers, implying dehydration. Pollen grains freshly taken from the scopae of solitary bees foraging in sunshine were smaller than those taken from anthers or foraging bees in early-morning overcast conditions, implying dehydration. The effect was reversible: hand pollination showed that scopal pollen was no less effective than fly pollen after removal from the bee. Pollen carried by such bees foraging in intense sunlight in flowers became dehydrated, causing an osmotic mismatch between the pollen and the stigmas. Transient heat-induced dehydration of pollen represents a novel pathway by which climate warming may disrupt plant reproduction, and helps us understand why flies could be more effective pollinators than bees in cool, high-radiation arctic or high-altitude sites.

Does florivory affect the attraction of floral visitors to buzz-pollinated Solanum rostratum

Mayumi Vega-Polanco, Luis Antonio Rodríguez-Islas, Raisa Yarina Escalona-Domenech, Leopoldo Cruz-López, Julio C. Rojas & Lislie Solís-Montero     |     Original Paper     |     Published: 17 October 2019

Abstract: Floral herbivory (florivory) can directly and indirectly affect plant reproduction through the loss of ovules or seeds and by reducing the visitation by pollinators through the reduction in flower attractiveness, respectively. We studied the effect of florivory on pollinator visitation in a buzz-pollinated herb. We used Solanum rostratum as the study model because its specialised morphology, heterantherous flowers that emit floral scents, demands a close association with its pollinators (buzzing bees). We hypothesized that when florivores consume the attractive structures (corolla and rewarding anthers), the pollinators would visit the damaged flowers less often, indirectly affecting S. rostratum reproductive success. Furthermore, we hypothesized that consumption of the reproductive structures (pollinating anther and pistil) would directly affect the plants reproductive success. We conducted observations of three S. rostratum populations in central Mexico. We observed twelve species of florivore consuming S. rostratum flowers. Florivores preferred to consume the attractive structures (corolla) over reproductive structures. However, they preferred to consume the anthers specialised for feeding pollinators over the anthers specialised for pollination. In addition, we recorded floral volatiles emitted by flowers damaged by florivory using solid-phase microextraction coupled with gas chromatography–mass spectrometry. We identified 25 volatile compounds in S. rostratum flowers, mainly aromatic, monoterpene and sesquiterpene compounds. The relative proportions of these compounds differed between undamaged and damaged flowers. Bioassays showed that both legitimate visitors (pollinators) and illegitimate visitors (thieves) visited undamaged flowers more often than flowers damaged by florivores; however, the decrease in visitation frequency did not affect fruit and seed production. In conclusion, the consumption of attractive (corolla) and reward floral structures (feeding anthers) reduced the frequency of visits by pollinators but does not affect S. rostratum reproductive success (fruit and seed set) probably because reproductive structures (pistil and pollinating anthers) are less often consumed.

Long-term yield trends of insect-pollinated crops vary regionally and are linked to neonicotinoid use, landscape complexity, and availability of pollinators 

Heikki M. T. Hokkanen, Ingeborg Menzler-Hokkanen & Maaria Keva     |     Original Paper     |     Published: 21 April 2017

Abstract: Time series data on crop yields for two main wind-pollinated crops (barley and wheat) and for three crops benefitting from insect pollination (turnip rapeseed, caraway, and black currant), were compiled from official agricultural statistics. In Finland, these statistics are available at aggregate national level, and at the level of each of the 15 provinces of the country. Yields of wind-pollinated crops have steadily increased in Finland, while yields of insect-pollinated crops have been highly variable. The largest crop benefitting from insect pollination is turnip rapeseed, which shows first a clear tendency to increased yields from 1980 to 1993, after which there has been a continuous decline in yields at the national average level. Regionally, the trends in turnip rapeseed yield show large variation, so that in six provinces of Finland, the trend has been significantly decreasing; in five provinces, there has been no significant trend; and in two provinces, there has been a significant linear increase in yields. Yield trends in the two other insect-pollinated crops, caraway and black currants, show similar trend variations. However, at the national average level, caraway yields show no significant trend, while black currant yields have increased during the past 6 years. The possible impact on the trends of insect-pollinated crops of three explanatory variables was analyzed. Significant linear correlation was found between the yield trends (slope of the trends) in rapeseed, and the extent of using neonicotinoid seed dressing in the provinces; the magnitude of yield decline in turnip rapeseed increased, as the use of neonicotinoid seed dressing increased. Similar significant linear correlation was found for the magnitude of yield decline in turnip rapeseed and the complexity of the agricultural landscape in each province; yield trend changed from negative to positive as the proportion of agricultural land of the total terrestrial land area declined from 28% to below 10%. The availability of honey bee colonies with respect to the growing area of crops benefitting from insect pollination also had a linear, significant impact on turnip rapeseed yield trends: yields tended to decline in provinces, where the supply of managed pollinators with respect to demand was low, but tended to increase in provinces, where the number of honey bee colonies were over 30% of the estimated demand. As neither the landscape complexity (proportion of arable land of total terrestrial land area), nor the number of honey bee colonies for pollination have changed significantly over the past 10–20 years, these factors cannot explain the observed differences in the yield trends of the examined insect-pollinated crops. It appears that only the uptake of neonicotinoid insecticide seed dressing about 15 years ago can explain the crop yield declines in several provinces, and at the national level for turnip rapeseed, most likely via disruption of pollination services by wild pollinators.

The immunological dependence of plant-feeding animals on their host’s medical properties may explain part of honey bee colony losses

Erik Tihelka     |     Forum Paper     |     Published: 31 July 2017

Abstract: The honey bee (Apis mellifera) is an important pollinator of agricultural and horticultural crops, but also of wild flowers. The species has been facing declines in many areas of the world, the causes being identified as multifactorial. Recently, it has been theorised that some plant-dwelling animals may develop a dependence on the medicinal properties of their hots plant’s secondary metabolites. Here, the question of honey bee self-medication using organic materials, namely propolis, nectar, honey, honeydew, pollen, wood, and algae for self-medication is addressed. Self-medication in honey bees is a largely unexplored area and thus a comprehensive overview of the field is provided. Prior studies suggest that recent honey bee colony declines are driven by decreased forage plant availability. The problem is expanded and it is suggested, that if honey bees developed a dependence on medical properties of some disappearing plants or materials, this could explain a part of the colony losses observed around the world. To date, convincing evidence points towards self-medication with honey and propolis. Bees also contact plant secondary metabolites, fatty acids, essential oils, and microorganisms that are active against the causative agents of American foulbrood, European foulbrood, nosemosis, chalkbrood, stonebrood, and varroasis. In the future, selected taxa of plants with medicinal properties may be planted to boost honey bee health without chemotherapy. Future directions of research are discussed.

Exploring the predation of UK bumblebees (Apidae, Bombus spp.) by the invasive pitcher plant Sarracenia purpurea: examining the effects of annual variation, seasonal variation, plant density and bumblebee gender

Elizabeth Franklin, Damian Evans, Ann Thornton, Chris Moody, Iain Green & Anita Diaz     |     Original Paper     |     Open Access     |     Published: 26 November 2016

Abstract: Invasive carnivorous plant species can impact the native invertebrate communities on which they prey. This article explores the predation of native UK bumblebees (Bombus spp.) by the invasive pitcher plant species Sarracenia purpurea and discusses the potential effect of S. purpurea on native bumblebees. Specifically, it evaluates whether the extent to which bumblebees are captured varies (i) over successive years, (ii) across June and July, (iii) with density of distribution of pitchers or (iv) with bumblebee gender. Pitcher contents were examined from an established population of Sarracenia purpurea growing in Dorset, UK. Results show that the total extent to which bumblebees were captured differed over the years 2012–2014 inclusive. A 1-year study in 2013 showed that more bumblebees were caught in July than in June and more bumblebees were captured when pitchers grew at high density. Results from 2013 also showed that more pitchers caught more than one bumblebee than would be expected based on a normal probability distribution and that this phenomenon affects female and male bumblebees equally. We discuss possible reasons for these results including that the bumblebees may be using S. purpurea as a resource. Further work is required to establish the exact underpinning mechanisms and the relative roles of plant and bumblebee behaviour within the relationship. Such interaction complexity may have consequences for consideration in invasive carnivorous plant management.

Bee foraging and flower handling behaviour

Bee foraging and flower handling behaviour 
7 articles

Floral abundance and bee density affect species-specific foraging patterns of alpine bumble bees

Akari Shibata & Gaku Kudo     |     Original article     |     Published: 21 October 2020

Abstract: In response to the qualitative and quantitative changes in floral resources, bumble bees flexibly forage multiple plant species throughout the growing season. During the short summer in an alpine ecosystem, the activity of worker bees is maximized in the middle of the season, when the competition for floral resources may be intense. We predicted that the foraging patterns of bumble bees are affected by both relative floral abundance and interactions between bumble bee species. We recorded the floral abundance of individual plant species and the foraging frequency of bumble bees in an alpine meadow during the major flowering period over 3 years. Two bumble bee species were common during the major flowering period. Although they tended to visit abundant floral species, the shorter-tongued species (Bombus hypocrita) showed a more diverse and flexible floral choice than the longer-tongued species (Bombus beaticola). The degree of floral use overlap between two bumble bee species tended to decrease when the foraging density of the longer-tongued species was high. These results indicated that multiple bumble bee species are able to coexist when certain bee species can flexibly change targeting flowers in response to the temporal variations in flowering species and the density of competing bee species. The extent of foraging flexibility is related to the morphological traits of bee species and availability of floral resources.

Bumble bees exhibit daily behavioral patterns in pollen foraging 

Anthony D. Vaudo, Harland M. Patch, David A. Mortensen, Christina M. Grozinger, John F. Tooker     |     Original Paper     |     Published: 07 June 2014

Abstract: In response to global declines in bee populations, several studies have focused on floral resource provisioning schemes to support bee communities and maintain their pollination services. Optimizing host-plant selection for supplemental floral provisioning requires an understanding of bee foraging behavior and preferences for host-plant species. However, fully characterizing these preferences is challenging due to multiple factors influencing foraging, including the large degree of spatiotemporal variability in floral resources. To understand bee pollen foraging patterns, we developed a highly controlled mechanistic framework to measure pollen foraging preferences of the bumble bee Bombus impatiens to nine plant species native to Pennsylvania. We recorded continuous observations of foraging behavior of the experimental bee community and individual bees, while simultaneously standardizing for the number of foragers in the environment and differences in floral display of each plant species, while controlling for flowering phenology such that bees only foraged when all plant species’ flowers were open. Our results demonstrate that B. impatiens exhibit predictable daily patterns in their pollen foraging choices, and their preferences are dominated by the host-plants they visit first. We hypothesize that these patterns at the community and individual levels are driven by the interplay between pollen abundance and quality. We recommend that daily cycles of host-plant visitation be considered in future studies to ensure precise and accurate interpretations of host-plant preference. Such precision is critical for comprehensive analyses of the proximate and ultimate mechanisms driving bee foraging behavior and the selection of host-plant species to use in habitat restoration protocols.

Floral temperature patterns can function as floral guides

Michael J. M. Harrap, Natalie Hempel de Ibarra, Heather M. Whitney & Sean A. Rands     |     Original Paper     |     Open Access     |     Published: 13 January 2020

Abstract: Floral guides are signal patterns that lead pollinators to floral rewards after they have located the flower, and increase foraging efficiency and pollen transfer. Patterns of several floral signalling modalities, particularly colour patterns, have been identified as being able to function as floral guides. Floral temperature frequently shows patterns that can be used by bumblebees for locating and recognising the flower, but whether these temperature patterns can function as a floral guide has not been explored. Furthermore, how combined patterns (using multiple signalling modalities) affect floral guide function has only been investigated in a few modality combinations. We assessed how artificial flowers induce behaviours in bumblebees when rewards are indicated by unimodal temperature patterns, unimodal colour patterns or multimodal combinations of these. Bees visiting flowers with unimodal temperature patterns showed an increased probability of finding rewards and increased learning of reward location, compared to bees visiting flowers without patterns. However, flowers with contrasting unimodal colour patterns showed further guide-related behavioural changes in addition to these, such as reduced reward search times and attraction to the rewarding feeder without learning. This shows that temperature patterns alone can function as a floral guide, but with reduced efficiency. When temperature patterns were added to colour patterns, bees showed similar improvements in learning reward location and reducing their number of failed visits in addition to the responses seen to colour patterns. This demonstrates that temperature pattern guides can have beneficial effects on flower handling both when alone or alongside colour patterns.

Distinguishing signals and cues: bumblebees use general footprints to generate adaptive behaviour at flowers and nest

Nehal Saleh, Alan G. Scott, Gareth P. Bryning, Lars Chittka     |     Original Paper     |     Published: 25 July 2007

Abstract: Chemicals used in communication are divided into signals and cues. Signals are moulded by natural selection to carry specific meanings in specific contexts. Cues, on the other hand, have not been moulded by natural selection to carry specific information for intended receivers. Distinguishing between these two modes of information transfer is difficult when animals do not perform obvious secretion behaviours. Although a number of insects have been suspected of leaving cues at food sites and nest entrances, studies have not attempted to experimentally distinguish between cues and signals. Here, we examine the chemical composition of the scent marks left by the bumblebee Bombus terrestris at food sites and compare it to those found at a neutral location. If bees are depositing a cue, we expect the same chemicals to be found at both sites, but if they deposit a signal we only expect to find the scent marks at the food site. We were also interested in identifying the chemicals left at the nest entrance to determine if they differed from those used to mark food sites. We find that bees deposit the same chemicals at food, nest and neutral sites. Therefore, bumblebees leave behind general chemical footprints everywhere they walk and we propose that they learn to use these footprints in a manner that ultimately enhances their fitness, for example, to improve their foraging efficiency and locate their nest. Experimentally, distinguishing these two modes of information transfer is crucial for understanding how they interact to shape animal behaviour and what chemical bouquets are under natural selection.

Attachment of honeybees and greenbottle flies to petal surfaces

Patrick Bräuer, Christoph Neinhuis, Dagmar Voigt     |     Original Paper     |     Published: 26 November 2016

Abstract: Flower surfaces play a key role in the interaction with pollinators acting as signals and landing sites to attach to. To test attachment, Carniolan honeybees and greenbottle flies were used. Both species represent pollinators equipped with smooth or hairy tarsal attachment devices, respectively. A combination of microscopic methods and traction force measurements was applied in order to understand and evaluate the efficiency of pollinator attachment to a variety of petal surfaces. Although the petal surface texture influenced the attachment, coevolutionary relationships or adaptations between flower surfaces and pollinator tarsi could not be confirmed. Since pollinators appear to be opportunistic, they are expected to attach to a variety of flower surfaces. Rougher surfaces, including conical and papillate epidermal cells, significantly increased the foothold of flies and honeybees, while flat, tabular epidermal cells covered with microstructures like cuticular folds and epicuticular wax crystals impaired attachment. Carniolan honeybees generated larger forces than greenbottle flies, but the latter showed higher safety factors. However, tendencies in attachment ability toward sufficient and insufficient substrates are similar in flies and bees.

Morphology and development of floral features recognised by pollinators

Heather M. Whitney, Beverley J. Glover     |     Review Paper     |     Published: 21 September 2007

Abstract: The diversity of angiosperm flowers is astounding. The conventional explanation for this diversity is that it represents the great variety of ways in which flowers have adapted to attract an even greater diversity of animal pollinators. Many animal behaviourists are therefore interested in how changes in floral morphology affect pollinator behaviour. The establishment of well-characterised model plant species has greatly furthered our understanding of how floral morphology is generated and varied. Many of these model species are pollinated by animals and attract their pollinators through the production of colour, shape, scent, size and rewards. An understanding of the developmental plasticity of floral morphology, and the constraints upon it, should inform research into animal responses to flowers. The use of genetically characterised model species, and the isogenic and near-isogenic lines available in them, will allow dissection of the different components of floral attraction and reward in natural systems.

Honey bee handling behaviour on the papilionate flower of Robinia pseudoacacia L. 

Manuela Giovanetti, Giovanna Aronne     |     Original Paper     |     Published: 12 October 2012

Abstract: Papilionate flowers, such as those of Robinia pseudoacacia L., show tripping mechanisms that prevent pollen release: only those bees which apply the right force on petals induce pollen to be deposited on their bodies. Apis mellifera is considered a poor visitor of such flowers, since individuals are usually too weak to trip the mechanism. Despite this, the honey bee pays frequent visits to flowers of R. pseudoacacia and produces a much appreciated unifloral honey. We investigated how bees manipulate R. pseudoacacia flowers, whether they contact the plant’s reproductive core and if there is any appreciable difference related to the manipulation of individual flowers. Honey bees showed two strategies for resource collection, namely legitimate visits and robberies. Legitimate visits were more frequent and about 63 % entailed contact with the flower’s reproductive core. We distinguished two behaviours, one to achieve successful positioning on the flower and the other for nectar intake. These behaviours were clearly perceptible and described by different curves of time frequency distribution. From the beginning to the end of anthesis, flowers were classified into four types on the basis of their morphological and phenological traits. Positioning time differed significantly depending on the flower type, with less time needed for more ageing flowers. Time spent in nectar intake was instead highly variable and independent of flower ageing. Selecting the right flower type would appear to lead to obtaining the R. pseudoacacia reward, overcoming species-specific physical inability. Moreover, the role of honey bees as pollinators of R. pseudoacacia is considered. Finally, the relations between petal characteristics and strength needed to trip the mechanism in papilionate flowers is also discussed in the light of nectar foragers.

Vision and learning in bees
Vision and learning in bees
5 articles

The attractive role of floral elements in heterantherous species without pronounced stamen differences

Vinícius Lourenço Garcia de Brito, Fernanda Barão Leite, Francismeire Jane Telles, Leonardo Ré Jorge & Marlies Sazima     |     Original Paper     |     Published: 19 November 2020

Abstract: Floral resources can be recognized by visitors through attractants that signal their presence. However, besides petals, it is still unclear how floral elements in heterantherous species are perceived by visiting bees. In this study, we aim to understand the role of stamens and petals of Pleroma granulosum and P. raddianum in attracting pollination bees, mainly by evaluating whether pollinator behaviour differs in response to different sized stamens between which there is no apparent colour contrast. Using colour visual models, we estimated bee colour discrimination between stamen sets and corolla in both species and carried out preference experiments among floral elements, using the bees Bombus morio and Xylocopa frontalis as models in the field. Pollination and feeding stamens are not discriminable by bees in both plant species. Bees only preferred flowers with petals, indicating that they are essential to long-distance attraction. During preferential tests, bees seemed to better respond to visual stimuli on the right side, suggesting lateralization. We also demonstrate that tactile stimulation by the anthers is necessary to trigger bee buzzing behaviour. Thus, since bees were not specifically attracted to any stamen set, heteranthery without colour differences between stamens is not enough to determine bee choice behaviour.

Carry-over effects of bumblebee associative learning in changing plant communities leads to increased costs of foraging

Antonina I. Internicola, Paul A. Page, Giorgina Bernasconi, Luc D. B. Gigord     |     Original Paper     |     Published: 16 November 2008

Abstract: Flower visitors learn to avoid food-deceptive plants and to prefer rewarding ones by associating floral cues to rewards. As co-occurring plant species have different phenologies, cue-reward associations vary over time. It is not known how these variations affect flower visitors’ foraging costs and learning. We trained bumblebees of two colonies to forage in a community of deceptive and rewarding artificial inflorescences whose flower colours were either similar or dissimilar. We then modified the community composition by turning the rewarding inflorescences into unrewarding and adding rewarding inflorescences of a novel flower colour. In the short term, bees trained to similar rather than dissimilar inflorescences experienced higher costs of foraging (decreased foraging speed and accuracy) in the novel community. The colonies differed in their speed-accuracy trade-off. In the longer term, bees adapted their foraging behaviour to the novel community composition by increasingly visiting the novel rewarding inflorescences.

Flower colour variation across a hybrid zone in Antirrhinum as perceived by bumblebee pollinators 

Emmanuelle Tastard, Christophe Andalo, Martin Giurfa, Monique Burrus, Christophe Thébaud     |     Original Paper     |     Published: 27 September 2008

Abstract: To assess if pollinators’ behaviour could explain the maintenance of hybrid zones between different flower colour morphs, we analyzed flower colour variation in an Antirrhinum hybrid zone using spectrometry and a model of bee perception. Some colours generated by hybridization were not observed in any Antirrhinum species and even appeared to be rare among angiosperms. Variation in flower colours within the hybrid zone was continuous; the most similar colours were predicted not to be discriminated from one another in natural foraging situations. However, when compared at a scale corresponding to bees’ foraging range, some flower colours could be discriminated from all colours displayed by neighbouring plants. This could affect pollinator behaviour and explain lower visitation rates within the centre of the hybrid zone. Behavioural studies involving bumblebees and plant mixtures of parental and hybrid flower colours carefully characterized with appropriate visual models will be necessary to test this hypothesis.

Chromatic and achromatic stimulus discrimination of long wavelength (red) visual stimuli by the honeybee Apis mellifera 

Carolina E. Reisenman, Martín Giurfa     |     Original Paper     |     Published: 13 June 2008

Abstract: It has long been assumed that bees cannot see red. However, bees visit red flowers, and the visual spectral sensitivity of bees extends into wavelengths to provide sensitivity to such flowers. We thus investigated whether bees can discriminate stimuli reflecting wavelengths above 560 nm, i.e., which appear orange and red to a human observer. Flowers do not reflect monochromatic (single wavelength) light; specifically orange and red flowers have reflectance patterns which are step functions, we thus used colored stimuli with such reflectance patterns. We first conditioned honey bees Apis mellifera to detect six stimuli reflecting light mostly above 560 nm and found that bees learned to detect only stimuli which were perceptually very different from a bee achromatic background. In a second experiment we conditioned bees to discriminate stimuli from a salient, negative (un-rewarded) yellow stimulus. In subsequent unrewarded tests we presented the bees with the trained situation and with five other tests in which the trained stimulus was presented against a novel one. We found that bees learned to discriminate the positive from the negative stimulus, and could unambiguously discriminate eight out of fifteen stimulus pairs. The performance of bees was positively correlated with differences between the trained and the novel stimulus in the receptor contrast for the long-wavelength bee photoreceptor and in the color distance (calculated using two models of the honeybee colors space). We found that the differential conditioning resulted in a concurrent inhibitory conditioning of the negative stimulus, which might have improved discrimination of stimuli which are perceptually similar. These results show that bees can detect long wavelength stimuli which appear reddish to a human observer. The mechanisms underlying discrimination of these stimuli are discussed.

Visual search and the importance of time in complex decision making by bees

Lars Chittka & Johannes Spaethe     |     Review Paper     |     Published: 08 March 2007

Abstracts: Psychophysicists studying decision making in animals have overwhelmingly focused on choice accuracy, not speed. Results from human visual search, however, show that there might be a tight link between the two. Here we review both visual-sensory and cognitive mechanisms that affect decision speed in flower visiting bees. We show that decision times are affected by contrast of targets and background, by similarity between targets and distractors, numbers of distractors present in a scene, illuminating light intensity, presence or absence of punishment, and complexity of tasks. We explore between-individual and within-individual speed-accuracy tradeoffs, and show that bees resort to highly dynamic strategies when solving visual search tasks. Where possible, we attempt to link the observed search behaviour to the temporal and spatial properties of neuronal circuits underlying visual object detection. We demonstrate that natural foraging speed may not only be limited by factors such as food item density, flight energetics and scramble competition, as often implied. Our results show that understanding the behavioural ecology of foraging can substantially gain from knowledge about mechanisms of visual information processing.