Do local conspecific density and floral display size influence fruit set via pollinator visitation in Orchis militaris?

Plant density varies naturally, from isolated plants to clumped individuals, and this can influence pollinator foraging behaviour and plant reproductive success. In addition, the effect of conspecific density on reproduction may depend on the pollination system, and deceptive species differ from rewarding ones in this regard, a high density being often associated with low fruit set in deceptive plants. In our study, we aimed to determine how local conspecific density and floral display size (i.e. number of flowers per plant) affect fruit set in a deceptive orchid (Orchis militaris) through changes in pollinator visitation. We measured fruit set in a natural population and recorded pollinator abundance and foraging behaviour within plots of different O. militaris densities. Detailed data were recorded for the most abundant potential pollinators of O. militaris, i.e. solitary bees. Floral display size was negatively correlated to fruit set in medium‐density plots, but uncorrelated in low‐ and high‐density plots. Plot density had no effect on solitary bee abundance and visitation, which may be due to low pollinator abundance within the study site. The proportion of visited flowers per inflorescence was negatively influenced by floral display size, which is in line with previous studies. In addition, solitary bees spent decreasing time in successive flowers within an inflorescence, and the time spent per flower was negatively affected by ambient temperature. Our results suggest that pollinator behaviour during visitation is poorly linked to pollen deposition and reproductive success in O. militaris.     

Male mate‐seeking and mating behaviors of Eucera nipponensis (Hymenoptera: Apidae) at a nectarless orchid habitat: Are empty flower patches a profitable rendezvous site?

Male solitary bees typically use emergence‐nesting areas and/or flower patches of food plants, where receptive females are relatively numerous, as rendezvous sites. However, mate‐seeking males have been also observed at food‐deceptive orchid patches, where numerous encounters with foraging females can hardly be expected, owing to the lack of floral rewards. Here, we describe the male mate‐seeking and mating behaviors of the Japanese long‐horned bee Eucera nipponensis at habitats of the food‐deceptive orchid Cymbidium goeringii. On the basis of the results, we report empty flower patches are not necessarily fruitless sites for mate‐seeking males because naive female bees, which are highly likely to be recently emerged and unmated, can be attracted to non‐rewarding orchids. We also suggest a possibility that a small number of the males could receive a “sexual reward” (i.e. mating opportunities), owing to the food‐deceptive orchid, in return for their pollination work. This occasional interaction could represent the initial stage in the evolution of sexually deceptive orchids from food‐deceptive orchids.     

The potential for floral mimicry in rewardless orchids: an experimental study

More than one-third of orchid species do not provide their pollinators with either pollen or nectar rewards. Floral mimicry could explain the maintenance of these rewardless orchid species, but most rewardless orchids do not appear to have a rewarding plant that they mimic specifically. We tested the hypothesis that floral mimicry can occur through similarity based on corolla colour alone, using naive bumble-bees foraging on arrays of plants with one rewarding model species, and one rewardless putative mimic species (Dactylorhiza sambucina) which had two colour morphs. We found that when bees were inexperienced, they visited both rewardless morphs randomly. However, after bees had gained experience with the rewarding model, and it was removed from the experiment, bees resampled preferentially the rewardless morph most similar to it in corolla colour. This is the first clear evidence, to our knowledge, that pollinators could select for floral mimicry. We suggest that floral mimicry can be a selective force acting on rewardless orchids, but only under some ecological conditions. In particular, we argue that selection on early-flowering rewardless orchids that receive visits from a large pool of naive pollinators will be weakly influenced by mimicry.     

Functional Significance of Labellum Pattern Variation in a Sexually Deceptive Orchid (Ophrys heldreichii): Evidence of Individual Signature Learning Effects

Mimicking female insects to attract male pollinators is an important strategy in sexually deceptive orchids of the genus Ophrys, and some species possess flowers with conspicuous labellum patterns. The function of the variation of the patterns remains unresolved, with suggestions that these enhance pollinator communication. We investigated the possible function of the labellum pattern in Ophrys heldreichii, an orchid species in which the conspicuous and complex labellum pattern contrasts with a dark background. The orchid is pollinated exclusively by males of the solitary bee, Eucera berlandi. Comparisons of labellum patterns revealed that patterns within inflorescences are more similar than those of other conspecific plants. Field observations showed that the males approach at a great speed and directly land on flowers, but after an unsuccessful copulation attempt, bees hover close and visually scan the labellum pattern for up to a minute. Learning experiments conducted with honeybees as an accessible model of bee vision demonstrated that labellum patterns of different plants can be reliably learnt; in contrast, patterns of flowers from the same inflorescence could not be discriminated. These results support the hypothesis that variable labellum patterns in O. heldreichii are involved in flower-pollinator communication which would likely help these plants to avoid geitonogamy.     

Should food‐deceptive species flower before or after rewarding species? An experimental test of pollinator visitation behaviour under contrasting phenologies

Many plant species reward their pollinators, whereas some species, particularly among orchids, do not. Similarity of floral cues between co‐flowering species influences how rapidly pollinators learn to avoid deceptive plants. This learning process, which affects the reproductive success of deceptive plants, may additionally depend on relative timing of flowering of sympatric rewarding and deceptive species. We tested the combined effects of corolla colour similarity and flowering order of rewarding and deceptive artificial inflorescences on visitation by naïve bumblebees. When deceptive inflorescences were offered after rewarding inflorescences, bumblebees visited them four times more often if both species were similar compared with when they were dissimilar. Pollinator visitation rate to deceptive inflorescences offered before rewarding inflorescences was intermediate and independent of similarity. Thus, early‐flowering deceptive species avoid the costs of dissimilarity with rewarding species. This mechanism may favour adaptive evolution of flowering phenology in deceptive species and explain why temperate deceptive orchids usually flower earlier than rewarding ones.     

Visual cues and foraging choices: bee visits to floral colour phases in Alkanna orientalis (Boraginaceae)

When a pollination vector is required, any mechanism that contributes to floral visitation will potentially benefit the reproductive fitness of a plant. We studied the effect of floral colour change in the desert perennial Alkanna orientalis on the foraging behaviour of the solitary bee Anthophora pauperata . Flowers changed colour over time from bright yellow (with moderate nectar reward) to pale yellow/white (with significantly lower nectar reward). Bee visitation was non-random with respect to colour phase availability within the flower population and was biased towards the more rewarding flowers. At plants where the availability of colour phases had been manipulated experimentally to produce 'bright' or 'pale' plants, bees visited significantly more flowers (and for longer periods) on the bright plants. The change of flower colour was not simply age-related; we observed variation in the temporal course of colour change and our data suggest that visitation, leading to deposition of cross-pollen, can accelerate the process. In subpopulations with limited pollinators, Alkanna can influence bees by using their colour-related foraging preferences to alter visitation patterns.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 427–435.     

Environmental determinants of genetic diversity in Caragana microphylla (Fabaceae) in northern China

Non‐rewarding orchids rely on various ruses to attract their pollinators. One of the most common is for them to resemble flowers sought by insects as food sources. This can range from generalized food deception to the mimicry of specific sympatric food plants. We investigated the basis of pollinator deception in the European food‐deceptive orchid Traunsteinera globosa, which has unusually compact flowerheads resembling those of sympatric rewarding species of Knautia and Scabiosa (Dipsacaceae), and Valeriana (Caprifoliaceae). Visual signals of T. globosa are similar in both fly and bee vision models to those of the sympatric food plants used in the choice experiments, but scent signals are divergent. Field experiments conducted in Austria and the Czech Republic showed that both naive and experienced (with respect to visitation of T. globosa) insect species approached the orchids at the same rate as food plants, but direct contact with orchid flowers was taxon specific. Flies were most easily duped into probing the orchid, and, in doing so, frequently received and deposited pollinaria, whereas most bees and butterflies avoided landing on orchid flowers. We conclude that T. globosa is a mimic of a guild of fly‐pollinated plants, but the ecological dependence of the orchid on its models remains to be fully tested. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180 , 269–294.     

Does bee or wasp mimicry by orchid flowers also deter herbivores?

General visual bee mimicry and specific chemical mimicry by flowers to solitary female bees or wasps are well known in several orchid genera, for example, the Mediterranean genus Ophrys, the Australian genera Cryptostylis and Chiloglottis, and the South-African Disa. This mimicry has been shown to attract solitary male bees or wasps, which are their species-specific pollinators. The visual and chemical signals are considered to be a type of deceptive pollination mechanism based on mimicry for the exploitation of perceptual biases of animals. We propose that in addition to this unique pollination mechanism, these plants exhibit another, rarely mentioned and practically forgotten, non-exclusive function of bee or wasp mimicry (Batesian mimicry). This mimicry may deter large mammalian herbivores, and possibly also insects from the plants and especially from their flowers by a type of visual and olfactory deceptive aposematism. While visiting the flowers, bees and wasps may add a Müllerian effect to this defense. We extend this hypothesis to many other rewarding flowers that are bee or wasp pollinated and propose that abundance of pollinating bees or wasps may deter herbivorous mammals and insects from the plants during their peak flowering season.     

Specialized pollination by carpenter bees in Calanthe striata (Orchidaceae), with a review of carpenter bee pollination in orchids

Calanthe striata has nectarless flowers that are self‐compatible, but pollinator dependent. Field observations showed that the flowers were pollinated exclusively by the carpenter bee Xylocopa appendiculata circumvolans, although the bees occasionally wasted pollen by delivering to the stigmatic surface pollinaria that retained their anther caps. Fruit set ratios at the population level varied spatiotemporally, but were generally low (8.3–17.3%). Calanthe striata blooms in spring when post‐overwintering carpenter bees have not yet started foraging for brood production. It can therefore exploit an abundance of opportunistic/naïve foragers. This timing may also increase the possibility of pollinator visits, because no rewarding co‐flowering plants are available in the orchid habitats. A literature review of Orchidaceae pollinated by carpenter bees revealed that at least 14 species of Orchidoideae and Epidendroideae have evolved flowers specialized for carpenter bee pollination. They typically have shallow pink/magenta flowers with a foothold for pollinators; pollinaria are attached to the head, ventral thorax or base of the middle legs of carpenter bees when they insert their heads and/or proboscises into flowers; pollination success is generally low, a probable consequence of the deceptive pollination systems. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 730–743.     

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

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.     

Generalized food deception: colour signals and efficient pollen transfer in bee‐pollinated species of Eulophia (Orchidaceae)

Non‐rewarding plants use a variety of ruses to attract their pollinators. One of the least understood of these is generalized food deception, in which flowers exploit non‐specific food‐seeking responses in their pollinators. Available evidence suggests that colour signals, scent and phenology may all play key roles in this form of deception. Here we investigate the pollination systems of five Eulophia spp. (Orchidaceae) lacking floral rewards. These species are pollinated by bees, notably Xylocopa (Anthophorinae, Apidae) or Megachile (Megachilidae) for the large‐flowered species and anthophorid (Anthophorinae, Apidae) or halictid (Halictidae) bees for the small‐flowered species. Spectra of the lateral petals and ultraviolet‐absorbing patches on the labella are strongly contrasting in a bee visual system, which may falsely signal the presence of pollen to bees. All five species possess pollinarium‐bending mechanisms that are likely to limit pollinator‐mediated self‐pollination. Flowering times extend over 3–4 months and the onset of flowering was not associated with the emergence of pollinators, some of which fly year round. Despite sharing pollinators with other plants and lacking rewards that would encourage fidelity, the Eulophia spp. exhibited relatively high levels of pollen transfer efficiency compared with other rewarding and deceptive orchids. We conclude that the study species employ generalized food deception and exploit food‐seeking bees. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 713–729.     

Pollination of the European food-deceptive Traunsteinera globosa (Orchidaceae): the importance of nectar-producing neighbouring plants

European food-deceptive orchids generally flower early in spring and rely on naïve pollinators for their reproduction. Some species however, flower later in the summer, when many other rewarding plants species are also in bloom. In dense flowering communities, deceptive orchids may suffer from competition for pollinator resources, or might alternatively benefit from higher community attractiveness. We investigated the pollination strategy of the deceptive species Traunsteinera globosa, and more specifically whether it benefited from the presence of coflowering rewarding species. We carried out a population survey to quantify the density and reproductive success of the orchid as well as the density of all coflowering species. Our results suggest that the deceptive orchid not only benefited from the presence of coflowering species, but that interestingly the density of the species Trifolium pratense was significantly positively correlated with the orchid's reproductive success. This species might simply act as a magnet species attracting pollinators near T. globosa, or could influence the orchid reproductive fitness through a more species-specific interaction. We propose that morphological or colour similarities between the two species should be investigated in more detail to decipher this pollination facilitation effect.     

Variable responses of hawkmoths to nectar-depleted plants in two native Petunia axillaris (Solanaceae) populations

Pollination success of deceptive orchids is affected by the density and distribution of nectar providing plant species and overall plant density. Here we extended the framework of how plant density can affect pollination to examine how it may promote the success of plant intraspecific cheaters. We compared hawkmoth behaviour in two native populations of Petunia axillaris, where we simultaneously offered rewarding and manually depleted P. axillaris. We asked whether pollinator foraging strategies change as a function of plant density and whether such changes may differentially affect nectarless plants. We observed the first choice and number of flowers visited by pollinators and found that in the dense population, pollinators visited more flowers on rewarding plants than on nectar-depleted plants. In the sparse population, such discrimination was absent. As we found no differences in nectar volume between plants of the two populations, the observed differences in plant density may be temporal. We reason that if differences were more permanent, an equivalent of the remote habitat hypothesis prevails: in a sparse population, cheating plants benefit from the absence of inter- and intraspecific competitors because pollinators tend to visit all potential resources. In a denser population, a pollinator’s optimal foraging strategy involves more selectivity. This would cause between-plant competition for pollinators in a pollinator-limited context, which applies to most hawkmoth-pollinated systems. We propose that nectar-provisioning of plants can be density-dependant, with cheaters able to persist in low density areas.     

Influence of functional traits on foraging behaviour and pollination efficiency of wild social and solitary bees visiting coffee (Coffea canephora) flowers in Uganda

An on-farm pollination experiment was conducted during the June–August and November–February blooming seasons of 2007 to 2008, in 30 small-scale coffee fields characterised by different habitat and vegetation types. The study was conducted in order to determine the best pollinator groups for coffee in Uganda and to collect relevant field information and determine the pollination efficiency of different bee species. Results indicate that across blooming seasons, coffee flowers were visited by 24–36 bee species. Hypotrigona gribodoi was the most frequent flower visitor, comprising over 60% of 5941 bee-visits recorded. Foraging rate and pollination speed varied among bee species. Solitary bees foraged on more flowers than social bees, but they spent less time per flower visited. Solitary bees visited more coffee trees and fields, but deposited less pollen, whereas social bees visited less trees and coffee fields in the landscape, but deposited more pollen on flowers. Fruit set was of 87%, 64% and 0.9%, respectively, in hand-cross pollination, open pollination and controlled-pollination treatments. Fruit abortion due to self-pollination was insignificant in this study. There was variability in pollination efficiency of different bee species. Pollination efficiency varied more significantly with sociality than with other bee functional traits and was not significantly influenced by tongue length and bee body size. Single-flower visits by social and solitary bees resulted in 89.7% and 68.14% fruit set, respectively. The most efficient bee species was Meliponula ferruginea (98.3%) followed by Meliponula nebulata (97.1%). Thus, very good pollinator species were wild social bees (mainly stingless bees) as opposed to honeybees and solitary bees that were previously reported to be the best pollinators of coffee in Panama and Indonesia. Morphological and anatomical characteristics of the bee pollen storage features may explain the difference in foraging behaviour activities and in pollination efficiency of social and solitary afrotropical bee species visiting lowland coffee in Uganda. In addition, pollination efficiency was influenced by land-use intensity, field management systems and habitat types found in the immediate surroundings of coffee fields, but not by coffee field size, coffee genotypes and mass blooming wild vegetation. It is recommended to farmers to adopt pollinator-friendly conservation and farming practices such as keeping an uncultivated portion (25%–30%) of their farms as pollinator reservoirs, protecting semi-natural habitats found in the vicinity of coffee fields, as well as promoting high on-farm tree cover to benefit a functionally diverse pollinator community.     

The adaptive significance of sensory bias in a foraging context: floral colour preferences in the bumblebee Bombus terrestris

Innate sensory biases could play an important role in helping na?ve animals to find food. As inexperienced bees are known to have strong innate colour biases we investigated whether bumblebee (Bombus terrestris) colonies with stronger biases for the most rewarding flower colour (violet) foraged more successfully in their local flora. To test the adaptive significance of variation in innate colour bias, we compared the performance of colour-na?ve bees, from nine bumblebee colonies raised from local wild-caught queens, in a laboratory colour bias paradigm using violet (bee UV-blue) and blue (bee blue) artificial flowers. The foraging performance of the same colonies was assessed under field conditions. Colonies with a stronger innate bias for violet over blue flowers in the laboratory harvested more nectar per unit time under field conditions. In fact, the colony with the strongest bias for violet (over blue) brought in 41% more nectar than the colony with the least strong bias. As violet flowers in the local area produce more nectar than blue flowers (the next most rewarding flower colour), these data are consistent with the hypothesis that local variation in flower traits could drive selection for innate colour biases.     

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

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

Bumble bees exhibit daily behavioral patterns in pollen foraging

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.     

Convergent evolution of floral signals underlies the success of Neotropical orchids

The great majority of plant species in the tropics require animals to achieve pollination, but the exact role of floral signals in attraction of animal pollinators is often debated. Many plants provide a floral reward to attract a guild of pollinators, and it has been proposed that floral signals of non-rewarding species may converge on those of rewarding species to exploit the relationship of the latter with their pollinators. In the orchid family (Orchidaceae), pollination is almost universally animal-mediated, but a third of species provide no floral reward, which suggests that deceptive pollination mechanisms are prevalent. Here, we examine floral colour and shape convergence in Neotropical plant communities, focusing on certain food-deceptive Oncidiinae orchids (e.g. Trichocentrum ascendens and Oncidium nebulosum) and rewarding species of Malpighiaceae. We show that the species from these two distantly related families are often more similar in floral colour and shape than expected by chance and propose that a system of multifarious floral mimicry—a form of Batesian mimicry that involves multiple models and is more complex than a simple one model–one mimic system—operates in these orchids. The same mimetic pollination system has evolved at least 14 times within the species-rich Oncidiinae throughout the Neotropics. These results help explain the extraordinary diversification of Neotropical orchids and highlight the complexity of plant–animal interactions.     

Anthecology of Orchis mascula (Orchidaceae)

Interactions between Orchis mascula L. ssp. mascula and anthophilous insects were studied mainly on the island of Öland, Sweden. The species is nectarless and acts by deceiving various bees (Hymenoptera, Apoidea). Temporary seeking/exploratory drives of bees for food–sources were exploited by means of superiority in floral display. A floral reflectance maximum at 440 nm (blue) largely determines the colour in the visual spectrum of bees. The floral scent is composed to about 90% of mono–terpenes. Nothing suggested mimesis of concurrent food–flowers either in colour or in scent. Anthesis covered a time period in late spring when (a) concurrent food–flowers for bees were rather few, (b) many bumble–bee queens (Bombus Latr. spp.) were inexperienced as regards food–flowers and had no foraging routines, (c) cuckoo bumble–bee females (Psithyrus Lep. spp.) recovery–fed on flowers after hibernation, (d) males of Eucera longicornis (L.) (Anthophoridae) patrolled far out from their nest–area, and when (e) many solitary bee species flew about. The pollinator fauna differed between sites, viz. either Bombus queens, Psithyrus females or E. longicornis males transported the majority of the pollinaria. The pollination system does not seem to be stabilised in the study areas. Floral morphology indicates that the plant's anthecological specialisation to bees as a group implies a graded unspecialisation to each species of bee in the legitimate pollinator group.