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Effect of floral symmetry on flower choice and foraging behaviour of bumble bees
Canadian Journal of Zoology
Abstract
Bumble bees are known to prefer symmetrical over asymmetrical flowers and bilateral over radial flower types. This study examined the basis of these preferences in three experiments with artificial flowers. The first experiment showed that flower-naive worker bees (Bombus impatiens) displayed no innate preference for symmetrical over asymmetrical or bilateral over radial flowers in choice tests. The second experiment tested whether bees showed a learning or memory bias for symmetrical over asymmetrical rewarding flowers when foraging on arrays of either bilateral or radial flower types. There was no evidence that bees learned or remembered symmetrical rewarding flowers better than asymmetrical rewarding flowers. The percentage of visits to rewarding flowers during test runs for bees foraging on arrays with bilateral flowers was consistently greater than on arrays with radial flowers. A third experiment examined the effect of nectar-guide symmetry on flower-handling and travel times. Bees were tested on homogeneous arrays with bilateral or radial flowers of either symmetrical or asymmetrical shapes and with symmetrical, asymmetrical, or no nectar guides. Guide symmetry had no effect on flower-handling or travel times. However, bees handled symmetrical flowers about 20% faster than asymmetrical flowers and bilateral flowers about 45% faster than radial flowers; travel times of bees on arrays with bilateral flowers were about 2.5 times faster than travel times of bees foraging on arrays of radial flowers.
... However, many plants can tolerate high levels of herbivory without substantial effects on individual fitness (Trumble et al., 1993;Lehtilä & Strauss, 1999), and leaf symmetry is thus not likely to be under strong natural selection. In contrast, symmetry of flowers can be selected for by pollinators (Møller & Eriksson, 1995;West & Laverty, 1998;Giurfa et al., 1999;Wignall et al., 2006). A preference of pollinators for symmetric flowers has even been proposed as an explanation for the repeated independent evolution of bilateral flowers from radially symmetric ancestors (Busch & Zachgo, 2009). ...
... However, the symmetry of the entire corolla has not yet been analysed. In an experiment with artificial flowers, symmetry of nectar guides did not influence pollinator behaviour, whereas symmetry of the flowers reduced handling time by pollinators (West & Laverty, 1998). For approaching insects, the shape of the large yellow flowers of M. guttatus may be visible before the nectar guide is recognized, and the symmetry of the central petal may influence the suitability for landing. ...
... Møller & Eriksson (1995) found that symmetric flowers contained more nectar than asymmetric flowers in some species but not others, and found no effect of FA on handling time in three plant species. In contrast, in a choice experiment with artificial flowers, bumblebees did not learn to prefer symmetric over asymmetric flowers when they contained more nectar, but handling time was shorter for symmetric than for asymmetric flowers (West & Laverty, 1998). In a study with M. guttatus, flowers of inbred plants were less attractive to pollinators and required longer handling time than flowers of outbred plants (Ivey & Carr, 2005). ...
Genetic and environmental disturbances are expected to increase developmental instability, which may result in higher fluctuating asymmetry (FA), i.e. small random deviations from symmetry. Plant leaves often do not show this pattern, possibly due to high phenotypic plasticity of leaf shape and low adaptive significance of leaf symmetry. In contrast, symmetry in many animal traits but also in flower shape is considered to be under selection, and FA in such traits may better reflect developmental instability. Using geometric morphometrics, I analysed the symmetry of flowers of inbred and outbred Mimulus guttatus (Phrymaceae) plants grown under five stress treatments with and without grass competition. Flower FA was not increased by abiotic stress, but by inbreeding and competition. As inbreeding and competition affected different principal components of flower FA, different mechanisms may be involved in their effects on FA. FA decreased with individual biomass particularly in selfed offspring, which suggests that inbreeding increased FA particularly when growth was limited by environmental or genetic constraints. Increased flower FA of inbred offspring may explain increased flower handling time and reduced pollinator preference for inbred plants in other M. guttatus studies, and could thus have important consequences for plant demography and plant–pollinator interactions.
... The terms "actinomorphy" and "zygomorphy" appear to be more ecological rather than structural ones: they distinguish flowers in which the position of an animal pollinator is strictly defined (as well as the flowers of pseudanthial inflorescences imitating petals), i.e., the zygomorphic ones, from all the other, i.e., actinomorphic, flowers [7,21]. Moreover, floral symmetry plays an important role in the visual perception of flower by a pollinator [7,9,13,[22][23][24]. Obviously, in this case, only the structure of the most conspicuous floral parts is significant; besides, the number of symmetry types distinguished by these animals cannot be high. ...
... Moreover, floral symmetry plays an important role in the visual perception of flower by a pollinator [7,9,13,[22][23][24]. Obviously, in this case, only the structure of the most conspicuous floral parts is significant; besides, the number of symmetry types distinguished by these animals cannot be high. Particularly, the insects were shown to be able to distinguish symmetrical vs asymmetrical flowers, and bilateral vs radial ones [22,23]. Tordylium aegyptiacum (L.) Poir., Figure 5D: Cyprus, Limassol area, around N 34 • Photographs of living plants were taken by M.S. Nuraliev with a Pentax Optio W80 (Pentax Corporation, Tokyo, Japan) digital camera. ...
Floral symmetry is widely known as one of the most important structural traits of reproductive organs in angiosperms. It is tightly related to the shape and arrangement of floral parts, and at the same time, it plays a key role in general appearance (visual gestalt) of a flower, which is especially important for the interactions of zoophilous flowers with their pollinators. The traditional classification of floral symmetry divides nearly all the diversity of angiosperm flowers into actinomorphic and zygomorphic ones. Within this system, which is useful for ecological studies, many variations of symmetry appear to be disregarded. At the same time, the diversity of floral symmetry is underpinned not only by ecological factors, but also by morphogenetic mechanisms and constraints. Sometimes it is not an easy task to uncover the adaptive or developmental significance of a change of the floral symmetry in a particular lineage. Using the asterid order Apiales as a model group, we demonstrate that such changes can correlate with the merism of the entire flower or of its particular whorl, with the relative orientation of gynoecium to the rest of the flower, with the presence of sterile floral elements and other morphological characters. Besides, in some taxa, the shape and symmetry of the flower change in the course of its development, which should be taken in consideration in morphological comparisons and evaluations of synapomorphies in a particular clade. Finally, we show that different results can be obtained due to employment of different approaches: for instance, many flowers that are traditionally described as actinomorphic turn out to be disymmetric, monosymmetric, or asymmetric from a more detailed look. The traditional method of division into actinomorphy and zygomorphy deals with the general appearance of a flower, and mainly considers the shape of the corolla, while the geometrical approach handles the entire three-dimensional structure of the flower, and provides an exact number of its symmetry planes.
... A radially symmetric pattern has multiple axes of symmetry, though it is not clear exactly how many axes are needed before a pattern can be labeled as radially symmetric. For example, two circles within one another (Møller & Sorci, 1998) and six-axis (Wignall, Heiling, Cheng, & Herberstein, 2006) or even three-axis (West & Laverty, 1998) symmetric patterns have been called radially symmetric. A bilaterally symmetric pattern is defined as the simplest type of symmetry along a single axis. ...
... Prior literature has been mixed on the effect of symmetry on choice behavior. Some experiments appear to suggest that an unlearned preference is a possibility (Giurfa, Eichmann, & Menzel, 1996; Rodríguez et al., 2004), while others suggest symmetry to be an effect of learning dynamics (Plowright et al., 2011; West & Laverty, 1998). Experiments examining the flower displays highlight the relevance of symmetry, although inferences about pollinators' information-processing biases are not possible to interpret from this perspective (Møller & Sorci, 1998; Neal et al., 1998). ...
The behavioral experiment herein tests the computational load hypothesis generated by an unsupervised neural network to examine bumblebee (Bombus impatiens) behavior at 2 visual properties: spatial frequency and symmetry. Untrained "flower-naïve" bumblebees were hypothesized to prefer symmetry only when the spatial frequency of artificial flowers is high and therefore places great information-processing demands on the bumblebees' visual system. Bumblebee choice behavior was recorded using high-definition motion-sensitive camcorders. The results support the computational model's prediction: 1-axis symmetry influenced bumblebees' preference behavior at low and high spatial frequency patterns. Additionally, increasing the level of symmetry from 1 axis to 4 axes amplified preference toward the symmetric patterns of both low and high spatial frequency patterns. The results are discussed in the context of the artificial neural network model and other hypotheses generated from the behavioral literature. (PsycINFO Database Record
(c) 2015 APA, all rights reserved).
... Foragers have innate abilities for discriminating colour and retain certain colour cues more effectively than others (Frisch, 1967 andMenzel, 1990). Also important as visual stimuli are floral shape or form (Free, 1970 andLamb and, pigmentation patterns (Petrikin and Wells, 1995) and floral symmetry (West and Laverty, 1998). Although colour is the main stimulus used by bees to locate flowers at a distance, odour is also used in flower selection (Beker et al., 1989 andKirchner andGrasser, 1998). ...
... Pollinators adjust the number and duration of flower visits depending on the amount and quality of pollen or nectar available (e.g., Robertson et al., 1999;Cnaani et al., 2006;Brunet et al., 2015), costly traits that are often reduced after inbreeding (Carr and Dudash, 1995;Ouborg et al., 2000;Kariyat et al., 2021) and in plant species that rely more on self-pollination (Sicard and Lenhard, 2011). Pollinators also prefer flowers with a short "handling time", which is influenced by the size and symmetry of flowers (West and Laverty, 1998), two traits that have been found to be affected by inbreeding (Ivey and Carr, 2005;Sandner, 2020). Inbreeding has also been found to reduce pollinator visitation via changes in flower scent (Haber et al., 2019;Kariyat et al., 2021;Schrieber et al., 2021). ...
Premise:
Ex situ cultivation is important for plant conservation, but cultivation in small populations may result in genetic changes by drift, inbreeding or unconscious selection. Repeated inbreeding potentially influences not only plant fitness, but also floral traits and interactions with pollinators, which has not yet been studied in an ex situ context.
Methods:
We studied the molecular genetic variation of Digitalis lutea L. from a botanic garden population cultivated for 30 years, a frozen seed bank conserving the original genetic structure, and two current wild populations including the source population. In a common garden we studied the effects of experimental inbreeding and between-population crosses on performance, reproductive traits and flower visitation of plants from the garden and a wild population.
Results:
Significant genetic differentiation was found between the garden population and the wild population from which the seeds had originally been gathered. After experimental selfing, inbreeding depression was only found in germination and leaf size of plants from the wild population, indicating a history of inbreeding in the smaller garden population. Moreover, garden plants flowered earlier and showed floral traits related to selfing, whereas wild plants showed traits related to attracting pollinators. Bumblebees visited more flowers of outbred than inbred plants and of wild than garden plants.
Conclusions:
Our case study suggests that high levels of inbreeding during ex situ cultivation can influence reproductive traits and thus interactions with pollinators. Together with the effects of genetic erosion and unconscious selection this may affect the success of reintroductions into natural habitats. This article is protected by copyright. All rights reserved.
... However, landing is only the first accomplishment towards successful foraging and does not guarantee that any naïve worker will successfully handle the flower to find and take up the reward. After landing, other visual signals, such as colour patterning, have been reported to promote effective exploration and handling behaviours, as well as increase the speed at which workers locate food during a first visit, helping the development of efficient foraging strategies (Leonard & Papaj, 2011;Orbán & Plowright, 2014;Waser & Price, 1983;West & Laverty, 1998). ...
Flying insects encounter a considerable amount of multisensorial information during their first foraging trip and need to extract and process relevant cues to efficiently navigate their environment and locate food sources. Previous studies used static stimuli to investigate visual information processing during flight and the role of floral features on detection, landing, and flower handling behaviours. However, bees come across visual information sequentially, while sampling the visual scene and presenting visual features that change after landing would allow further understanding of the chronological aspect of visual information processing. Here, we describe a new methodology that uses the ShadowSense™ Multitouch technology to present interactive floral displays where a change in visual features is triggered upon a bee's landing. Two colonies of flower naïve bumblebees (Bombus impatiens) were exposed to unicoloured and bicoloured unrewarded floral images in which floral guides in the form of dummy stamens were added, removed, or remained unchanged in the centre upon landing. Our findings confirm preference by flower-naïve bumblebees for bicoloured flowers and corroborate that small central visual guides direct the place of landing. Therefore, we establish proof-of-concept of this new methodology for bee research by reproducing previously demonstrated behaviours and by reporting that bees react to a change in visual information on the touchscreen. To our knowledge, this is the first research providing a touchscreen technology that can reliably be used with bees. While its efficiency with similar-sized insects is yet to be confirmed, this technology provides new approaches for research on visual information processing as well as various behaviours in insects.
... They have also been noticed that these insects relatively favour symmetrical flowers than asymmetrical ones (Moler, 1995;Moller and Sorci, 1998). And from the symmetry the bilateral symmetry is chosen over radial symmetry (West and Laverty, 1998). Raina et al. 2019 observed that in the upper Indian Himalayas predominantly the trees of less alpine meadows between 3500m to 5400m asl and the vegetation that is conserved predominantly by the species of bumblebees include wide range of herbs, shrubs, grasses and medicinal plants having small flowers. ...
Bumblebees are one among the anthophilous form and play a significant role in the pollination of major agricultural crops like medicinal, aromatic, ornamental and various other horticultural plants. They are abundant and mostly confined to flowers present in the temperate, alpine and arctic climates of the northern continents. The bumblebees are considered as most important pollinators and are mainly responsible for the conservation of high altitude vegetation germplasm where other insect pollinators are very much limited. They are more successful pollinators and can visit large number of flowers per minute than other bees and are perfect for picking up and transferring appreciable amount of compatible pollen to flowers and thus perform buzz pollination. It is quite evident that the population of bumblebee is gradually declining throughout the globe for the last 7 decades due to agricultural intensification, habitat loss, deforestation, overgrazing, pesticide poisoning and climate change. The present paper addresses this issue on the basis of literature survey.
... Both hummingbirds (Salasphorus platycercus and S. rufus) and bumblebees (Bombus appositus, B. nevadensis and B. flavifrons) show a preference for visually patterned flowers of montane larkspur (Delphinium nelsonii) compared to their albino morphs (Waser & Price, 1985). It is possible that these guides may also act to reinforce flower constancy, whereby foragers preferentially visit flowers of a single species (Waser, 1986), as these guides could act as an additional trait which can be used to distinguish flowers (West & Laverty, 1998;Fauria et al., 2002). Floral guides can also increase the relative frequency of legitimate visits by decreasing nectar robbing on flowers which are at risk (Leonard et al., 2013), highlighting how the presence of floral guides can have direct benefits to plant fitness. ...
Many floral displays incorporate complex contrasting stimuli patterns in visual, olfactory and other sensory modalities. These 'floral guides' can increase pollen transfer rates and visitation rates for flowers while reducing the search times of pollinators. Although these guides are important in mediating the relationship between plants and pollinators, little is known about the evolution of these guides or the conditions needed for them to evolve. Here we use a novel approach by applying a genetic algorithm, a modelling method inspired by biological evolution, to investigate floral guide evolution. Specifically, we examine the ways in which pollinator behaviour can affect the evolution of radiating floral guides and what conditions are necessary for this development. The results suggest that flower size and pollinator directionality, starting location and movement type affect the development of radiating guides. A preference for cues over a lack of cue is also necessary for this development. These findings suggest that radiating floral guides can evolve independently of specific perceptual biases by the pollinator other than a preference for cues over their absence. Despite these findings, we are aware of the limitations of computational models, and hope that these findings inform and motivate future models and empirical studies.
... For bumblebees, the handling speed for symmetrical flowers is 20% faster than for asymmetric flowers, and 20% and 45% faster for bilateral and radial flowers, respectively. This increases the number of flowers visited per unit of time and increases pollination efficiency (West and Laverty, 1998). Floral morphology also plays a role . ...
Développer des systèmes de culture respectant voire favorisant la biodiversité est un enjeu important pour les agronomes dans le contexte sociétal actuel. Pour ce faire, ceux-ci ont besoin de méthodes prédictives d’évaluation des effets des pratiques agricoles sur la biodiversité pour caractériser et évaluer les systèmes étudiés. Les écologues reconnaissent la nécessité d’aborder la biodiversité non seulement comme la richesse spécifique mais aussi par le biais des services écosystémiques qu’elle peut rendre à l’homme. Il existe de nombreuses propositions d’indicateurs de biodiversité mais ceux-ci reposent, soit sur des mesures de diversité au sein de groupes taxonomiques, soit sur des variables de pratiques et ne sont pas prédictifs. L’objectif de la thèse a été de concevoir un indicateur prédictif des effets des pratiques agricoles sur la biodiversité et ses services. Pour effectuer ce travail, nous avons choisi de nous baser sur la diversité floristique en bordure de champ et sur les services qui lui sont liés : la valeur patrimoniale, enjeu sociétal et la pollinisation, enjeu majeur pour l’agriculture. Nous avons structuré ce travail en trois étapes. En premier lieu, nous avons sélectionné les pratiques agricoles connues pour leurs effets combinés sur la biodiversité et ses services, identifié leurs natures et estimé l’ampleur de leurs effets à l'échelle de la bordure de champ. Dans une seconde étape, nous avons intégré par expertise la connaissance sur ces effets dans un modèle opérationnel.A la suite de ce travail de conception, nous avons évalué la sensibilité, et la qualité prédictive du modèle en le confrontant à un jeu de données mesurées sur le terrain dans le cadre de la thèse ou acquises dans le cadre d’autres travaux. Enfin, nous avons transformé les sorties du modèle (probabilité de présence pour 338 espèces) en un indicateur en les agrégeant en une valeur synthétique. Nous avons positionné ensuite celle-ci par rapport à des références que nous avons sélectionnées, et sur une échelle de notation lisible. Le développement de cet indicateur prédictif opérationnel permettra aux agronomes d’évaluer les effets positifs et négatifs des pratiques agricoles, et d’identifier des pratiques innovantes respectueuses de la biodiversité et de ses services. L’indicateur pourra être utilisé avec d’autres indicateurs environnementaux, économiques et sociaux dans la perspective de l’étude de la durabilité des exploitations agricoles en grandes cultures.
... Some specialized bee pollinators are only attracted by monosymmetric flowers (Giurfa et al. 1996;West and Laverty 1998;Giurfa et al. 1999). In a context of monosymmetry, the probability of success is increased, once flowers promote the approach of pollinators from a particular orientation plane (Cubas 2004). ...
Floral monosymmetry appears to be a derived condition, arising independently many times, with a multiplicity of forms, and related to both, pollinator and plant diversification. It reduces interference between sexual functions in flowers and increases cross-pollination and allogamy. But since the description and assessment of the functioning of those floral features depend on fresh material and field observations, the number of groups thoroughly observed is limited. In the mostly Neotropical and actinomorphic Melastomataceae, monosymmetric flowers seem to be derived and the resulting herkogamy may constitute a mechanism to avoid anther–stigma interference and self-pollination. Here we studied Tococa guianensis, a Neotropical widespread shrub or treelet well known for its leaf–domatia ant interaction, but still lacking details on its breeding biology. We studied a population in Uberlândia, Central Brazil, observing floral biology features, diversity of visitors and breeding system. Flowers showed diurnal anthesis and a single-day life span. Pollen was the only floral resource offered, and poricidal anthers were clustered in the centre of the flower, while style was bent away from flower axis creating a transient herkogamy and flower monosymmetry. Style moves towards the floral axis during the day facilitating pollination. To date we do not know other Tococa species displaying such stylar features, which may be an intermediate form between the actinomorphic Miconieae and specialized zygomorphic Tococa. Contrasting with previous studies, the self-incompatibility found in T. guianensis indicates that transient herkogamy may function to avoid stigma clogging with self-pollen and allow flexible use of specialized buzz-pollinating bees.
... The "more threatened" plants examined here were found to have more frequently bilaterally symmetrical flowers (44.3% of the "more threatened" plants) compared to the "less threatened" (28%). Bilateral floral symmetry is suggested to provide multiple advantages for a plant, such as higher visitation, more efficient recognition and faster handling by pollinators and higher outcrossing rates than radial symmetry [78][79][80]. Moreover, in a community context floral symmetry has been shown to predict differences in pollinator visitation within a plant-pollinator network [81]. ...
The architectural complexity of flower structures (hereafter referred to as floral complexity) may be linked to pollination by specialized pollinators that can increase the probability of successful seed set. As plant-pollinator systems become fragile, a loss of such specialized pollinators could presumably result in an increased likelihood of pollination failure. This is an issue likely to be particularly evident in plants that are currently rare. Using a novel index describing floral complexity we explored whether this aspect of the structure of flowers could be used to predict vulnerability of plant species to extinction. To do this we defined plant vulnerability using the Red Data Book of Rare and Threatened Plants of Greece, a Mediterranean biodiversity hotspot. We also tested whether other intrinsic (e.g. life form, asexual reproduction) or extrinsic (e.g. habitat, altitude, range-restrictedness) factors could affect plant vulnerability. We found that plants with high floral complexity scores were significantly more likely to be vulnerable to extinction. Among all the floral complexity components only floral symmetry was found to have a significant effect, with radial-flower plants appearing to be less vulnerable. Life form was also a predictor of vulnerability, with woody perennial plants having significantly lower risk of extinction. Among the extrinsic factors, both habitat and maximum range were significantly associated with plant vulnerability (coastal plants and narrow-ranged plants are more likely to face higher risk). Although extrinsic and in particular anthropogenic factors determine plant extinction risk, intrinsic traits can indicate a plant's proneness to vulnerability. This raises the potential threat of declining global pollinator diversity interacting with floral complexity to increase the vulnerability of individual plant species. There is potential scope for using plant-pollinator specializations to identify plant species particularly at risk and so target conservation efforts towards them.
... The bodies of most animals have a bilateral (left-right) symmetry. Flowers often have radially or bilaterally symmetric shapes, which have been found to aid bumble bees in their foraging process [7]. In general, one can find symmetries from a minuscule scale such as in atomic or molecular lattices, all the way to the cosmic scale such as in galaxies that are hundreds of thousands light years in diameter across. ...
In this thesis we study symmetric structures in Hilbert spaces known as
symmetric informationally complete positive operator-valued measures
(SIC-POVMs), mutually unbiased bases (MUBs), and MUB-balanced states. Our tools
include symmetries such as the Weyl-Heisenberg (WH) group symmetry, Clifford
unitaries, Zauner symmetry, and Galois-unitaries (g-unitaries), which are
non-linear operators defined to generalize the notion of anti-unitaries.
... Angiosperm flowers are predominantly symmetric or very rarely asymmetric [17] (see Fig. 1i). It was shown that some pollinators (bees, for instance) are only attracted by symmetric flowers [24] [25] [26]. A symmetric flower can be polysymmetric, disymmetric (with two perpendicular symmetry planes) or monosymmetric (Fig. 1). ...
The genetic determinants of the organisation and variation of the flower, a striking feature of the angiosperms, are only beginning to be deciphered. Floral symmetry has recurrently evolved among angiosperms, zygomorphy (monosymmetry) being a key innovation due to its role in the plant-pollination interaction. As such, it represents a case study for evo-devo. Phylogenetic comparative studies conducted in two eudicot clades, the Ranunculales and the Asteridae sensu APGII, have shown that the evolution of this trait is dependent upon the architectural context of the flower. Genetic and developmental bases of zygomorphy have been investigated in several unrelated model species. In all these species, zygomorphy appears to be controlled, at least partially, by genes belonging to the TCP gene family of transcription factors and named CYC-like genes. Exploring the molecular bases of zygomorphy in non-model species spanning the diversity of angiosperms, but also the developmental processes involved, are now essential to understand the evolution of floral symmetry.
... Healy/Hurly regular intervals. Various invertebrates fulfill these criteria and have proved to be useful test subjects, e.g., symmetry learning in honey bees [Giurfa et al., 1996], in bumble bees [West and Laverty, 1998], navigation in desert ants [Collett and Zeil, 1998]. Invertebrates are also much more easily brought into and tested in a laboratory setting than many vertebrate species [see reviews in Collett and Zeil, 1998; Weiss, 2001]. ...
Behavioral ecologists, well versed in addressing functional aspects of behavior, are acknowledging more and more the attention they need also to pay to mechanistic processes. One of these is the role of cognition. Song learning and imprinting are familiar examples of behaviors for which cognition plays an important role, but attention is now turning to other behaviors and a wider diversity of species. We focus here on work that investigates the nature of spatial learning and memory in the context of behaviors such as foraging and food storing. We also briefly explore the difficulties of studying cognition in the field. The common thread to all of this work is the value of using psychological techniques as tools for assessing learning and memory abilities in order to address questions of interest to behavioral ecologists.
Pollinator behavior is vital to plant-pollinator interactions, affecting the acquisition of floral rewards, patterns of pollen transfer, and plant reproductive success. During buzz pollination, bees produce vibrations with their indirect flight muscles to extract pollen from tube-like flowers. Vibrations can be transmitted to the flower via the mandibles, abdomen, legs, or thorax directly. Vibration amplitude at the flower determines the rate of pollen release and should vary with the coupling of bee and flower. This coupling often occurs through anther biting, but no studies have quantified how biting affects flower vibration. Here, we used high-speed filmography to investigate how flower vibration amplitude changes during biting in Bombus terrestris visiting two species of buzz-pollinated flowering plants: Solanum dulcamara and Solanum rostratum (Solanaceae). We found that floral buzzing drives head vibrations up to 3 times greater than those of the thorax, which doubles the vibration amplitude of the anther during biting compared with indirect vibration transmission when not biting. However, the efficiency of this vibration transmission depends on the angle at which the bee bites the anther. Variation in transmission mechanisms, combined with the diversity of vibrations across bee species, yields a rich assortment of potential strategies that bees could employ to access rewards from buzz-pollinated flowers.
Plants have evolved complex flowers that differ in visual traits such as colour, size and shape, to attract pollinators. However, pollinators seem to respond differently to individual traits. Our objective was to unravel the effect of individual traits and their interplay in forming pollinator preferences. We measured the preferences of naive drone flies, Eristalis tenax (Syrphidae), for artificial flowers differing in colour, size and flower symmetry, in controlled conditions to untangle the effects of individual traits on pollinator behaviour. Eristalis tenax showed the highest selectivity for colour, followed by size, and only moderate selectivity in relationship to flower symmetry. Flower colour interacted with flower size, in that yellow colour was generally preferred, particularly when the flowers were large in comparison to other forms. Our results suggest that preferences for flower traits are structured, which might suggest that there have been different evolutionary pressures on individual floral traits.
Impatiens edgeworthii is an important plant species endemic to Western Himalaya. In this species male reproductive organs conceal the stigma – seat of pollen reception during male phase therefore acts as barrier for self-pollination. In addition the stigma become receptive only after the androecium of the same flower is shed and then receptive stigma become exposed. This unique type of dichogamy and arrangement of essential organs are contrivance for cross-pollination in the species. The large showy flowers, production of large quantities of nectar, protandry, presence of nectar guides, ornamented exine sculpturing, high pollen to ovule ratio points towards cross-pollinated mode of reproduction is operative in this species. This was also established by breeding experiments. Our study may prove useful in conservation of this Himalayan endemic plant species and also useful in understanding the evolution of breeding system in the genus.
(1) The research conducted including its rationale: Floral traits are recognized to evolve under selections of abiotic factors and biotic factors. Complex zygomorphic flowers usually face horizontally. It has been proved that a horizontal orientation facilitates pollinator recognition and pollination efficiency, but its significance in adaption to abiotic factors remained unknown.
(2) Central methods applied: The floral orientation of Abelia × grandiflora naturally varies around horizontal (with an angle of ‐30°~33° between floral main axis and the horizontal), and we examined whether floral orientation affected flower thermal condition, response to rain and pollination.
(3) Key results: Results showed that floral orientation has no effect on the diurnal variation of flower temperature. The anthers of all flower orientations got wet by rainfall, but the inclined upward flowers was filled with significantly more rain water. The horizontal flowers received significantly more visitation by hawkmoth and stigmatic pollen load. By contrast, the upward orientation reduced pollination precision, and facing downward decreased pollinator attraction.
(4) Main conclusions including key points of discussion: The study indicate that the horizontal flowers may evolved as a trade‐off of rain protection and pollination. Zygomorphic flowers which deviate from horizontal orientation may have lower fitness because of flower flooding by rain and decreased pollen transfer.
The foraging behavior of bees is a complex phenomenon that depends on numerous physical features of flowers. Of particular importance are accessibility of floral rewards, floral proportions, symmetry and orientation. The flowers of Roepera are characterized by the presence of staminal scales (SS), which play an important role in nectar protection. We studied two species of Roepera with different symmetry and flower orientation, which are mainly visited by honeybees (Apis mellifera). We aimed to show how the foraging behavior of honey bees is affected by the function of SS, floral symmetry and orientation. The foraging behavior was documented by video photography. Handling time, access to nectar, percentage of pollen/nectar foraging, percentage of pollen contact and pollen deposition site on the honey bee's body were assessed. The morphometric features of the honey bees and flowers were analyzed. We found that the SS restricted pollinator access to nectar. Our results indicated consistency of visitation patterns in zygomorphic, laterally oriented flowers of R. fuscata versus random patterns in actinomorphic, diversely oriented flowers of R. leptopetala. The relative proportions of SS and proboscis length appear to be crucial for the success of pollinators. The directionality of the honey bees' movement, together with the different positioning of reproductive organs, plays an important role in the accuracy of pollen transfer and pollination efficiency. We found that the staminal scales restricted pollinator access to nectar. Our results indicated consistency of visitation patterns in zygomorphic, laterally oriented flowers of R. fuscata versus random patterns in actinomorphic, diversely oriented flowers of R. leptopetala. The directionality of the honey bees' movement, together with the different positioning of reproductive organs, plays an important role in the accuracy of pollen transfer and pollination efficiency.
Bombus rufofasciatus SMITH is a Tibetan species, widely distributed in the Oriental region. It is a medium tongued species abundant in both the north-east and north-west Indian Himalaya, covering an altitude range from 2400 to 4200 m. Because of its abundance and very wide distribution, it is associated with a sizeable number of host plants. Males and workers are similar in colour pattern, but the queen is a little different. The species shows a preference for highaltitude mountain slopes and is found in abundance in the open meadows of Affarwatt, Sheeshnag, Daksum, the Razdan Pass and the Lahul-spiti Valley of Himachal Pradesh in the north-western Himalaya. For preference it forages on Aconitum spp. (Ranunculaceae), Trifolium spp. (Papilionaceae), Cirsium spp. (Asteraceae) and certain members of Lamiaceae. Due emphasis has been laid on its detailed taxonomic descriptions, synonymy, host plants, pollination ecology, distribution pattern and illustrations. 51 food plants of this species have been recorded for the first time from the areas under study.
This study examines the mechanism underlying one way in which bumblebees are known to develop a preference for symmetric patterns: through prior non-differential reinforcement on simple patterns (black discs and white discs). In three experiments, bees were given a choice among symmetric and asymmetric black-and-white non-rewarding patterns presented at the ends of corridors in a radial maze. Experimental groups had prior rewarded non-discrimination training on white patterns and black patterns, while control groups had no pre-test experience outside the colony. No preference for symmetry was obtained for any of the control groups. Prior training with circular patterns highlighting a horizontal axis of symmetry led to a specific subsequent preference for horizontal over vertical symmetry, while training with a vertical axis abolished this effect. Circles highlighting both axes created a general avoidance of asymmetry in favour of symmetric patterns with vertical, horizontal or both axes of symmetry. Training with plain circles, but not with deformed circles, led to a preference for symmetry: there was no evidence that the preference emerged just by virtue of having attention drawn away from irrelevant pattern differences. Our results point to a preference for symmetry developing gradually through first learning to extract an axis of symmetry from simple patterns and subsequently recognizing that axis in new patterns. They highlight the importance of continued learning through non-differential reinforcement by skilled foragers. Floral guides can function not only to guide pollinators to the source of reward but also to highlight an axis of symmetry for use in subsequent floral encounters.
Floral displays are often composed of areas of contrasting stimuli which flower visitors use as guides, increasing both foraging efficiency and the likelihood of pollen transfer. Many aspects of how these displays benefit foraging efficiency are still unexplored, particularly those surrounding multimodal signals and the spatial arrangement of the display components. We compare the nectar discovery times of forager bumblebees (Bombus terrestris) when presented with artificial flowers with unimodal or compound displays of visual and/or olfactory stimuli, positioned in either radiating or non-radiating arrangements. We found that the addition of individual display components from either modality reduces nectar discovery time but there was no time benefit to bimodal displays over unimodal displays or any benefit to radiating stimuli arrangements over non-radiating arrangements. However, preference tests revealed a time advantage to radiating unimodal visual patterns over non-radiating unimodal visual patterns when both types were displayed simultaneously. These results suggest that the benefits of multimodal stimuli arrangements to pollinators are unrelated to benefits in nectar discovery time. Our results also suggest that spatial patterns of scent can be used as nectar guides and can reduce nectar discovery times without the aid of visual stimuli.
Despite the importance of wild pollination as an ecosystem service, little is known about the spatial and temporal variation of pollination services. Variation in insect pollinator emergence or forb flowers can lead to inconsistent delivery of pollination service to the forb community. A variety of factors, such as air temperature, flower abundance, pollinator abundance, and forb species richness influence the stability of pollination service. All of these factors exhibit spatial and temporal variability. Furthermore, anthropogenic disturbances endanger the persistence of pollination service. To assess the variability of pollination we compared the number of insect flower visits at different locations throughout the summer for two consecutive years in Dalbay Valley, Mongolia. Within this spatio-temporal framework, we investigated the stability of plant-pollinator networks and the effect of ungulate grazing cessation on pollinator visits.
Flower visits, forb flower abundance, and measures of plant-pollinator network stability varied greatly over space and time. Hymenoptera visits were positively correlated with only network specialization and Diptera visits were positively correlated with only network nestedness. The exclusion of ungulate grazing altered the composition and abundance of both the forb species and flower visitor communities, but there was no difference in total flower visits between grazed and ungrazed plots. Our results suggest the forb and pollinator community may persist despite the removal of the consistent ungulate grazing pressure. Furthermore, the contribution towards network stability may not be synergistic. Hymenoptera visits were associated with increased network specialization, which tends to lower plant-pollinator network resilience against perturbations, while Diptera visits were associated with increased nestedness, which tends to increase network resilience.
Bilateral symmetry has evolved from radial symmetry in several floral lineages, and multiple hypotheses have been proposed to account for the success of this floral plan. One of these hypotheses posits that bilateral symmetry (or, more generally, a reduced number of planes of floral symmetry) allows for more precise pollen placement on pollinators. Greater precision would maximize the efficacy of pollen transfer to conspecifics, while minimizing reproductive interference amongstplant species. Despite the intuitiveness of this hypothesis, it has little experimental support. Here, we tested whether a reduction in the number of floral planes of symmetry (as in the transition from radial to bilateral symmetry) increases the potential precision of pollen placement. We analyzed video recordings of bumblebees (Bombus impatiens) visiting artificial flowers to determine whether consistency in flower entry angle differed between radial (round) and disymmetric (rectangular) “flowers”. We observed more consistent entry angles for disymmetric flowers than for radial flowers, with entry angles to radial flowers 43% more variable on average (standard deviations of 30° vs. 21°). Bees trained on flowers with an intermediate (square) morphology exhibited a slight, non-significant preference for radial symmetry over disymmetry. Our results show that disymmetry—an evolutionarily intermediate form of floral symmetry—has the potential to increase pollen transfer to conspecific stigmas, relative to radial symmetry. Thus, evolutionary reduction in the number of planes of floral symmetry likely provides benefits in terms of pollen delivery, as suggested by the pollen-placement-accuracy hypothesis. These findings offer insight into the evolution of floral symmetry.
Much of the literature on foraging behaviour in bees focuses on what they learn after they have had rewarded experience with flowers. This review focuses on how honeybees and bumblebees are drawn to candidate food sources in the first place: the foundation on which learning is built. Prior to rewarded foraging experience, flower-nave bumblebees and honeybees rely heavily on visual cues to discover their first flower. This review lists methodological issues that surround the study of flower-nave behaviour and describes technological advances. The role of distinct visual properties of flowers in attracting bees is considered: colour, floral size, patterning and social cues. The research reviewed is multi-disciplinary and takes the perspectives of both the bees and the plants they visit. Several avenues for future research are proposed.
1. Many floral displays are visually complex, transmitting multi‐coloured patterns that are thought to direct pollinators to nectar rewards. These ‘nectar guides’ may be mutually beneficial, if they reduce pollinators’ handling time, leading to an increased visitation rate and promoting pollen transfer. Yet, many details regarding how floral patterns influence foraging efficiency are unknown, as is the potential for pollinator learning to alter this relationship.
2. We compared the responses of bumblebee ( Bombus impatiens Cresson) foragers to artificial flowers that either possessed or lacked star‐like patterns. By presenting each bee with two different foraging scenarios (patterned flowers rewarding/plain flowers unrewarding, plain flowers rewarding/patterned flowers unrewarding) on different days, we were able to assess both short‐ and long‐term effects of patterns on bee foraging behaviour.
3. Bees discovered rewards more quickly on patterned flowers and were less likely to miss the reward, regardless of whether corollas were circular or had petals. Nectar guides’ effect on nectar discovery was immediate (innate) and persisted even after experience, although nectar discovery itself also had a learned component. We also found that bees departed patterned flowers sooner after feeding. Finally, when conditions changed such that flowers no longer provided a reward, bees visited the now‐unrewarding flowers more persistently when they were patterned.
4. On the time‐scale of a single foraging bout, our results provide some of the first data on how pollinators learn to forage efficiently using this common floral trait. Our bees’ persistent response to patterned flowers even after rewards ceased suggests that, rather than being consistently mutually beneficial to plant and pollinator, nectar guide patterns can at times promote pollen transfer for the plant at the expense of a bee’s foraging success.
The degree to which fine-scaled variation in floral symmetry is associated with variation in plant fitness remains unresolved, as does the question of whether floral symmetry is in itself a target of pollinator-mediated selection. Geranium robertianum (Geraniaceae) is a broadly distributed species whose five-petaled flowers vary widely with respect to their degree of rotational asymmetry. In this study, we used a naturally occurring population of plants to investigate whether floral rotational asymmetry and leaf bilateral symmetry were phenotypically correlated with a series of fitness-related traits, and also used an experimental array with model flowers to investigate the preference of insect visitors for varying degrees of floral size and symmetry. We found that leaf asymmetry was not associated with any of the phenotypic traits measured, and that the degree of floral rotational asymmetry was strongly associated with decreased flower size and decreased pollen production. Our experimental arrays showed that insect visitors did not discriminate among model flowers on the basis of size or symmetry alone; however, insect visitors preferentially visited smaller, symmetric model flowers over larger, severely asymmetric model flowers. Taken together, our results suggest that floral and leaf symmetry in G. robertianum are not likely strong indicators of phenotypic quality, and that floral symmetry is unlikely to be a target of pollinator-mediated selection. However, the relationship between floral asymmetry and pollen production may provide a role for fecundity selection on symmetry in this species. These data importantly add to the growing literature on the adaptive nature of floral symmetry in the wild.
The effects of floral herbivores on floral traits may result in alterations in pollinator foraging behaviour and subsequently influence plant reproductive success. Fed-upon plants may have evolved mechanisms to compensate for herbivore-related decreased fecundity. We conducted a series of field experiments to determine the relative contribution of floral herbivores and pollinators to female reproductive success in an alpine herb, Pedicularis gruina, in two natural populations over two consecutive years. Experimental manipulations included bagging, hand supplemental, geitonogamous pollination, and simulated floral herbivory. Bumblebees not only avoided damaged flowers and plants but also decreased successive visits of flowers in damaged plants, and the latter may reduce the level of geitonogamy. Although seed set per fruit within damaged plants was higher than that in intact plants, total seed number in damaged plants was less than that in intact plants, since floral herbivory-mediated pollinator limitation led to a sharp reduction of fruit set. Overall, the results suggest that resource reallocation within inflorescences of damaged plants may partially compensate for a reduction in seed production. Additionally, a novel finding was the decrease in successive within-plant bumblebee visits following floral herbivory. This may increase seed quantity and quality of P. gruina since self-compatible species exhibit inbreeding depression. The patterns of compensation of herbivory and its consequences reported in this study give an insight into the combined effects of interactions between floral herbivory and pollination on plant reproductive fitness.
Fluctuating asymmetry (FA), a measure of random deviation of organismal traits from perfect bilateral symmetry, can be induced by environmental and/or genetic stress. We have conducted a replicated experiment to test the effect of a locally abundant heavy metal pollutant, lead, on the FA of a common wetland invasive species, Lythrum salicaria (purple loosestrife). The exposure to lead significantly reduced the shoot length, number and length of leaves as well as the biomass, but increased FA of L. salicaria leaves. The investigation suggests that FA in L. salicaria may be used as an ecological indicator to identify environmental stress caused by certain heavy metal pollutants. However, more studies are needed for the use of FA in L. salicaria as a comprehensive tool for biomonitoring of a wider array of environmental pollutants.
Truly flower-naïve bumblebees, with no prior rewarded experience for visits on any visual patterns outside the colony, were tested for their choice of bilaterally symmetric over asymmetric patterns in a radial-arm maze. No preference for symmetry was found. Prior training with rewarded black and white disks did, however, lead to a significant preference for symmetry. The preference was not specific to symmetry along the vertical axis: a preference for horizontal symmetry was found as well. The results challenge the notion that a preference for bilateral symmetry is unlearned. The preference for symmetry was the product of non-differential conditioning.
Mimulus luteus (Scrophulariaceae) is a perennial herb occurring in the South American Andes that shows a wide variation in the size and shape of a red spot on the lower lobe of the yellow flower. We describe the preference of four insects (three bees and one butterfly) and one hummingbird species for floral characters, and estimated the strength, direction, and form of pollinator-mediated selection through female fitness. We applied geometric morphometrics to describe the preference of pollinator species for different guide shapes. Our results revealed striking differences in the floral phenotypes preferred by insects and hummingbirds. Insects visited flowers with corollas 1.25-fold larger and guides 1.72-fold larger than the hummingbird species did. While insects preferred flowers with nectar guides pointing toward the corolla tube, the hummingbird preferred flowers with heart-shaped nectar guides. Most of the floral preferences shown by pollinators translated into significant linear and nonlinear selection coefficients. When selection was analyzed on a per-flower basis and for female fitness, corolla size was under positive directional selection, and nectar guide size and shape were under disruptive selection. Because the insect and hummingbird pollinators showed a strong segregation in their daily activity time, we suggest that current disruptive selection on the nectar guide phenotype can result from the differ-ential availability of the rewarding floral variants over a day. Our findings suggest that pollinator-mediated selection favoring extreme phenotypes in M. luteus may not only con-tribute to high nectar guide variation found in this species, but also can promote divergence of corolla and nectar guide traits.
The bees' spontaneous preferences toward various black-and-white patterns were studied using a multiple-choice test procedure. The patterns are presented on vertical planes, and the bees' choices at a fixed distance from the patterns are recorded. To exclude a possible influence of the bees' previous experience with natural flowers, the bees are trained to randomized checkerboard patterns prior to testing them with sets of other patterns. We find that, when the test patterns are of the same kind, but differ in their spatial frequencies, the bees prefer low over high frequencies. However, when the patterns differ in type, the bees express, regardless of spatial frequency, a positive preference for patterns containing radiating elements, and a negative preference for patterns containing circular elements or elements arranged at random. We find, in addition, that symmetrical patterns are more attractive than less symmetrical or non-symmetrical patterns. We propose that bees respond innately to some features of natural flowers, resulting in a spontaneous preference for radiating, as well as symmetrical patterns.
The level of fluctuating asymmetry in a secondary sexual character is
believed to reveal aspects of male quality. Previous investigations have
demonstrated that females may pay attention to this information when
making mate choice decisions; females prefer symmetric over asymmetric
males. However, these studies have involved either manipulation of
functionally important flight feathers, or of artificial ornaments.
Here, we manipulate an existing secondary sexual plumage trait, one that
does not influence flight performance, within the boundaries of natural
asymmetry. Through manipulations of chest plumage, we demonstrate that
female zebra finches choose to display more and for longer in front of
males with symmetric, as opposed to asymmetric, chest plumage.
Symmetrical visual patterns have a salient status in human perception, as evinced by their prevalent occurrence in art, and also in animal perception, where they may be an indicator of phenotypic and genotypic quality. Symmetry perception has been demonstrated in humans, birds, dolphins and apes. Here we show that bees trained to discriminate bilaterally symmetrical from non-symmetrical patterns learn the task and transfer it appropriately to novel stimuli, thus demonstrating a capacity to detect and generalize symmetry or asymmetry. We conclude that bees, and possibly flower-visiting insects in general, can acquire a generalized preference towards symmetrical or, alternatively, asymmetrical patterns depending on experience, and that symmetry detection is preformed or can be learned as perceptual category by insects, because it can be extracted as an independent visual pattern feature. Bees show a predisposition for learning and generalized symmetry because, if trained to it, they choose it more frequently, come closer to and hover longer in front of the novel symmetrical stimuli than the bees trained for asymmetry do for the novel asymmetrical stimuli. Thus, even organisms with comparatively small nervous systems can generalize about symmetry, and favour symmetrical over asymmetrical patterns.
The accord between symmetries of flower shape (external contours) and nectar guides (internal contours) was examined using the bulbous flora of South Africa, and in the general floras of Britain, Alpine Colorado, Canadian Arctic and Israel. It was found that radially symmetrical flowers have radially symmetrical nectar guides whereas bilaterally symmetrical flowers have bilaterally symmetrical nectar guides. It is suggested that the complementarity between the external and the internal contours of the flower increases the probability that, and efficiency with which, a bee moves into the flower's centre and towards the sporophylls and access to floral rewards, regardless of the flower's form and the bee's previous experience. Patterns of coloration of tepals against background and nectar guides against tepals also accord with behavioural and sensory characteristics of pollinators. It is suggested that the complementarity of contours is probably constrained by floral development, but patterns of coloration of tepals against background and nectar guides against tepals is constrained by pollinators' sensory physiology.
Floral characters are often subject to strong directional selection from pollinators, and this may disrupt developmental homeostasis in flowers that therefore develop large degrees of fluctuating asymmetry. Fluctuating asymmetry in floral traits may lead to sexual selection in plants if pollinators assortatively visit symmetrical flowers. We studied the relationship between pollination and floral asymmetry in ten different flowering plant species in Spain, Denmark, and Sweden. Pollinators preferentially visited symmetrical flowers independently of whether the plant species produced nectar. Symmetrical flowers of some species had higher pollinator rewards in terms of nectar content than asymmetrical flowers. Handling time of flowers was unaffected by asymmetry since insect visits to symmetrical flowers lasted as long as visits to asymmetrical flowers. Insect preferences for symmetrical flowers should have resulted in sexual selection with respect to symmetry. The evolution of pollinator preferences for symmetrical flowers and the potential fitness benefits to plants with symmetrical flowers due to this preference are discussed.
Bumblebees of any one species in Maine forage for pollen and/or nectar from a large variety of morphologically diverse flowers, but individuals have limited foraging repertoires at any one time. Unspecialized individuals were sometimes unsuccessful in extracting nectar and/or pollen from highly rewarding flowers. In any one area with a variety of concurrently blooming plants, the bumblebees had apparent species preferences. Superimposed on the species preferences were individual preferences. Individuals had primary foraging specialties (their majors) and secondary specialities (their minors). Minors were often bridges to new majors. Queens in Maine necessarily have several successive majors during their lifetime since the blooming time of the plants they utilize are brief relative to their life-span as foragers. However, the blooming time of most plants available to Bombus fervidus workers are long relative to their lifetime. Switching was rarely observed in these bees, even in some individuals observed daily for up to 1 mo at the same foraging area containing other plant species in bloom that were highly attractive to other individuals of the same bumblebee species. On a per flower basis, those flowers producing the most food rewards generally had the largest number of bees majoring from them, and the food rewards available were roughly comparable between different kinds of flowers, regardless of their differences in rates of nectar production. Specializing was usually preceded by sampling a variety of rewarding as well as nonrewarding flowers. When the flowers from which bees were majoring in an area were experimentally removed many of the bees sampled flowers of other concurrently blooming plants, but they generally did not switch to flowers from which the food rewards were being depleted by specialists, unless these were experimentally fortified with syrup. Upon finding superior food rewards in enriched blossoms, they switched immediately. Flower-specificity is related to site-specificity. Many bees shared the same foraging area, but different individual bees at the same site utilized the flowers of different plant species. When the foraging area contained landmarks, the bees visited clumps of flowers in a sequence (foraging path) that was generally repeated several times on the same foraging trip when the foraging site was small. The foraging behavior of bumblebees is discussed from a comparative standpoint with other bees and in relation to food distribution and availability in the environment.
I. Honeybees were trained to collect syrup from coloured discs and then presented with a choice of 'model' flowers. 2. The colour of a model was an important distinguishing feature, but its scent was even more important. A foreign odour made the models less attractive than no odour. 3. The size of a training model did not influence the size of model later chosen, but the bees preferred radially symmetrical to bilaterally symmetrical models, and models with a disruptive outline to circular models, even though trained to circular ones. 4. Adding nectar guides to a model increased its attractiveness, independently of conditioning ; dotted lines were more attractive than continuous lines, and a group of dots was more attractive than a black circle in the centre of a model. Adding a disruptive outline to a model similarly increased attractiveness and effects of a disruptive outline and nectar guide lines were additive. However, a limit was soon reached in which more guide lines or further segmentation failed to increase attractiveness. 5. Bees showed no preference to alight in the centres of circular models, and preferred the edges of the petaloid or star-shaped models. 6. Nectar guide lines had a directing function only when the bees had learned to seek food at a particular site in relation to them. Training to a point where nectar guide lines converged was quickly achieved, and could be transferred to models of other types. A nectar guide ring in the centre of a model sometimes slightly increased the proportion of visits to its centre, but conditioning was again necessary to obtain much effect. 7. Bees without previous training were attracted to a black central area, and this was still more effective after training. The bees' behaviour was not affected by attempts to give models an illusion of depth.
1) The effect which the honey-guides of flowers have upon visiting bees is investigated with the use of large model flowers. 2) It is found that bumble-bees have a strong tendency to react to the edge of plain shapes, where there is a line of colour contrast with the background. If a contrasting honey-guide pattern is added, the bees still fly initially to the edge, but subsequently react often to the contrast margins formed by the pattern. On real flowers the honey-guide is arranged around the entrance to the nectaries and thus could direct the bees' reactions there. 3) The total patterns formed by honey-guides have no significance for bumble-bees. They follow converging lines to the flower's centre only because they always arrive first at the outer edge. 4) Bumble-bees do not distinguish between plain and honey-guided models when choosing from a distance, but having flown to a model, they hover longer over the latter. 5) Various observations on bees visiting real flowers are described and the validity of arguing from models to real flowers is discussed. It is believed that honey-guides will have qualitatively the same effect on both. 6) Some aspects of the effects of the honey-guides and the scent of flowers are discussed.
In orchids a number of variants of specific parameters of the floral image appear to have arisen from a common ancestral type and to have become established as genetically constant ones in the determination of sub-generic taxa. At the present time little is known of the genetic basis for their origin or establishment. Though it is not known at present whether perception and storage of a complex floral pattern play a role in the determination of flower constancy in pollinators (and thus in the genetic isolation of variants), we hypothesize that they do. As a step toward gaining the ability to test this hypothesis, we present a method for the comparative quantification of specific characteristics of floral images, which must bear some relation to the level of sophistication necessary in a processor if visual recognition is to be effected. A number of parameters in the images of orchid flowers have been so analyzed. The relation of these results to the possibility that the evolution of these images has been effected by visually mediated natural selection is discussed.
Pollinating insects, bees, bumble-bees, butterflies, and moths have been found able to distinguish numbers, if these are expressed in symmetrical figures as pictured in fig. 3. This ability seems to be dependent upon the stage of psychic development of insects and varies considerably among different groups. Different groups of numbers are clearly expressed in the flower types (fig. 4) and may serve as pointers for pollinating insects to find their plants. The comparative study of trimerous, tetramerous, and pentamerous flower types provides a new approach to the evolution of flowering plants.
The time required for naive bumble bees to learn flower handling skills was compared among nine plant species with flowers of varying morphological complexity. Learning was measured as the time to reach a criterion of 80% correct flower visits, and as the rate at which naive bees improved their flower handling efficiency relative to experienced bees. On shallow, cup-shaped flowers with exposed nectar and on most long-tubed flowers with an open entrance, all naive bees located the nectary on their first attempt. On these relatively simple flowers, naive bees reached the learning criterion after a few minutes and took 3-10 min to approach the handling efficiency of experienced bees. On more complex flowers, with nectar concealed in a closed tube or in an unusual location, 55-71% of bees failed to find the nectar on their first visits. Bees that did find concealed nectar took 5-30 min to reach the learning criterion and 20-60 min to approach the handling efficiency of experienced bees. In general, morphologically complex flower designs took bees longer to learn than open-tubed or cup-shaped designs. However, specific predictions about the relative difficulty of learning to handle flowers could not be made from general flower morphology. Variation among bees in reaching the learning criterion was associated with individual age and size, although much of the variation was unexplained. Previous experience with simple flowers of one plant species decreased subsequent learning on other species with simple flowers but not on species with complex flowers.
The basic characteristics of orchids, possessing the greatest number of complex floral images of any Angiosperm family, are reviewed. Bilateral symmetry (zygomorphy) is shown by use of information theory techniques to give much greater possibilities for the transmission of visually mediated information than radial symmetry. The difference in information content is further enhanced by motion. The analysis is offered as evidence that the evolution of diversity in complex images, if effected by the unique behavioral specificity of pollinators known as “flower constancy”, is most economically explained by hypothesizing recognition and storage of the total image (“gestalt”) in the agents of natural selection.
Videotape records of flower-visiting behaviour of bumble bees (Bombus spp.) without previous foraging experience were compared with records of experienced foragers on flowers of six plant species representing a range of morphological complexity. Although the behaviour of experienced bees was relatively consistent, those without previous experience made many types of "errors" on their first flower visits. These included landing on inappropriate areas of flowers, assuming incorrect positions, and probing into areas of flowers other than in the vicinity of the nectary. The proportion of inexperienced foragers achieving a success criterion, defined as three sequential "errorless" visits, differed significantly among plant species. The time spent in trial and error learning before the criterion was obtained was significantly greater for flowers of high structural complexity than for those of intermediate and low complexity.The initial probing response of inexperienced bumble bees is mainly instinctive behaviour. However, exploitation of flowers also involves a learning component during which initial responses are modified according to the location of rewards in flowers of different plant species.f
The present article reviews recent and older literature on the
spatial parameters that flowers
display, as well as on the capacities of anthophilous insects to
perceive and use these
parameters for optimizing their foraging success. Although co-evolution
of plants and
pollinators has frequently been discussed with respect to floral
colours and insect colour
vision, it has rarely been assessed with respect to insect spatial
vision and spatial floral cues,
such as shape, pattern, size, contrast, symmetry, spatial frequency,
contour density and
orientation of contours. This review is an attempt to fill
this gap. From experimental findings
and observations on both flowers and insects, we arrive at the
conclusion that all of the spatial
and spatio-temporal parameters that flowers offer are relevant
to the foraging task and are
tuned to the insect's visual capacities and visually guided
behaviour. We try, in addition, to
indicate that temporal cues are closely related to spatial cues, and
must therefore be included
when flower–pollinator interactions are examined. We include
results that show that colour
vision and spatial vision have diverged over the course of evolution,
particularly regarding the
processing of spatio-temporal information, but that colour vision
plays a role in the processing
of spatial cues that are independent of temporal parameters. By
presenting this review we hope
to contribute to closer collaboration among scientists working in the
vast fields of botany, ecology, evolution, ethology and sensory physiology.
1.
We established apparently normal foraging behavior in captive bumblebees utilizing artificial flowers. Syrup rewards of flowers visited were experimentally manipulated to correspond to nectar volumes found in flowers utilized in the field.
2.
Bees became >90% flower-constant to either of two flower types (distinguished by color) when rewarded with 1.0 l 50% sucrose at each visit to flowers of one color, while the others remained unrewarded.
3.
Flower-constancy to blue was achieved within 50 flower visits, but equal flower constancy to white was achieved only after 250 flower visits.
4.
While being trained to white flowers the bees increased their percent correct (rewarding) flower choice over consecutive foraging trips during the day, but decreased their performance overnight.
5.
Bees trained to blue did not switch to white flowers even when the white were subsequently rewarded with more food than the blue. However, bees trained to white utilized blue flowers.
6.
Most bees simultaneously presented with white flowers having six times greater syrup rewards than blue visited both in approximately equal proportions independent of flower density, while some individuals visited primarily blue flowers.
7.
The laboratory experiments suggest that bumblebees, once conditioned, are relatively constant foragers despite changes in resource availability.
The outermost tail feathers of barn swallows Hirundo rustica apparently reliably signal the quality of males, because individuals with the longest tails have the lowest degree of fluctuating asymmetry (random deviations from symmetry in the otherwise symmetrical tail trait) despite the size of their secondary sexual character. I experimentally tested whether females preferred males with symmetrical tails without altering the aerodynamic properties of birds by painting the tips of the outermost tail feathers with white or black correction fluid. Unmated males were randomly assigned to one of four treatments: (i) asymmetrical tails, where the outermost 20 mm of one tail feather was painted white and the other black; (ii) symmetrical tails where the outermost 10 mm of both tail feathers was painted white (symmetric I); (iii) symmetrical tails where the outermost 20 mm of both tail feathers was painted white (symmetric II); or (iv) controls where the outermost 20 mm of both tail feathers was painted black. The experimental treatment affected the duration of the premating period since it took longer for asymmetrical males to acquire a mate than for either group of symmetrical males or control males. This gave rise to a delayed start of laying among males with apparently asymmetrical tails. The seasonal production of fledglings therefore decreased from control males through males with either symmetrical treatment to males with the asymmetrical treatment. Females therefore pay direct attention to the level of fluctuating asymmetry in secondary sexual characters even when the asymmetry does not affect the aerodynamic properties of males.
Fluctuating asymmetry is defined as small, random deviations from perfect bilateral symmetry in a morphological trait. Although fluctuating asymmetry has been of interest to population and conservation biologists for decades because it is often negatively correlated with heterozygosity, growth, fecundity and survival, fluctuating asymmetry's role in sexual selection has only recently been investigated. In fights for nuptial food items between adult males of the Japanese scorpionfly, Panorpa japonica, under field conditions, fluctuating asymmetry of forewing length is significantly less in winners than in losers. Also, mating males in nature have relatively low fluctuating asymmetry compared with non-mating males. Males that lose competition for nuptial gifts become satellites of males with gifts, and the losers attempt forced copulation but have very low mating success relative to gift-holding males because females prefer to mate with gift-holders and actively avoid satellites. Under semi-natural cage conditions, fluctuating asymmetry and both male mating success and survival are significantly negatively correlated; the same correlation was found in caged females for survival but not for mating success. The fluctuating asymmetry and male body size relationship differs markedly between two populations. In one population, males show the relationship that is often found in studies of fluctuating asymmetry, that is, the largest and smallest individuals have maximum fluctuating asymmetry, and individuals of intermediate size have the least fluctuating asymmetry. In the second population, males of all body sizes show similar variation in fluctuating asymmetry. Inbreeding, parasites and/or physical conditions may play a causal role in variation in fluctuating asymmetry within and between populations of P. japonica.
Male Chironomus plumosus most successful at acquiring mates showed lower levels of fluctuating asymmetry in length of wing than their rivals. These males were not of the most common size, but were the smallest in the population. These results are consistent with the prediction that where there is directional selection for small individuals, fluctuating asymmetry will be positively correlated with size. However, for a species that mates on the wing, selection may act upon symmetry per se rather than body size. Uncoupling the effects of size from those of asymmetry suggested that fluctuating asymmetry might, on its own, account for the observed mating success of C. plumosus. It is suggested that the success of the more symmetrical males is due to their improved aerobatic ability. Chironomus plumosus provides an example of the importance of fluctuating asymmetry in male characters that are not purely ornamental and these results are therefore more readily interpreted in terms of natural rather than sexual selection.
Evolutionary biologists continue to disagree about the relative importance of natural selection, drift and phylogenetic constraint in determining characteristics of an organism1. Because of the difficulty of identifying examples of selection in nature there are few rigorous field studies of selection2-6. We have been studying selection on flower colour in the small perennial larkspur Delphinium nelsonii, a native to mountains of the western USA. Previously we showed that white-flowered forms, which are very rare in natural populations, produce fewer seeds than their common blue-flowered conspecifics, and that this selective disadvantage results from partial discrimination against white flowers by bumblebee and hummingbird pollinators7. Here we present evidence that discrimination occurs because white flowers have inferior `nectar guides' and therefore require longer handling times than blue flowers. Pollinators may thus experience lower net rates of energy intake on white flowers, a sufficient reason for undervisitation by optimally-foraging animals.
Many secondary sexual characters are supposed to have evolved as a response to female choice of the most extravagantly ornamented males, a hypothesis supported by studies demonstrating female preferences for the most ornamented males. Comparative studies of elaborate feather ornaments in birds have shown that (1) ornaments have larger degrees of fluctuating asymmetry (small, random deviations from bilateral symmetry caused by an inability of individuals to cope with environmental and genetic stress during development of a character) than other morphological traits, and (2) the degree of fluctuating asymmetry is often negatively related to the size of the ornament. The negative relationship between ornament asymmetry and size suggests that ornament size reliably reflects male quality because the largest secondary sex traits demonstrate the least degree of fluctuating asymmetry. I manipulated tail length and tail asymmetry independently in male swallows (Hirundo rustica) to determine whether ornament size or asymmetry were used as cues in mate choice. Male swallows with elongated, symmetric tails mated earlier, and enjoyed larger annual reproductive success than did males with shortened tails and increased asymmetry. Females therefore prefer large as well as symmetric ornaments, which suggests that females in their mate choice use ornament asymmetry and size as reliable indicators of male quality.
Fluctuating asymmetry, which represents small random deviations from otherwise bilateral symmetry, is a measure of the phenotypic quality of individuals indicating the ability of controlled development under given environmental and genetic conditions. I tested whether floral symmetry reliably reflects phenotypic quality measured in terms of pollinator rewards and whether pollinators respond to floral symmetry in a series of observations and experiments on Epilobium angustifolium (Onagraceae). Lower petal asymmetry was negatively related to mean lower petal length, whereas asymmetry in leaf width was positively related to mean leaf width. Flowers visited by bumblebees were larger and more symmetrical than the nearest neighboring flower. This relationship between pollinator preference for large and symmetrical flowers was demonstrated to be causal in experiments in which the lower petals were manipulated symmetrically or asymmetrically. Nectar production was larger in symmetrical flowers, and this may explain the bumblebee preference for flower symmetry. Floral symmetry therefore reliably reflects nectar production and hence enhances pollen transport. Extensive embryo abortion has been documented in E. angustifolium and other outcrossing plant species. Floral fluctuating asymmetry, which reflects general developmental homeostasis, may explain such developmental selection in these plants.
- Davenport D.
- Dafni A.