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.     

Identification of learning mechanisms in a wild meerkat population

Vigorous debates as to the evolutionary origins of culture remain unresolved due to an absence of methods for identifying learning mechanisms in natural populations. While laboratory experiments on captive animals have revealed evidence for a number of mechanisms, these may not necessarily reflect the processes typically operating in nature. We developed a novel method that allows social and asocial learning mechanisms to be determined in animal groups from the patterns of interaction with, and solving of, a task. We deployed it to analyse learning in groups of wild meerkats (Suricata suricatta) presented with a novel foraging apparatus. We identify nine separate learning processes underlying the meerkats' foraging behaviour, in each case precisely quantifying their strength and duration, including local enhancement, emulation, and a hitherto unrecognized form of social learning, which we term 'observational perseverance'. Our analysis suggests a key factor underlying the stability of behavioural traditions is a high ratio of specific to generalized social learning effects. The approach has widespread potential as an ecologically valid tool to investigate learning mechanisms in natural groups of animals, including humans.     

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.     

Foraging errors play a role in resource exploration by bumble bees (Bombus terrrestris)

If the cognitive performance of animals reflects their particular ecological requirements, how can we explain appreciable variation in learning ability amongst closely related individuals (e.g. foraging workers within a bumble bee colony)? One possibility is that apparent ‘errors’ in a learning task actually represent an alternative foraging strategy. In this study we investigate the potential relationship between foraging ‘errors’ and foraging success among bumble bee (Bombus terrestris) workers. Individual foragers were trained to choose yellow, rewarded flowers and ignore blue, unrewarded flowers. We recorded the number of errors (visits to unrewarded flowers) each bee made during training, then tested them to determine how quickly they discovered a more profitable food source (either familiar blue flowers, or novel green flowers). We found that error prone bees discovered the novel food source significantly faster than accurate bees. Furthermore, we demonstrate that the time taken to discover the novel, more profitable, food source is positively correlated with foraging success. These results suggest that foraging errors are part of an ‘exploration’ foraging strategy, which could be advantageous in changeable foraging environments. This could explain the observed variation in learning performance amongst foragers within social insect colonies.     

Odour and colour information in the foraging choice behaviour of the honeybee

1. Honeybees Apis mellifera ligustica were trained to work on a patch with artificial rewarding and non-rewarding flowers, coupled to an air extractor. The perceptual colour distance between the rewarding and the non-rewarding flowers was varied and the flower choice and the repellent scent-marking behaviour of the bees were recorded. 2. The discrimination between rewarding and non-rewarding flowers depended on their colour distance, improving with a greater colour difference. This task was guided thus visually and was not affected by activating the air extractor. 3. The scent-marking activity was only observable when the colour information of both groups of flowers was the same or very similar. This thus represents the first reported case of a modulation of an olfactory activity through the visual input provided by colour distances. When the air extractor was activated, rejections associated with the scent-marking behaviour disappeared, thus confirming the olfactory nature of this behaviour. 4. Honeybees are thus capable of using one or more sensory cues to enhance their foraging efficiency, according to the environmental situation. This great plasticity allows them to attain an enhanced efficiency while foraging. 5. We successfully applied the model of colour choice behaviour of the honeybee. Since the original theory was developed for Apis mellifera carnica, this work also constitutes the first attempt to describe the behaviour of the honeybee race, Apis mellifera ligustica, using the postulated model, and reaffirms thus its generality.     

Floral choices by honeybees in relation to the relative distances to flowers

ABSTRACT. Honeybees ( Apis mellifera L.) were presented with a series of binary choices between two equally rewarding yellow or blue artificial flowers. When flowers were placed equidistant from each other, the bees maintained high degrees of constancy to one flower colour. When flowers were spaced unequally, the bees most often chose to visit the closest flower, as is predicted by an optimal foraging model.     

Honeybee (Apis mellifera ligustica) Response to Differences in Handling Time, Rewards and Flower Colours

Free flying honeybees were tested outdoors on blue–white and blue–yellow dimorphic artificial flower patches to examine the influence of reward difference, flower handling‐time difference and flower colour choice on foraging decisions. We employed different flower‐well depths to vary handling times (costs), and differences in sucrose molarity to vary reward quality. Tests were performed with 2 and 6 μl rewards to vary quantity. We show that when handling time is correlated with flower‐colour morphs on a pedicellate artificial flower patch, a honeybee's foraging behaviour is dependent on the flower colours used in the choice tests. This supports a honeybee foraging model where constraints are a significant factor in decision making. Bees visiting blue–yellow flower patches exhibited flower constancy to colour, where they restricted most visits to a single flower colour, some bees to blue and others to yellow, irrespective of handing time differences. When offered a choice of equally rewarding blue or white flowers, bees were not constrained by flower colour and chose to visit flowers with a lower handling time. When reward molarity varied with well depth between blue and white flowers, foragers chose shallow‐well flowers (short‐handling time) with a smaller net harvest rate over deep‐well flowers (long‐handling time) with a greater net harvest rate. Results using the blue–white dimorphic flower patch suggest that when foraging options simultaneously involve reward and handling‐time choices, honeybee forager behaviour is inconsistent with an absolute method of evaluating profit.     

Predator crypsis enhances behaviourally mediated indirect effects on plants by altering bumblebee foraging preferences

Predators of pollinators can influence pollination services and plant fitness via both consumptive (reducing pollinator density) and non-consumptive (altering pollinator behaviour) effects. However, a better knowledge of the mechanisms underlying behaviourally mediated indirect effects of predators is necessary to properly understand their role in community dynamics. We used the tripartite relationship between bumblebees, predatory crab spiders and flowers to ask whether behaviourally mediated effects are localized to flowers harbouring predators, or whether bees extend their avoidance to entire plant species. In a tightly controlled laboratory environment, bumblebees (Bombus terrestris) were exposed to a random mixture of equally rewarding yellow and white artificial flowers, but foraging on yellow flowers was very risky: bees had a 25 per cent chance of receiving a simulated predation attempt by ‘robotic’ crab spiders. As bees learnt to avoid ‘dangerous’ flowers, their foraging preferences changed and they began to visit fewer yellow flowers than expected by chance. Bees avoided spider-free yellow flowers as well as dangerous yellow flowers when spiders were more difficult to detect (the colour of yellow spiders was indistinguishable from that of yellow flowers). Therefore, this interaction between bee learning and predator crypsis could lead flower species harbouring cryptic predators to suffer from reduced reproductive success.     

草乌花蜜产量的梯度分布及熊蜂自下而上的访花行为

收益降低假说(declining reward hypothesis)认为熊蜂自下而上的访花顺序是对花蜜产量的直接响应,先访问下部花蜜产量高的花可以获得更多的收益;花开口方向假说认为自下而上访花是因为熊蜂更容易看见其上部的花朵。为了验证上述两个假说,我们于2008年8月在北京小龙门国家森林公园调查了红光熊蜂(Bombus ignitus)访问草乌(Aconitum kusnezoffii)直立和倒立顶生花序的访问顺序,测量了直立花序下部雌性阶段花和上部雄性阶段花花蜜的糖浓度、体积,计算了花蜜中的糖含量。结果表明,红光熊蜂在直立花序和倒立花序内均以向上运动为主,分别占总运动次数的62.77%和68.35%;直立花序下部雌性阶段花花蜜糖浓度比上部雄性阶段花低1.44%,但是花蜜体积和花蜜中的糖含量都显著高于雄性阶段的花。由于熊蜂访问倒立花序时先访问的是下部的低回报雄性阶段的花,然后再访问上部高回报的雌性阶段的花,这与收益降低假说矛盾,表明红光熊蜂自下而上访问草乌直立花序可能不是受到花蜜产量的调节。     

Geitonogamy in rewarding and unrewarding inflorescences: modelling pollen transfer on actual foraging sequences

Many orchid species are unusual in that they provide no nectar or pollen rewards for their pollinators. Absence of reward is expected to have a fundamental effect on pollinator visitation patterns. In particular the number of flowers visited per inflorescence is expected to be affected in both unrewarding and co-flowering rewarding species. We used arrays of artificial inflorescences, which could be either rewarding or unrewarding and were differentiated by their colour, to test how many flowers bumblebees visit in each type of inflorescence. The frequency of the two colours was varied, thus modelling the case where different frequencies of both an unrewarding and rewarding species were present in a patch. We found that bumblebees visited more flowers per rewarding inflorescence after they have experienced unrewarding or partially emptied rewarding inflorescences. We used these results to simulate pollen transfer and thus predict selfing rates on rewarding inflorescences. We found these increased when nectar depleted or when there was a greater proportion of unrewarding inflorescences in the patch. Conversely, we found that the number of flowers bumblebees visited on each unrewarding inflorescence did not significantly change through experiments. Selfing rates for unrewarding inflorescences were predicted to depend principally on the number of these inflorescences bumblebees visited rather than on the number of flowers they visit per inflorescence. This was because most visitors to orchids are supposed to be naive, and pollinators that commence foraging carrying no pollen will necessarily self any flower they pollinate on the first inflorescence they visit. Thus the average selfing rate is expected to increase as the sequence of inflorescences visited decreases in length.     

A Field Study of Spatial Memory in Green-Backed Firecrown Hummingbirds (Sephanoides sephaniodes)

The foraging ecology of hummingbirds involves the exploitation of a high number of patchily distributed flowers. This scenario seems to have influenced capabilities related to learning and memory, which help to avoid recently visited flowers and to allocate exploitation to the most rewarding flowers, once learning has occurred. We carried out two field experiments with the green‐backed firecrown hummingbird (Sephanoides sephaniodes, Trochilidae) in order to examine the ability of birds, first, to recall a nectar location, and secondly, to remember the location of the most rewarding flower among lower quality flowers. The first experiment showed that subjects were able to recall the location of nectar among flowers of identical appearance. In the second experiment, hummingbirds were also able to recall the location of the most rewarding nectar among less rewarding flowers with the same appearance. The results of this study suggest that S. sephaniodes can remember the location of the most rewarding patch, facilitating efficient exploitation of flowers in the absence of visual cues related to nectar quality.     

Colour similarity to rewarding model plants affects pollination in a food deceptive orchid, Orchis boryi

We studied the pollination of Orchis boryi at five different locations on the Greek mainland. Orchis boryi is food deceptive and obligatorily insect pollinated. Primary pollinators were Apis mellifera and Bombus spp., which foraged on rewarding plant species nearby and visited O. boryi in between. To analyse floral colour similarity among rewarding plants and O. boryi as perceived by bees, a model of bee colour vision was employed. For each food plant an index was calculated that described the probability of a bee foraging on it to subsequently choose an orchid flower. This choice probability correlated to colour distance according to the model of bee colour vision, indicating that bees chose the deceptive orchid more frequently if they foraged on more similarly coloured species. At different sites different plant species served as models. Bees foraging on food plants from which a high choice rate to the orchid was observed visited the orchid less often after approaching it than other bees, which is likely to reflect avoidance learning. In general, the pollination syndrome appears to be a generalized form of Batesian mimicry, in which similarity to rewarding plants determines reproductive success. As expected by negative density-dependent selection, individual fruit set and pollinia export rate correlated negatively with orchid density, but were unaffected by food plant density, orchid frequency, individual variation of labellum colour, labellum size, or mouth width of the flowers.     

Traffic noise inhibits cognitive performance in a songbird

Noise pollution is commonly associated with human environments and mounting evidence indicates that noise has a variety of negative effects on wildlife. Noise has also been linked to cognitive impairment in humans and because many animals use cognitively intensive processes to overcome environmental challenges, noise pollution has the potential to interfere with cognitive function in animals living in urban areas or near roads. We experimentally examined how road traffic noise impacts avian cognitive performance by testing adult zebra finches (Taeniopygia guttata) on a battery of foraging tasks in the presence or absence of traffic noise playback. Here, we show that traffic noise reduces cognitive performance, including inhibitory control, motor learning, spatial memory and social learning, but not associative colour learning. This study demonstrates a novel mechanism through which anthropogenic noise can impact animals, namely through cognitive interference, and suggests that noise pollution may have previously unconsidered consequences for animals.     

Colour constancy in insects

Colour constancy is the perceptual phenomenon that the colour of an object appears largely unchanged, even if the spectral composition of the illuminating light changes. Colour constancy has been found in all insect species so far tested. Especially the pollinating insects offer a remarkable opportunity to study the ecological significance of colour constancy since they spend much of their adult lives identifying and choosing between colour targets (flowers) under continuously changing ambient lighting conditions. In bees, whose colour vision is best studied among the insects, the compensation provided by colour constancy is only partial and its efficiency depends on the area of colour space. There is no evidence for complete ‘discounting’ of the illuminant in bees, and the spectral composition of the light can itself be used as adaptive information. In patchy illumination, bees adjust their spatial foraging to minimise transitions between variously illuminated zones. Modelling allows the quantification of the adaptive benefits of various colour constancy mechanisms in the economy of nature. We also discuss the neural mechanisms and cognitive operations that might underpin colour constancy in insects.     

Contrasting responses of bumble bees to feeding conspecifics on their familiar and unfamiliar flowers

Animals exploiting their familiar food items often avoid spatio-temporal aggregation with others by avoiding scents, less rewarding areas or visual contacts, thereby minimizing competition or interference when resources are replenished slowly in patches. When animals are searching or assessing available food sources, however, they may benefit from reducing sampling costs by following others at food sites. Therefore, animals may adjust their responses to others depending on their familiarity with foraging situations. Here, we conducted field experiments to test whether nectar-collecting bumble bees make this adjustment. We allowed free-foraging bees to choose between two inflorescences, one occupied by a conspecific bee and another unoccupied. When bees were presented with flowers of a familiar type, they avoided occupied inflorescences. In contrast, bees visited an occupied inflorescence when the flower type was unfamiliar. To our knowledge, this is the first report suggesting that animals adjust their responses to feeding conspecifics depending on their familiarity with food sources. Such behavioural flexibilities should allow foragers to both explore and exploit their environments efficiently.     

Structural colour and iridescence in plants: the poorly studied relations of pigment colour

Background

Colour is a consequence of the optical properties of an object and the visual system of the animal perceiving it. Colour is produced through chemical and structural means, but structural colour has been relatively poorly studied in plants.

Scope

This Botanical Briefing describes the mechanisms by which structures can produce colour. In plants, as in animals, the most common mechanisms are multilayers and diffraction gratings. The functions of structural colour are then discussed. In animals, these colours act primarily as signals between members of the same species, although they can also play roles in camouflaging animals from their predators. In plants, multilayers are found predominantly in shade-plant leaves, suggesting a role either in photoprotection or in optimizing capture of photosynthetically active light. Diffraction gratings may be a surprisingly common feature of petals, and recent work has shown that they can be used by bees as cues to identify rewarding flowers.

Conclusions

Structural colour may be surprisingly frequent in the plant kingdom, playing important roles alongside pigment colour. Much remains to be discovered about its distribution, development and function.     

Comparison of Diuraphis noxia resistance in wheat isolines and plant introduction lines

A bioassay to examine the foraging behaviour of the aphidophagous hoverfly, Episyrphus balteatus was used in which various stimuli purported to influence flower choice were tested using model flowers. In choice experiments, E. balteatus exhibited enhanced behavioural responses to the colour yellow, as previously seen in Eristalis by several workers. Previous suggestions that the generalist forager E. balteatus has no preference for colour are re-examined in the light of this new evidence. The other advertisement cue tested, size, was also demonstrated to play an important role in determining foraging behaviour, with the smaller artificial flowers seemingly preferred. Of the rewards tested, E. balteatus showed preference for the greatest nectar concentrations, whilst increasing pollen did not affect behaviour. These bioassays provided an opportunity to isolate the individual components of decision-making by E. balteatus during foraging. The separation of sexes and ages in these experiments permitted analysis of inter-sexual and inter-generation differences in behaviour, a factor apparently not investigated in previous work.     

Insect odour perception: recognition of odour components by flower foraging moths

Odours emitted by flowers are complex blends of volatile compounds. These odours are learnt by flower-visiting insect species, improving their recognition of rewarding flowers and thus foraging efficiency. We investigated the flexibility of floral odour learning by testing whether adult moths recognize single compounds common to flowers on which they forage. Dual choice preference tests on Helicoverpa armigera moths allowed free flying moths to forage on one of three flower species; Argyranthemum frutescens (federation daisy), Cajanus cajan (pigeonpea) or Nicotiana tabacum (tobacco). Results showed that, (i) a benzenoid (phenylacetaldehyde) and a monoterpene (linalool) were subsequently recognized after visits to flowers that emitted these volatile constituents, (ii) in a preference test, other monoterpenes in the flowers' odour did not affect the moths' ability to recognize the monoterpene linalool and (iii) relative preferences for two volatiles changed after foraging experience on a single flower species that emitted both volatiles. The importance of using free flying insects and real flowers to understand the mechanisms involved in floral odour learning in nature are discussed in the context of our findings.     

Pink flower preference in sunbirds does not translate into plant fitness differences in a polymorphic Erica species

Bird-pollinated plants typically have reddish flowers, but it is not clear whether this trait can be attributed to selection by birds. Here we experimentally test for the first time the foraging behaviour of sunbirds in relation to flower colour, using the Orange-breasted Sunbird Anthobaphes violacea (Nectariniidae) and the colour dimorphic Erica perspicua (Ericaceae). Pink and white flower morphotypes co-flower in intermixed populations and have similar nectar volumes and concentrations. Using floral arrays in a field aviary, we found that sunbirds preferred pink flowers; 95 % of their first choices were to pink inflorescences and they visited and probed more pink inflorescences and flowers, respectively. We also tested for flower constancy (the tendency to move between same colour rather than different colour morphotypes), but found no evidence for this in the sequence of their foraging choices, indicating that this mechanism did not maintain flower colour differences in sympatry. There was evidence for optimal foraging: 80 % of moves were to adjacent inflorescences. Unexpectedly, the preference for pink flowers observed in the aviary did not translate into a female fitness advantage for this morphotype in the field, since no difference is found in natural pollination rate, fruit or seed set. This may be because the minimization of flight distances between plants is the primary factor in sunbird foraging choices, overriding their colour preference. Antagonistic nectar robbers did not act as a selective force on the polymorphism, since nectar-robbing rates were equal between white and pink morphotypes in the field.     

Trade-off between travel distance and prioritization of high-reward sites in traplining bumblebees

1.Animals exploiting renewable resource patches are faced with complex multi-location routing problems. In many species, individuals visit foraging patches in predictable sequences called traplines. However, whether and how they optimize their routes remains poorly understood.2.In this study, we demonstrate that traplining bumblebees (Bombus terrestris) make a trade-off between minimizing travel distance and prioritizing the most rewarding feeding locations.3.Individual bees trained to forage on five artificial flowers of equal reward value selected the shortest possible route as a trapline. After introducing a single highly rewarding flower to the array, they re-adjusted their routes visiting the most rewarding flower first provided the departure distance from the shortest possible route remained small (18%). When routes optimizing the initial rate of reward intake were much longer (42%), bees prioritized short travel distances.4.Under natural conditions, in which individual flowers vary in nectar productivity and replenish continuously, it might pay bees to prioritize highly rewarding locations, both to minimize the overall number of flowers to visit and to beat competitors.5.We discuss how combined memories of location and quality of resource patches could allow bees and other traplining animals to optimize their routing decisions in heterogeneous environments.