The effect of age and visual cues on floral patch use by bananaquits (aves: Emberizidae)

The foraging abilities of naive, hand-reared juvenile bananaquits, Coereba flaveola, were compared to those of captive wild adults foraging in an artificial flower patch containing either open or closed flowers. Foragers removed the tops from covered flowers in order to feed, thereby marking all visited flowers. Open flowers provided no clues as to previous visitation. Adults searched the patch more thoroughly and made fewer flower revisits during each foraging bout than did juveniles. Flower revisitations by juveniles were more than expected by chance while those made by adults were fewer than expected by chance. This was true for both open and covered flower types. The increase in foraging efficiency with age involves several different characteristics. On open flowers, adults and juveniles differed in the frequency of their patch departures and returns, and in their pattern of turning in the patch, thus resulting in a more complete search of the patch by adults. On covered flowers, however, the two age classes differed primarily in their patterns of turning, and adults made a more complete search of the patch. Both age classes used the presence or absence of flower covers as a clue to previous visitation.     

An evolved spatial memory bias in a nectar-feeding bird?

Studies have shown that nectar-feeding birds more easily learn to avoid a previously rewarding location (to win-shift) than to return to such a location (to win-stay). This pattern has been interpreted as evidence of an evolved adaptation to the fact that nectar is a depleting resource; however, such a conclusion requires ruling out the possibility that this tendency is a consequence of the experience of individual birds, and is more compelling if performance in the memory task reveals sensitivity to detailed features of the spatiotemporal distribution of nectar in the environment. We tested the tendency of captive-reared Regent honeyeaters, Xanthomyza phrygia, a species of nectar-feeding bird, to win-shift or win-stay at different intervisit intervals. The birds generally avoided rewarding locations after a short retention interval (10 min), but returned to these locations after a long retention interval (3 h). This behaviour tracks the replenishment rate of the flowers exploited by this species in the wild, even though the subjects were born and reared in captivity. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Two intertidal fish species use visual association learning to track the status of food patches in a radial maze

We tested fifteen-spined sticklebacks, Spinachia spinachia, and corkwing wrasse, Crenilabrus melops, for their ability to associate visual spatial cues with food sources in a radial maze and so to track renewal frequencies and productivity. When all locations contained food or were empty, subjects displayed win-shift or lose-shift behaviour by avoiding recently visited locations; this behaviour therefore appeared to be a basic trait. Both species readily learned food-cue associations, although with less efficiency as the diversity of cues increased. They used this information to distinguish food sources renewed within and between daily foraging bouts from those that remained empty. Moreover, both species distinguished between renewable food sources differing in productivity, preferentially visiting those containing more food. Reversal of cue roles caused an immediate decline in foraging efficiency, followed by rapid recovery as new food-cue associations were learned. Evidently, therefore, subjects tracked the status of potential food sources by continued sampling and could switch from win-shift to win-stay behaviour, when preferred locations were persistently revisited, as appropriate. The formation of food-cue associations, together with sampling and flexible use of win-shift and win-stay behaviour, would enable these rocky intertidal fish species to exploit patchily distributed food sources whose status changes during the tidal cycle. Copyright 2000 The Association for the Study of Animal Behaviour.     

Observational Learning in the White-Eared Hummingbird (Hylocharis leucotis): Experimental Evidence

The adoption of new food resources can be facilitated by the ability to learn through observation of other individuals who use them. This behavior, termed observational learning, applies to any problem solving in which a naive individual who has observed an experienced individual learns a behavior faster than another who has not. Hummingbirds consume nectar from flowers of a large number of plant species, which are very diverse in morphology and color. During their local or migratory movements, they can observe the use of floral resources by conspecifics and heterospecifics which may change their foraging preferences. Although there is evidence that hummingbirds can use observational learning to exploit new floral resources, it is necessary to generate additional information by studying different hummingbird species. In this work, the learning performance of White‐eared hummingbirds (Hylocharis leucotis) was studied in the presence or absence of a knowledgeable tutor. In a first experiment, naïve hummingbirds learned to feed on arrays of artificial flower of two colors: red (previously known resource) and yellow (novel resource), where only one color had nectar. Naive hummingbirds visited red flowers faster and more often than rewarded yellow flowers. Individuals with the best performance on each color were further trained to ensure that they only visited flowers of a specific color, and were then used as tutors in the next experiment, in which new naive hummingbirds, caged individually, were allowed to observe them foraging on the artificial arrays. These naïve individual were then exposed alone to the same array used by their tutor. Tutored hummingbirds learned to feed faster and more frequently from nectar‐containing flowers of the array than naive individuals. Likewise, all tutored individuals only visited flowers of the color that had been previously visited by their tutors. This study provides experimental evidence that hummingbirds taken directly from the field can use observational learning as an efficient strategy to access new floral resources.     

Pigs shift too: foraging strategies and spatial memory in the domestic pig

In a previous experiment, we showed that domestic pigs, Sus scrofa, unlike many other species, performed accurately in a spatial memory task, where visits to a previously baited food trough were rewarded (win-stay). We investigated whether pigs have a predisposition for this strategy, by comparing their performance in a radial arm maze under either win-stay (N=10) or win-shift (N=10) reward contingencies. Contrary to our earlier results, only one of the animals in the win-stay condition was able to reach the imposed criterion level of accuracy. The performances of the other win-stay pigs did not deviate from random. All pigs in the win-shift condition reached criterion by day 25 of the experiment, and performed better than expected by chance. Analysis of the types of errors made matched our a priori predictions that shift movements would occur more frequently, especially within visits to the maze. We suggest that the difference in learning rates may reflect the fact that win-stay pigs needed to use two different rules, stay between trials and shift within trials, while win-shift pigs only needed to use the shift rule. In our previous study, win-stay pigs did not experience a conflict of rules and this may have facilitated stay learning. We found evidence of a recency effect in win-shift animals and a primacy effect in the win-stay group. However, we discuss the unsuitability of these specific terms in this type of experiment, and propose an alternative interpretation of the results. Copyright 2000 The Association for the Study of Animal Behaviour.     

Food-specific spatial memory biases in an omnivorous bird

The tendency of nectarivorous birds to perform better on tasks requiring them to avoid previously rewarding locations (to win-shift) than to return to them (win-stay) has been explained as an adaptation to the depleting nature of nectar. This interpretation relies on the previously untested assumption that the win-shift tendency is not associated with food types possessing a different distribution. To test this assumption, we examined the specificity of this bias to different food types in an omnivorous honeyeater, the noisy miner (Manorina melanocephala). As predicted, we found that the win-shift bias was sensitive to foraging context, manifesting only in association with foraging for nectar, not with foraging for invertebrates.     

Flower orientation enhances pollen transfer in bilaterally symmetrical flowers

Zygomorphic flowers are usually more complex than actinomorphic flowers and are more likely to be visited by specialized pollinators. Complex zygomorphic flowers tend to be oriented horizontally. It is hypothesized that a horizontal flower orientation ensures effective pollen transfer by facilitating pollinator recognition (the recognition-facilitation hypothesis) and/or pollinator landing (the landing-control hypothesis). To examine these two hypotheses, we altered the angle of Commelina communis flowers and examined the efficiency of pollen transfer, as well as the behavior of their visitors. We exposed unmanipulated (horizontal-), upward-, and downward-facing flowers to syrphid flies (mostly Episyrphus balteatus), which are natural visitors to C. communis. The frequency of pollinator approaches and landings, as well as the amount of pollen deposited by E. balteatus, decreased for the downward-facing flowers, supporting both hypotheses. The upward-facing flowers received the same numbers of approaches and landings as the unmanipulated flowers, but experienced more illegitimate landings. In addition, the visitors failed to touch the stigmas or anthers on the upward-facing flowers, leading to reduced pollen export and receipt, and supporting the landing-control hypothesis. Collectively, our data suggested that the horizontal orientation of zygomorphic flowers enhances pollen transfer by both facilitating pollinator recognition and controlling pollinator landing position. These findings suggest that zygomorphic flowers which deviate from a horizontal orientation may have lower fitness because of decreased pollen transfer.     

Possible Mechanisms for the Formation of Flower Size Preferences by Foraging Bumblebees

Large flowers often contain larger nectar rewards, and receive more pollinator visits, than small flowers. We studied possible behavioral mechanisms underlying the formation of flower size preferences in bumblebees, using a two-phase laboratory experiment. Experimentally naive Bombus terrestris (L.) foraged on artificial flowers that bore either a large (3.8 cm diameter) or a small (2.7 cm diameter) display of a uniform color. Only flowers of one display size contained nectar rewards. We changed the display color and the locations of large and small flowers in the second experimental phase. We recorded the bees' choices in both phases. Almost half of the bees (41%) made their first visit to a small flower. The bees learned to associate display size with food reward, and chose rewarding flowers with >85% accuracy by the end of each experimental phase. Some learning occurred within the bees' first three flower visits. Learning of the size–reward association was equally good for large and small displays in the first experimental phase, but better for small displays in the second phase. Formation of size–reward associations followed a similar course in both phases. This suggests that the bees did not apply their experience from the first learning phase to the new situation of the second phase. Rather, they treated each phase of the experiment as an independent learning task. Our results suggest that associative learning is involved in the formation of preferences for large displays by bees. Moreover, bees that had learned to prefer large displays in one foraging situation may not transfer this preference to a novel situation that is sufficiently different. We propose that this feature of the bees' behavior can select for honest advertising in flowers.     

The learning abilities of the white cabbage butterfly,Pieris rapae,foraging for flowers

This study examines the role of learning and memory in the butterflyPieris rapae crucivora Boisduval during foraging for flowers. In an outdoor cage with 6 flower species,P. rapae showed various visiting patterns: some visited only one species, while others visited several species in a day. The foraging process for flowers ofErigeron annuus (L.) Pers. could be divided into two successive steps: (1) landing on the nectaring caputs, and (2) finding the source of nectar in the caput. Butterflies learned to proceed through the two steps more efficiently with successive attempts: they gradually decreased landings on nectarless caputs and probings on the nectarless petals of ligulate flowers respectively. As a result, handling time per unit caputs became shorter, and apparent rewards per unit time, i.e. the efficiency of collecting nectar, increased. In addition, once learned,P. rapae could remember a rewarding flower color for 3 days, which was not interfered with by learning another flower color. This indicates thatP. rapae keeps memory for a period longer than 3 days, and that they can remember at least two flower species as suitable flower resources. Furthermore, data indicated that they sometimes can apply the foraging skills obtained on other flower species to a novel one. These abilities could enable butterflies to easily switch flower species, or to enhance labile preference. It has been known thatP. rapae also shows flower constancy, which may be due to memory constraints. Therefore, they may appropriately use two foraging tactics: visit consistency and labile preference, to get enough nectar according to their circumstances.     

The role of pollinators in maintaining variation in flower colour in the Rocky Mountain columbine,Aquilegia coerulea

Background and Aims Flower colour varies within and among populations of the Rocky Mountain columbine, Aquilegia coerulea, in conjunction with the abundance of its two major pollinators, hawkmoths and bumble-bees. This study seeks to understand whether the choice of flower colour by these major pollinators can help explain the variation in flower colour observed in A. coerulea populations.Methods Dual choice assays and experimental arrays of blue and white flowers were used to determine the preference of hawkmoths and bumble-bees for flower colour. A test was made to determine whether a differential preference for flower colour, with bumble-bees preferring blue and hawkmoths white flowers, could explain the variation in flower colour. Whether a single pollinator could maintain a flower colour polymorphism was examined by testing to see if preference for a flower colour varied between day and dusk for hawkmoths and whether bumble-bees preferred novel or rare flower colour morphs.Key Results Hawkmoths preferred blue flowers under both day and dusk light conditions. Naïve bumble-bees preferred blue flowers but quickly learned to forage randomly on the two colour morphs when similar rewards were presented in the flowers. Bees quickly learned to associate a flower colour with a pollen reward. Prior experience affected the choice of flower colour by bees, but they did not preferentially visit novel flower colours or rare or common colour morphs.Conclusions Differences in flower colour preference between the two major pollinators could not explain the variation in flower colour observed in A. coerulea. The preference of hawkmoths for flower colour did not change between day and dusk, and bumble-bees did not prefer a novel or a rare flower colour morph. The data therefore suggest that factors other than pollinators may be more likely to affect the flower colour variation observed in A. coerulea.     

Floral display size in comfrey, Symphytum officinale L. (Boraginaceae): relationships with visitation by three bumblebee species and subsequent seed set

The fecundity of insect-pollinated plants may not be linearly related to the number of flowers produced, since floral display will influence pollinator foraging patterns. We may expect more visits to plants with more flowers, but do these large plants receive more or fewer visits per flower than small plants? Do all pollinator species respond in the same way? We would also expect foragers to move less between plants when the number of flowers per plant are large, which may reduce cross-pollination compared to plants with few flowers. We examine the relationships between numbers of inflorescence per plant, bumblebee foraging behaviour and seed set in comfrey, Symphytum officinale, a self-incompatible perennial herb. Bumblebee species differed in their response to the size of floral display. More individuals of Bombus pratorum and the nectar-robbing B.?terrestris were attracted to plants with larger floral displays, but B. pascuorum exhibited no increase in recruitment according to display size. Once attracted, all bee species visited more inflorescences per plant on plants with more inflorescences. Overall the visitation rate per inflorescence and seed set per flower was independent of the number of inflorescences per plant. Variation in seed set was not explained by the numbers of bumblebees attracted or by the number of inflorescences they visited for any bee species. However, the mean seed set per flower (1.18) was far below the maximum possible (4 per flower). We suggest that in this system seed set is not limited by pollination but by other factors, possibly nutritional resources.     

Can flower constancy in nectaring butterflies be explained by Darwin’s interference hypothesis?

 When foraging for nectar many insects exhibit flower constancy (a preference for flower species which they have previously visited) and frequently ignore rewarding flowers of other species. Darwin proposed the favoured explanation for this behaviour, hypothesizing that learning of handling skills for one flower species interferes with the ability to recall handling skills for previously learned species. A crucial element of this hypothesis is that savings in handling time resulting from constancy must exceed increases in travelling time necessitated by ignoring other suitable species. A convincing quantification of this trade-off has not been achieved and tests to date on bumblebees indicate that savings in handling time are too small to offset an increase in travelling time. To assess further the validity of Darwin’s hypothesis, handling and flight times of the butterfly, Thymelicus flavus, were measured under natural conditions, and the abundance and reward provided by the available flower species quantified to enable estimation of foraging efficiency. Butterflies exhibited a mean increase in handling time of 0.85 s per flower associated with switching between flower species, although the magnitude of this difference varied greatly among flower species. Switching was not associated with a decrease in travelling time, contrary to expectation. Switching was more frequent following a lower than average reward from the last flower visited. In butterflies, flights serve functions other than movement between nectar sources, such as mate location (unlike worker bees). Hence constancy may be a viable strategy to reduce time spent in handling flowers and increase time available for other activities. Although savings in handling time may be small, Darwin’s interference hypothesis remains a valid explanation for flower constancy in foraging butterflies. Received: 27 January 1997 / Accepted: 5 June 1997     

Optimal resource allocation model for excessive flower production in a pollinating seed-predator mutualism

Many plants produce excessive flowers and several hypotheses have been proposed for adaptive significances of this behavior. Here, I develop a simple resource allocation model for plants in a mutualism with pollinating seed-predators to examine a novel hypothesis that excessive flower production can be favored to “dilute” seed predation by the pollinators. Pollinators visit flowers to deposit pollen and oviposit on them, and their offspring feed on a portion of the seeds, leaving the remainder intact. Further pollinator visits increase seed mortality by over-oviposition. Excessive flower production is favored if it decreases pollinator-visit frequency per flower, while it incurs decrease in seed production because of the resource trade-off. I examine three plant strategies: (1) no abortion, the plant allocates resource to all pollinated flowers to mature; (2) selective abortion, the plant aborts flowers depending on how many times they were visited by pollinators; and (3) random abortion, the plant indiscriminately aborts a fraction of pollinated flowers irrespective of how many times they were visited. I show that the random abortion strategy can perform much more effectively than the no-abortion strategy when the amount of resource is small, the production cost per flower is low, and the pollinator density is high, although the selective abortion strategy is always the best. This “predator dilution” effect has not been considered with regard to previous excessive flower production hypotheses.     

The Role of Flower Width in Hummingbird Bill Length‐Flower Length Relationships1

Observations of hummingbirds feeding at flowers longer or shorter than their bills seem to contradict the view that bill lengths of hummingbirds evolved in concert with the lengths of their flowers. Recent experiments, however, indicate that a hummingbird's ability to feed at artificial flowers of different lengths depends on the widths of the flowers. We examined if the broad range of flower lengths visited by many hummingbird species can be explained by the widths of the flowers. We predicted that both short‐ and long‐billed hummingbirds would include long, wide flower species in their diets, but that short‐billed hummingbirds would not include long, narrow flower species because nectar in these species might be beyond the reach of their bills. If so, the slope of the regression for flower width versus flower length should be smaller for flower species visited by longer‐billed hummingbirds relative to those visited by shorter‐billed hummingbirds. Analyses of data sets for some North American and Monteverde hummingbirds and their food plants were consistent with this prediction, and bill lengths were significantly correlated with the slopes of the regressions of flower width versus length for seven hummingbird species. Comparisons of observed flower use by some Monteverde hummingbird species to flower assemblages generated at random suggest that these significant regressions were not simply a result of allometric relationships between flower lengths and widths, but in some cases reflected active choice by the birds. The two hummingbird–flower data sets also differed significandy in the scaling of corolla width relative to corolla length. In particular, the Monteverde data set contained a large number of long, narrow flower species, which we suggest is a consequence of a different floral evolutionary history and association with long‐billed hummingbird species. The evolutionary effects of hummingbirds and their flowers upon one another are more complex than has generally been realized, and a consideration of corolla length jointly with other floral characters may improve our understanding of hummingbird‐flower relationships.     

Flower color change accelerated by bee pollination in Tibouchina (Melastomataceae)

Floral color changes are common among Melastomataceae and have been interpreted as a warning mechanism for bees to avoid old flowers, albeit increasing long-distance flower display. Here the reproductive systems of Tibouchina pulchra and T. sellowiana were investigated by controlled pollinations. Their pollinators were identified, and experiments on floral color and fragrance changes were conduced to verify if those changes affect the floral visitation. Both Tibouchina species are self compatible. The flowers lasted three days or more, and the floral color changed from white in the 1st day to pink in the following days. Pollen deposition on stigma induced floral color change. The effectiveness of the pollination is dependent on bees’ size; only large bees were regarded as effective pollinators. In experimental tests, the bees in T. pulchra preferred the natural white flowers while the visitors of T. sellowiana were attracted by both natural and mimetic 1st-day flowers (2nd-day flowers with experimentally attached 1st-day flower petals). During the experiments on floral fragrance, the bees visited both natural and mimetic 1st-day flowers (2nd-day flowers with 1st-day flower scents). In both experiments, the bees avoided natural 2nd-day flowers, but seldom visited modified 2nd-day flowers. The attractiveness of T. pulchra and T. sellowiana flowers cannot be attributed exclusively to the color or the fragrance separately, both factors seemingly act together.     

Honeybees mark with scent and reject recently visited flowers

Summary Experimental evidence is reported for flower-marking by honeybees (Apis mellifera ligustica) while they were foraging on an artificial patch of flowers yielding a continuous and equal flow of sucrose solution. Honeybees marked with scent and rejected all recently visited and nectar-depleted flowers. The short fade-out time of this scent allowed discrimination of flowers that temporarily provided no food. The repellent nature of this scent mark was demonstrated by the use of an air extractor connected to the patch; when the apparatus was turned on, the rejection behaviour disappeared. The movement pattern of foraging bees also contributed to foraging efficiency, as the probability of an immediate return to the flower just abandoned was very low. However, when a quick repeat visit took place, the presence of the repellent scent-mark promoted rapid rejection.     

Causes of Fruit Set Variation in Polygonatum odoratum (Liliaceae)

Abstract: In Polygonatum odoratum (Liliaceae), flowers located distally within the flowering shoot typically exhibit lower fruit set than flowers located proximally. In this study, experiments were performed to investigate whether the lower fruit set of distal flowers is due to pollen limitation, resource competition or "architectural" effects. We found that (1) fruit set and mean number of ovules per flower decline within the flowering shoot from proximal to distal position; (2) variations in the amount of pollen received do not explain the observed differences in fruit set; (3) the fruit set of the most distal flowers was significantly increased by removal of other flower buds in the flowering shoot just before flower opening, indicating that fruit set in these flowers is resource-limited; and (4) removal of proximal flowers increased the fruit set of later flowers to levels similar to those of early flowers of control shoots, arguing against the architectural effects hypothesis.     

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

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

Differences in the diversity and composition of the pollinator assemblage of two co-flowering congeneric alpine wallflowers, Erysimum nevadense and E. baeticum

Many alpine plants display a generalist pollination system where almost any available flower visitor could act as a legitimate pollinator. Co-flowering related plant species displaying a generalized pollination system can decrease their fitness due to interspecific mating. In this study, we determine the difference in diversity and composition of the pollination systems of two co-occurring species endemic to the alpine region of the Sierra Nevada (SE Spain), Erysimum nevadense Reut. and Erysimum baeticum baeticum (Heywood) Polatschek (Brassicaceae), and check for the potential role of floral and plant traits in explaining the observed differences. For this, we labeled 30 plants in two populations of each plant species located in the same area. We determined flower visitor assemblage by sampling all insects approaching the flowers and contacting the sexual organs during 60-min surveys. We found that the diversity of the pollinator assemblage was similar between the two studied wallflower species, both species showing a much generalized pollination system. However, the composition of the pollinator assemblage was different, since the flowers of E. nevadense were visited mostly by beetles and in a lesser extent by hover-flies, whereas the flowers of E. baeticum baeticum were visited mostly by ants and bees. Interestingly, flower traits varied between species, with E. nevadense displaying yellow, smaller and shallower flowers and E. baeticum baeticum displaying purple, large and deeper flowers. These findings suggest that differences in floral traits can explain the observed differences in the composition of the pollinator assemblage between both wallflower species.     

Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae)

The effectiveness of flower visitors as pollinators will determine their potential role as selective agents on flower traits. Pitcairnia angustifolia has floral characters that would fit pollination by long-billed hummingbirds, and they should be the most effective pollinators for this plant. To test this prediction, we characterized the behavior of visitors toward flowers and their pollination effectiveness. Coereba flaveola (bananaquits) was the most frequent flower visitor and acted as a primary nectar robber; however, they pollinated incidentally and deposited pollen on stigmas. The endemic short-billed hummingbird Chlorostilbon maugaeus behaved as a secondary robber and did not pollinate flowers. As expected, the long-billed hummingbird, Anthracothorax viridis, was the most efficient visitor in terms of pollen deposition; however, it was the least frequent flower visitor. Introduced Apis mellifera (honeybees) were second in efficiency at depositing pollen and performed one third of the flower visits. Estimates of the expected rate of pollen deposition by each pollinator did not identify a single most effective pollinator. For P. angustifolia at least three flower visitors including an exotic bee and a nectar robber may be equally important to reproductive success. While these results limit our ability to make predictions on the role of hummingbird-pollination on current flower evolution, they do suggest the potential for pollination redundancy among flower visitors for P. angustifolia populations.