Flower Constancy Research Articles

Effects of a reward downshift on the consummatory behavior and flower choices of bumblebee foragers

Insect foragers often exhibit flower constancy, the tendency to visit single flower types rather than sample alternative flowers that provide equal or higher levels of reward. We employed a negative incentive contrast procedure to examine whether a decrease of sucrose concentration in a regularly visited flower type affects bumblebee ( Bombus impatiens) consummatory or choice behavior. Subjects were trained to enter a test arena where they foraged on a single, red, artificial flower that contained 140 μl of sucrose solution. Subjects were reinforced with a concentration of either 0.50 or 0.20 sucrose solution in 20 trials and in 12 subsequent test trials subjects were given a choice between a red and yellow flower that each contained 140 μl of 0.20 sucrose solution. Subjects that experienced a downshift of reward showed an abrupt disruption in consumption of sucrose solution from the red flower. These subjects were also significantly more likely to visit the novel yellow flower than subjects that were reinforced with 0.20 sucrose solution in red flowers in all trials. However, the effects of the downshift of reward were transient and appeared to disrupt consummatory behavior more strongly than flower preferences. These results support the idea that bumblebee foragers form expectations of reward in flowers—as is implied by the results of studies of honeybees—and suggest that unrealized expectations of reward may cause foragers to sample alternative flowers or to fly considerable distances in search of particular types of flowers.

Pollination and breeding system of Eritrichium nanum (Boraginaceae)

Flower development, pollination and breeding system of the high alpine cushion plant, Eritrichium nanum (Boraginaceae), were investigated in nine populations from the European Alps at altitudes of 2700 m–3200 m. Peak flowering period lasts longer than a month, from mid-June to the end of July. In contrast to statements in the literature that flowers are protogynous and nutlets remain in their calyx until spring we found a distinct protandry and nutlets being dispersed before mid-September. Various insects from 12 families, but mostly Diptera, frequently visited E. nanum flowers, with flies from the families Anthomyiidae and Muscidae being the predominant visitors. Under optimal conditions (max. solar radiation, min. wind force), visitation rates of 200 simultaneously observed flowers reached 32.5–46.7 insects per hour, i.e. 0.16–0.24 insects per flower per hour. However, the commonly observed Anthomyiidae and Muscidae clearly preferred the white-yellowish flowers of Saxifraga exarata and Saxifraga bryoides which are abundant at E. nanum sites and which are certainly also pollinated by species of these two fly families. The flowers of these Saxifraga species offer plenty of nectar and may compete for pollinators with E. nanum, when they are flowering in its proximity. However, various other insects like Pontia callidice and Psodos sp. (Lepidoptera) as well as Andrena sp. (Hymenoptera) and especially Eristalis tenax and closely related hoverflies showed a higher degree of flower constancy to E. nanum, often flying from a blue Eritrichium cushion to the next and hence causing outcrossing. The five fornices of E. nanum flowers which obstruct the tube containing stamens and nectar, are a feature which differs distinctly from the syndrome of fly-pollinated flowers with easily accessible nectar. Consequently pollination by flies in E. nanum seems to be caused mainly by the unfavorable ecological conditions at high altitudes, where flies are the most frequent insects. Bagging experiments showed that outcrossing and geitonogamy are the prevailing pollination modes, and autogamy, although possible, plays only a minor role.

Foraging decisions in nectarivores: unexpected interactions between flower constancy and energetic rewards

Foraging decisions are based on a suite of choices that include energetics and physiological constraints. Although travelling farther to harvest a greater net energetic reward is beneficial, many animals opt for a smaller net reward that requires less travel. Recent discoveries of a visual basis for flower constancy in the honeybee, Apis mellifera, led us to examine older reports that colour cues are superceded by energetic considerations. Here we show that when individual bees foraged on pedicellate artificial flowers varying in colour and interfloral distance, their behaviour depended on the colours in the choice test. Colours of similar spectral reflectance (blue versus white), that would be clustered in the bee's visual colour space, elicited more visits to the closest flower when rewards were equal, but individuals travelled a greater distance to harvest a higher energetic reward when reward quality varied. Bees chose the closest flower more often when reward volume decreased while quality remained constant. Yet, even when all flowers were identical (morphology and reward), and only interfloral distance varied, bees did not always visit the closest flower. A dramatic difference was seen when the dimorphism was yellow-blue, colours quite separate in the bee colour space and known to elicit constancy behaviour. Here, bees visited the closest flower only 5% of the time, and varying reward volume did not elicit different behaviour. Animals thus display differential foraging behaviour with respect to environmental cues that must be considered when asking questions about other behavioural parameters.

Evidence for handedness in bumblebees

We describe a simple study of how bumblebees (Bombus spp.) behave when visiting florets which are arranged in a circle around a vertical inflorescence. In four species of bees, individuals showed a tendency for rotation in the same direction around each inflorescence on successive visits, i.e., each individual tended to go either clockwise or anticlockwise. Similar behavior has also been observed in mammals including humans. The implications of this tendency to repeat tasks in the same way are discussed, particularly in relation to our understanding of the phenomenon known as flower constancy. In humans, the tendency for individuals to turn in a particular direction is strongly related to handedness. In three of the four bee species there was a significant overall tendency for the bees to rotate in a preferred direction, suggesting that they too may exhibit handedness.

Transposition of flower height by bumble bee foragers (Bombus impatiens)

Honeybees learn visual characteristics of reinforced and non-reinforced flowers in differential conditioning experiments (i.e., experiments that require subjects to choose between a reinforced and non-reinforced flower). In this study bumble bee foragers (Bombus impatiens) were trained in a transposition paradigm to determine if the relational properties of flowers also influence choice behavior. Subjects in one group (group A) were trained with repeated choices between a medium-height flower replete with sucrose solution and an empty tall flower until the medium-height flower was sampled preferentially in five consecutive trials. A second group (group B) was trained on the medium height flower alone for five trials. In a single test trial subjects were given a choice between the medium-height flower and a short flower, each filled with water. A control group showed no preference in this test. Group B subjects showed a significant preference for the medium-height flower and group A subjects that exhibited flower constancy (i.e., sampled only the medium-height flower in training trials) showed an identical pattern of choice. Subjects in group A that sampled both flowers during training, in contrast, transposed flower height and preferred the short flower. These results suggest that the choice behavior of bumble bee foragers is influenced by relational and absolute properties of flowers. The flower characteristics learned by foragers appear to depend on the difficulty of the discrimination problem and the context in which flowers are sampled. Patches of flowers limited in phenotypic variability may produce simple associative learning and flower constancy by foragers.

Are insects flower constant because they use search images to find flowers?

Many insects which gather nectar or pollen exhibit flower constancy, a learned fidelity to a particular species of plant. Recent studies suggest that foraging insects may use a perceptual mechanism akin to a search image to detect flowers, in a manner analogous to the way that predators search for prey. This has emerged as an alternative (but not mutually exclusive) explanation for flower constancy to that proposed by Darwin, who suggested that it may result from a limited ability to learning or remember the handling skills appropriate for particular flowers. However, search images are thought to be a mechanism for locating cryptic prey. Plants which are pollinated by animals have evolved brightly coloured flowers to attract the attention of their pollinators. It thus seems implausible to argue that flowers may actually be cryptic. One possible explanation for this apparent contradiction is that flowers are effectively cryptic when viewed against a background which contains many other flowers of similar colour. I present experimental evidence which suggests that a background of flowers of similar colour does reduce foraging efficiency of bumblebees, but that a background of dissimilarly coloured flowers has no effect. This I interpret as evidence that flowers may be cryptic, suggesting that pollinators may indeed use a search image in location of flowers. However, the relative importance of constraints on foragers’ abilities to locate flowers versus their abilities to handle them as causes of flower constancy remain to be elucidated.

Inflorescence Height Affects Visitation Behavior of Bees–A Case Study of an Aquatic Plant Community in Bolivia1

ABSTRACTWe studied the bee fauna visiting a plant community of 10 species of flowering aquatic plants in an inundated savanna region in Bolivia. In total we observed 36 bee species in 17 genera at the flowers. Cluster analysis of the similarities among the plant species in terms of their visitor spectra showed a division into two groups: plants with inflorescence heights shorter than the grass height and plants with inflorescences projecting out of the surrounding vegetation. Larger bees of the genera Apis, Melipona, Bombus, and Xylocopa were observed only at flowers above the surrounding vegetation. Smaller, mainly solitary bees (e.g., Augochlorella, Ancyloscelis) visited flowers in the dense vegetation near the water surface. Analyses of the pollen loads revealed that most individuals were highly flower constant. When bees carried different pollen types, it was generally pollen from flowers within a single stratum. We discuss specialization, flower constancy, competition, and different foraging strategies as possible reasons for stratum fidelity.

Flower Constancy, Insect Psychology, and Plant Evolution

Individuals of some species of pollinating insects tend to restrict their visits to only a few of the available plant species, in the process bypassing valuable food sources. The question of why this flower constancy exists is a rich and important one with implications for the organization of natural communities of plants, floral evolution, and our understanding of the learning processes involved in finding food. Some scientists have assumed that flower constancy is adaptive per se. Others argued that constancy occurs because memory capacity for floral features in insects is limited, but attempts to identify the limitations often remained rather simplistic. We elucidate now different sensory and motor memories from natural foraging tasks are stored and retrieved, using concepts from modern learning science and visual search, and conclude that flower constancy is likely to have multiple causes. Possible constraints favoring constancy are interference sensitivity of short-term memory, and temporal limitations on retrieving information from long-term memory as rapidly as from short-term memory, but further empirical evidence is needed to substantiate these possibilities. In addition, retrieving memories may be slower and more prone to errors when there are several options than when an insect copes with only a single task. In addition to memory limitations, we also point out alternative explanations for flower constancy. We then consider the way in which floral parameters, such as interplant distances, nectar rewards, flower morphology, and floral color (as seen through bees' eyes) affect constancy. Finally, we discuss the implications of pollinator constancy for plant evolution. To date there is no evidence that flowers have diverged to favor constancy, although the appropriate tests may not have yet been conducted. However, there is good evidence against the notion that pollinator constancy is involved in speciation or maintenance of plant species integrity.

Floral constancy in Trigona stingless bees foraging on artificial flower patches: a comparative study

SUMMARYFlower constancy is described qualitatively and quantitatively for stingless bees (Apidae, Meliponinae). Flower constancy has been reported for various insects, but the degree of constancy seems to differ from species to species. To test the hypotheses that the degree of flower constancy depends on colony size and foraging strategy, flower constancy was measured in three species of stingless bees that differed in colony size and foraging strategies. When the artificial flower types differed in colour or odour, most bees preferred one of the two flower types. On average, 77% of successive visits were directed towards the previously visited flower type without major differences between the species. Constancy on odour was not generally overruled by constancy on colour or vice versa. When flower types differed in shape, the majority of the bees visited the two types in a random way. Thus, differences in colony size and foraging strategy did not relate to flower choice performance in the Trigona species. The degree of flower constancy in the stingless bee species studied was lower than that reported for European honey bees (Apis mellifera), but comparable with that reported for Asian honey bees (Apis cerana). We hypothesize that bees of tropical climates will be generally less constant than bees of temperate climates, due to different (environmentally imposed) optimal foraging strategies.

Flower constancy in the hoverflies Episyrphus balteatus (Degeer) and Syrphus ribesii (L.) (Syrphidae)

The causes and consequences of flower constancy have been the focus of many studies, but almost all have examined the foraging behavior of bumblebees, honeybees, or butterflies. We test whether constancy occurs in an overlooked group of pollinators, the syrphid flies. Foraging sequences of wild flies of two species, Episyrphus balteatus and Syrphus ribesii were examined when visiting flowers in seminatural plant communities and in artificial arrays of two color morphs of Lobularia maritima planted at a range of frequencies. Both species exhibited marked floral constancy when foraging in the mixed-plant community. Because all groups of pollinating insect so far examined exhibit constancy at least under some circumstances, we suggest that this is the predominant strategy used by pollinators and that there is probably a common explanation. Neither syrphid species exhibited constancy to different color morphs within a plant species, in contrast to previously published studies of Hymenoptera foraging among polymorphic flowers, which all describe positive frequency-dependent selection. Possible explanations for this discrepancy are discussed. We argue that constancy in these syrphids is unlikely to result from learning constraints on handling ability, currently the most widely accepted explanation for flower constancy, because they forage primarily for pollen which is easily located inmost flowers they visit.

Sensori-motor learning and its relevance for task specialization in bumble bees

Individual bees often restrict their visits to only a few species out of the multitude of available plants. This flower constancy is likely caused by limitations of memory for motor patterns, sensory stimuli, or reward levels. Here we test the implications of sensori-motor learning and memory for flower constancy. Artificial “flowers” with two distinct “morphologies” were used, so that in each flower type, a different motor pattern was needed to reach the nectar. As in natural flowers, these morphological types were associated with sensory signals (blue and yellow color stimuli). Bees which learned only a single task were more efficient in several ways than those which had learned two: they made fewer errors, had shorter flower handling times, took shorter times to correct errors, and transitions between flowers were initially more rapid. For bees which had learned two tasks, performance depended strongly on the training schedule: if each task was learned with blocked trials, the memory for the second appeared to interfere with that for the first. Interference affected only the association between flower signal and motor pattern, not the motor pattern itself. This was not the case if bees were trained for both tasks with alternating trials. In that case, bees rapidly learned both tasks, albeit with worse saturation levels than bees which had learned only one. Bees transferred the experience gained on one task to a second task: their initial performance on the second task was better than their initial performance on the first. On the other hand, performance on the second task in the saturation level (in which bees no longer improve their efficiency) was worse than on the first task (negative transfer). In the saturation phase, performance did not directly depend on switch frequency, but on whether the bee had one or two options in memory. Thus, while bees would become proficient at two tasks more quickly if their acquisition phase included switches, such switches had no measurable effect in the saturation phase. The implications of these findings for foraging are discussed using modern learning theory.

HUMMINGBIRD BEHAVIOR AND MECHANISMS OF SELECTION ON FLOWER COLOR INIPOMOPSIS

Apparent associations between flower color and type of pollinator might be explained by correlations between color and other floral traits, rather than by narrow pol- linator preferences for color. To explore this possibility, we obtained flowers varying nat- urally in color, nectar reward, and morphology, from a hybrid zone between Ipomopsis aggregate and L tenuituba in western Colorado, United States. We used aviary and field experiments to study preferences of hummingbirds for unmanipulated flowers and for flow- ers in which we experimentally dissociated color from nectar reward and morphology. Hummingbirds preferred red flowers of L aggregate, which contain superior nectar rewards and have relatively broad corolla tubes, relative to flowers of L tenuituba, which are white, contain small nectar rewards, and have narrow tubes. There was no evidence of flower constancy. When presented with flowers differing only in color, birds showed a spontaneous preference for red. However, this preference could be reversed by making white flowers more rewarding than red. When plants of both parental species and their hybrids were placed in an array in the field, with all flowers painted red, hummingbirds preferred to visit the more rewarding, wider tubed L aggregate. These results suggest that pollinator-mediated selection could act on color, shape, and nectar separately. Experimental manipulations that dissociate these traits are essential to distinguish direct from correlated selection. Also, hummingbird selection favoring red flowers may result from past experience and, thus, may depend on the ecological context.

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.

Spontaneous flower constancy and learning in honey bees as a function of colour

When presented with an artificial flower patch of blue and yellow pedicellate flowers, individual honey bees,Apis melliferaL., became constant to one of the two flower colours, rarely even sampling the alternative colour. Some bees visited only blue flowers while others visited only yellow flowers. This paper describes the onset of constancy for bees that had had no experience with the experimental apparatus. In 3020 visits, bees failed to land on or drink from the flower colour on which they first landed only 17 times. This behaviour was not modified by quality or quantity of reward, training to the experimental site, group effects or presence of odour during trials. However, when we trained bees to a target painted with two colours and then forced them to sample monomorphic flower patches in sequence, all bees visited the only colour present: yellow or blue. When we subsequently offered these same bees yellow and blue flowers simultaneously (rewarded choices), they became constant. Eleven of 23 bees showed constancy to the less rewarding flower morph without even sampling the alternative. Those bees failed to sample even though they had previously been forced to visit the alternative flower morph, which offered a reward with twice the calories/volume. Constancy is thus spontaneous in honey bees, but it can be hidden by some experimental protocols designed to study learning.

A Preliminary Study of the Pollination Ecology of Pedicularis in the Chinese Himalaya

Abstract The pollination ecology of fourteen species of Pedicularis (Scrophulariaceae) was studied in the subalpinealpine zone of the Sichuan Himalaya. Bumblebees (Bombus Latr.) sternotribically pollinated rostrate, nectarless species with very long corolla tubes by scraping pollen. Pollinators on short‐tubed, nectarless, rostrate species scraped or vibrated pollen, and nectariferous species were pollinated nototribically by nectar foragers or sternotribically by pollen foragers. Stigmas contacted residual pollen in the midline of the insect body. No evidence of lepidopteran pollination was found in any Pedicularis species. Pedicularis floral structure and function are considered to have coevolved with foraging selection by bumblebees, but pollination syndromes are not specific for a single bumblebee species nor are Bombus foragers restricted to a single plant species. Analysis of corbicular pollen loads of foragers on Pedicularis revealed a moderate degree of flower constancy, especially among foragers on nectarless flowers, probably contributing to speciation in the genus. Up to nine Pedicularis species flowered sympatrically and synchronously, and some species exhibited microhabitat selection. No putative hybrids were identified. Concepts of floral evoution in Pedicularis are in need of revision in light of new evidence presented here.

Foraging strategies in the small skipper butterfly,Thymelicus flavus: when to switch?

Many insects foraging for nectar or pollen exhibit flower constancy, a learned fidelity to a particular species of plant that previously provided a reward. Constancy may persist even when alternative flowers are available that provide a greater or less variable reward. This strategy entails more travelling time than one of generalization (visiting all suitable flowers as they are encountered). The consensus at present is that this increase in travelling time is offset by decreases in handling time; switching between flower species incurs a cost in time spent learning to ‘handle’ the new flower species that is avoided by remaining constant. If this is so, then the optimal strategy should depend upon the density of flower species (and thus the travelling time), with switching occurring below a threshold density of the target flower species. This prediction is tested using the butterfly,Thymelicus flavus, by analysing foraging patterns under natural conditions. This species exhibited constancy: of 465 visits to flowers 85% were to the same species as last visited. As predicted switches between flower species occurred in response to low encounter rates of the flower species on which the individual had previously fed. However, butterflies ignored the vast majority of suitable flowers that they encountered, even when they were of the species to which they were constant. This casts doubt on explanations for flower constancy as an adaptive strategy that minimizes handling time and maximizes resource acquisition per unit time within learning constraints.

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

AbstractThis study examines the role of learning and memory in the butterfly Pieris 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 of Erigeron 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 that P. 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 that P. 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.

Effect of flower complexity on relearning flower-handling skills in bumble bees

Pollinators often forage sequentially among the flowers of the same plant species while bypassing flowers of other rewarding species. Darwin proposed that it is more efficient for pollinators to remain constant to one plant species because switching to a second species interferes with their ability to recall a previously learned flower-handling technique. This interference hypothesis was tested using Bombus impatiens workers. Bees that had learned to handle one type of flower (species A) were retested on species A after they had learned to handle a second type of flower (species B). Interference effects were detected by comparing flower access times (time to insert the tongue into the flower) during the retesting period with initial access times on species A. Bees retested on both simple (red clover, Trifolium pratense) and complex (toadflax, Linaria vulgaris) flowers showed no evidence of interference after learning simple-flowered plant species (blueweed, Echium vulgare; purple loosestrife, Lythrum salicaria). However, bees relearning the complex flowers of toadflax showed a 2.2-s (81%) increase over their initial access time after switching to a second complex-flowered species (orange touch-me-not, Impatiens capensis). These results suggest that the interference effects incurred by bees switching between toadflax and orange touch-me-not under biologically realistic conditions are relatively small, and are unlikely to account for flower constancy in bumble bees.

Pollen‐Foraging Dynamics of Subalpine Bumblebees (Bombus Latr.)

Abstract A 23‐year study on Mount Rainier of nectar‐foraging hummingbirds and pollen‐foraging bumblebees (Bom‐bus Latr.) indicated a constant relative frequency of Bombus species in the area and a wide occurrence of insect species on flowers plus a wide range of flower species pollinated by a single insect. Early‐blooming plants had a high queen/worker pollinator ratio, while workers predominated on later‐blooming plants. No altitudinal difference in distribution of Bombus species occurred. Analysis of 955 corbicular pollen loads from 1158 bumblebees collected yielded 49.5% monolecty for queens and 34.5% for workers with a wider range for queens than for workers. Colors of corollas photographed in visible and ultraviolet light corresponded to the visual spectra of animal pollinators. In the stable plant‐pollinator community investigated, pollinating insect activity appears phenologically controlled by floral anthesis and behaviorally related to floral form and function. Bumblebee tongue length, however. Is not a valid determinant for foraging niche separation except in Castilleja with a deep corolla tube accommodating long tongues of hummingbirds and bumblebees. It is concluded that in a biotic community well‐coordinated with the physical environment, limited flower constancy of pollen‐foraging pollinators appears to contribute a necessary degree of adaptive versatility through sharing of insect and floral resources. Flower constancy is primarily a function of the circumstance in which a pollinator operates and not simply a characteristic of the pollinator itself.

Pollen Harvest by Stingless Bee Foragers (Hymenoptera, Apidae, Meliponinae)

Abstract Data on pollen load capacity and flower constancy are discussed for nine stingless bee species. The foragers present high levels of flower constancy and often visit only one flower type (on average 97% of bee foragers), rarely a few flower types (on average 3% of bee foragers), during the same foraging trip. The latter foragers exhibit no tendencies for choosing similar sources, related either to flower type or to pollen type. Pollen load capacity (the ratio between pollen load weight/worker weight) decreases as forager body weight increases, so it is larger in smaller stingless bees species and smaller in larger ones. Nevertheless, it seems that specific load capacity also depends on pollen types.