Optimal foraging in bumblebees and coevolution with their plants

Summary The aims of this paper were to consider the coevolution between bumblebee movement patterns within plants and various properties of the plants such as the spatial distribution of their flowers, and to determine the extent to which the bumblebees and the plants can be considered to be maximally adaptive or optimal. Attention was restricted to plants which have flowers arranged on vertical inflorescences and to the bumblebees which visit these plants.It was found that the bumblebees tend to commence foraging at the bottom of each infloresence, that they tend to move from one flower to the closest vertically higher flower, that they miss flowers as they move upwards and that they tend to leave each inflorescence before reaching the top. It was also found for the four common plant species considered that nectar abundance per flower decreases with flower height on an inflorescence, that the flowers with receptive stigmas are restricted to the bottoms of the inflorescences while the flowers shedding pollen occur above them, and that the flowers are arranged approximately in spirals on the inflorescences.The pattern of movements of the bumblebees and the various properties of the plants appear to represent coevolved adaptations. Furthermore the bumblebees' movement patterns appear to be optimal in the sense that they result in the maximum net rate of energy gain to the bumblebees. Further studies are necessary, however, to determine whether or not the plants can be considered to be optimal.An exception to the above scheme is provided by a plant which is quite uncommon in the study area. This plant also has flowers on vertical inflorescences and appears to be pollinated by bumblebees. However, while the pattern of movements of the bumblebees on this plant species are extremely similar to those on the four common species, this plant species exhibits quite different properties from the other four. Two possible explanations for this exception are presented.     

Mechanisms that limit pollinator range in Ericaceae

Studies were conducted in 2001-2003 at Valdai National Park (Novgorod region) and at the Zvenigorod biological station of Moscow State University. The morphology of flowers, flowering dynamics and composition of insect visiting flowers of Ericaceae species: Andromeda polifolia, Chamaedaphne calyculata, Ledum palustre, Oxycoccus palustris, Vaccinium myrtillus, V. uliginosum, and V. vitis-idaea L. were studied. Some species of insects visiting flowers were excluded from the list of pollinators on the basis of observation on their behavior. L. palustre was visited mainly by flies where as other investigated species were visited mainly by bumblebees. In some cases bumblebees were the only visitors of the investigated plants. Mechanisms that protect flowers from flies and short-tongued solitary bees visits and ensure a best pollination by bumblebees are various among different species of Ericaceae. Efficiency of nectary protection also differs among different plant species and is defined by particularities of their habitats and flowering phenology. As far as all species of this family during the flowering are dominants in typical habitats, a competition for the pollination with species of other families in most cases is megligible. Flowering periods of V. vitis-idaea and V. myrtillus in forest ecosystems overlapped weakly. Moreover, V. myrtillus is pollinated mainly by bumblebee queens where as pollinators of V. vitis-idaea are bumblebee workers, solitary bees and horse flies. The other investigated plant species inhabit only oligotrophic peat bogs. Thery are pollinated by bumblebees but periods of flowering are not overlapped and consequently follow one after another. L. palustre and V. uliginosum flower simultaneosly but they are pollinated by different pollinators.     

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.     

Direct and indirect estimates of the selfing rate in small and large individuals of the bumblebee pollinated Cynoglossum officinale L (Boraginaceae)

We measured the relationship between selfing rates and flower number in an experimental population of bumblebee pollinated Cynoglossum officinale , with plants differing in flower number. Results were compared with the prediction of a model based on pollen dynamics and pollinator behaviour. The selfing rate, as measured by multilocus oligonucleotide DNA fingerprinting, increased with flower number and ranged from 0% to 70%. Flowers on large plants received an equal number of visits from bumblebees as flowers on small plants. On large plants more flowers in a row were visited, inducing geitonogamy. The overall relationship between selfing rate and number of flowers can be explained by pollen dynamics and pollinator behaviour without invoking postpollination processes such as differential pollen tube growth and abortion.     

Multi-cycle synchronous protandry in raceme-like inflorescences of a bumblebee-pollinated herb Aconitum grossedentatum

Multi-cycle synchronous dichogamy is expected to be a mechanism for reducing self-pollination and sexual interference. It is often found in plants with umbellate inflorescences where pollinator movement is unpredictable, but not in plants with raceme inflorescences that are pollinated by bumblebees. Plants with raceme inflorescences often acropetally open flowers, resulting in an arrangement of females at lower level and males at upper level. This is good enough to preclude geitonogamy because bees tend to move upwardly within the inflorescences. Furthermore, although the degree of segregation of sexes varies among species, their intraspecific variations within a population have rarely been examined. Here, we present a synchronous protandry in bee-pollinated Aconitum grossedentatum, which has a raceme-like inflorescence and opens flowers basipetally. To evaluate the functional significance of synchronous dichogamy in mating, we firstly observed the distribution of sex phases of open flowers. Then, we assessed the effect of each phase flower on foraging behavior by pollinators and seed-set success. The inflorescences tended to exhibit either male- or female-phase flowers at any moment early in the flowering season, but the degree of segregation of sexes declined over time within a population. The degree of the segregation did not affect bumblebee visits to flowers, but it decreased seed-set success of female-phase flowers at that time. Our results demonstrated that synchronous protandry was beneficial for pollination success in A. grossedentatum by avoiding geitonogamy. Nevertheless, we also found asynchronous protandry late in the season, suggesting that the benefits by synchronous protandry decreased over the season.

     

Risk‐averse inflorescence departure in hummingbirds and bumble bees: could plants benefit from variable nectar volumes?

Most hermaphroditic, many-flowered plants should suffer reduced fitness from within-plant selfing (geitonogamy). Large inflorescences are most attractive to pollinators, but also promote many flower visits during a single plant visit, which may increase selfing and decrease pollen export. A plant might avoid the negative consequences of attractiveness through modification of the floral display to promote fewer flower visits, while retaining attractiveness. This report shows that increasing only the variance in nectar volume per flower results in fewer flower visits per inflorescence by wild hummingbirds ( Selasphorus rufus ) and captive bumble bees ( Bombus flavifrons ) foraging on artificial inflorescences. Inflorescences were either constant (all flowers contained the same nectar volume) or variable (half the flowers were empty, the other half contained twice as much nectar as in the constant flowers). Both types of inflorescence were simultaneously available to foragers. Risk-averse foraging behaviour was expressed as a patch departure preference: birds and bees visited fewer flowers on variable inflorescences, and this preference was expressed when resource variability could be determined only by concurrent sampling. When variance treatments were clearly labelled with colour and offered to hummingbirds, the departure effect was maintained; however, when preference was measured by inflorescence choice, birds did not consistently prefer to visit constant inflorescences. The reduced visitation lengths on variable inflorescences by both birds and bees documented in this study imply that variance in nectar production rates within inflorescences may represent an adaptive trait to avoid the costs of geitonogamy.     

Size-dependent pollination efficiency in Anchusa officinalis (Boraginaceae): causes and consequences

Summary Bumblebees foraging on the self-incompatible Anchusa officinalis fly between near neighbour plants and between near neighbour inflorescences within plants. Although many-flowered plants attracted most bumblebees these plants received fewer visits on a per flower basis than smaller plants, and each bumblebee visited a smaller proportion of the flowers. The calculated effective visitation rate per flower was highest on plants of an intermediate size. If pollen-carryover was assumed to be limited the most efficient plant was predicted to be smaller since the proportion of fertilized flowers per bumblebee visit is expected to decrease further on the largest plants in relation to the total flower number. These predictions were tested by measuring fruit-set in the field. The percentage fruit-set decreased with plant size at all sizes that were investigated. That the most efficient plant was small indicates that pollen-carryover was indeed limited. However, the low percentage fruit-set associated with large size did not present a serious problem since the total estimated seed production per plant still increased with size. Selection favoring smaller plants may be low or absent in Anchusa.     

Floral colour change in Pedicularis monbeigiana (Orobanchaceae)

We examined the effects of the retention of colour-changed flowers on long- and short-distance attractiveness of bumblebees and the likelihood of successive flower visits by bumblebees in Pedicularis monbeigiana. The lower lip changed colour with age from white to purple. Hand geitonogamous pollination significantly reduced seed production. No pollen limitation occurred in this species. Purple-phase flowers contributed minimally to pollinator attractiveness at long distance. The combination of less reproductive flowers with a lower amount of reward and floral colour change enabled plants to direct pollinators to reproductive, highly rewarding white flowers at close range. A high percentage of purple-phase flowers in an inflorescence was associated with a marked reduction in the frequency of successive flower visits to individual plants. We suggest floral colour change in P. monbeigiana may serve as a mechanism for enhancing inter-individual pollen transfer and reducing intra-individual pollen transfer.     

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 generalised mimicry system involving angiosperm flower colour, pollen and bumblebees’ innate colour preferences

Flower colour is a major advertisement signal of zoophilous plants for pollinators. Bees, the main pollinators, exhibit innate colour preferences, which have often been attributed to only one single floral colour, though most flowers display a pattern of two or several colours. The existing studies of floral colour patterns are mostly qualitative studies. Using a model of bee colour vision we quantitatively investigate two questions: whether or not component colours of floral colour patterns may mimic pollen signals, and whether or not bumblebees exhibit innate preferences for distinct parameters of naturally existing floral colour patterns. We analysed the spectral reflectances of 162 plant species with multicoloured flowers and inflorescences, distiniguishing between inner and outer colours of floral colour patterns irrespective of the particular structures so coloured.We found that:– The inner colour of radially symmetrical flowers and inflorescences and of zygomorphic flowers appears less diverse to bees than the peripheral colour.– The inner colour of most radial flowers and inflorescences as well as the inner colour of a large number of non-related zygomorphic flowers appears to bees to be very similar to that of pollen.– Bumblebees (Bombus terrestris) exhibit innate preferences for two-coloured over single-coloured dummy flowers in a spontaneous choice test.– Bumblebees exhibit innate preferences for dummy flowers with a large over those with a small centre area.– Bumblebees exhibit innate preferences for dummy flowers with a centre colour similar to that of pollen over those with another centre colour.Our findings support the hypotheses that the inner component of floral colour patterns could be interpreted as a generalised and little recognised form of mimicry of the colour of visually displayed pollen, that bumblebees exhibit innate preferences regarding colour and size parameters of floral colour patterns, and that these correspond to visually displayed pollen. These findings together suggest a prominent role of floral colour patterns in advertisement to and guidance of naive flower visitors.     

Pollination and breeding system of the enigmatic South African parasitic plant Mystropetalon thomii (Mystropetalaceae): rodents welcome,but not needed

• Unrelated plants adapted to particular pollinator types tend to exhibit convergent evolution in floral traits. However, inferences about likely pollinators from ‘pollination syndromes’ can be problematic due to trait overlap among some syndromes and unusual floral architecture in some lineages. An example is the rare South African parasitic plant Mystropetalon thomii (Mystropetalaceae), which has highly unusual brush‐like inflorescences that exhibit features of both bird and rodent pollination syndromes.
• We used camera traps to record flower visitors, quantified floral spectral reflectance and nectar and scent production, experimentally determined self‐compatibility and breeding system, and studied pollen dispersal using fluorescent dyes.
• The dark‐red inflorescences are usually monoecious, with female flowers maturing before male flowers, but some inflorescences are purely female (gynoecious). Inflorescences were visited intensively by several rodent species that carried large pollen loads, while visits by birds were extremely rare. Rodents prefer male‐ over female‐phase inflorescences, likely because of the male flowers’ higher nectar and scent production. The floral scent contains several compounds known to attract rodents. Despite the obvious pollen transfer by rodents, we found that flowers on both monoecious and gynoecious inflorescences readily set seed in the absence of rodents and even when all flower visitors are excluded.
• Our findings suggest that seed production occurs at least partially through apomixis and that M. thomii is not ecologically dependent on its rodent pollinators. Our study adds another species and family to the growing list of rodent‐pollinated plants, thus contributing to our understanding of the floral traits associated with pollination by non‐flying mammals.

     

Unidirectionality of floral colour changes

Many angiosperms have arranged their flowers in inflorescences forming a distinct signalling unit to flower visitors. In some species, the flowers of inflorescences undergo a temporal colour change corresponding exactly to a change in the reward status. Based on information obtained from the spectral reflection curves of pre-change and postchage colours of flower corollas and/or floral guides, it was possible to demonstrate that the colour phase associated with reward closely corresponds to the visual stimuli which trigger behavioural responses of inexperienced flower visitors, and that the colour phase associated with less reward corresponds to visual stimuli less attractive to naïve flower visitors. Reciprocal colour changes were not observed. It is to be assumed that the unidirectionality of floral colour changes is an adaptation of angiosperms aimed at the guidance of first-time flower visitors. Signalling reward to inexperienced flower visitors is an additional function of floral colour changes. The main function of floral colour changes, however, is to provide cues with which the flower visitors can learn to associate one colour phase with reward.     

The mechanisms of the restriction of pollinator range in the fireweed (Chamaenerion angustifolium) and 2 species of geranium (Geranium palustre) and G. pratense)

Flowers of Chamaenerion angustifolium, Geranium palustre and G. pratense are visited by more than 100 insect species. For all plants the spectrum of visitors is similar. However the role of insects species in pollination is different and depends on the stamen and stigma length, flexibility of pedicle and feeding behaviour of insect inside flower. The possibility to take and to transport pollen grains usually increase with the size of insect. The nature of this correlation is determined by stamen and stigma length. Pollinators of G. palustre with short stamens and stigmas are smaller than those of Ch. angustifolium and G. pratense. On the other hand, more flexible pedicle of G. palustre prevent the flowers from visits of big insects. Three plants studied by the authors are not equally attractive for different insect groups. Dense in fluorescence of Ch. angustifolium and G. pratense that usually are lifter under the grass are very attractive for foraging social insects (honey bee, bumblebee). Flies avoid long distance travelling and prefer single flowers located not far from each other. For instance G. palustre is more attractive for flies not for social bees. It is pollinated mainly by flies and solitary bees with average weight of 10-70 mg. The main pollinators of Ch. angustifolium and G. pratense are honey bees, bumblebees and wasps with average mass exceeding 70 mg.     

Modification of bumblebee behavior by floral color change and implications for pollen transfer in <Emphasis Type="Italic">Weigela middendorffiana</Emphasis>

Flowers of Weigela middendorffiana change the color from yellow to red. The previous study revealed that red-phase flowers no longer have sexual function and nectar, and bumblebees selectively visit yellow-phase flowers. The present study examined how retaining color-changed flowers can regulate the foraging behavior of bumblebees and pollen transport among flowers within (geitonogamous pollination) and between (outcrossing pollination) plants and how the behavior is influenced by display size (i.e., number of functional flowers) and visitation frequency. The visitation frequencies of bumblebees to plants and successive flower probes within plants were observed in the field using plants whose flower number and composition of the two color-phase flowers had been manipulated. To evaluate pollination efficiency over multiple pollinator visits, a pollen transport model was constructed based on the observed bumblebee behavior. In the simulation, three flowering patterns associated with display size and existence of color-changed flowers were postulated as follows: Type 1, large display (100 functional flowers) and no retention of color-changed flowers; Type 2, small display (50 functional flowers) and retention of color-changed flowers (50 old flowers), and; Type 3, large display (100 functional flowers) and retention of color-changed flowers (100 old flowers). Color-changed flowers did not contribute to increasing bumblebee attraction at a distance but reduced the number of successive flower probes within plants. Comparisons of pollen transfer between Types 1 and 3 revealed that the retention of color-changed flowers did not influence the total amount of pollen exported when pollinator visits were abundant (>100 visits) but decreased geitonogamous pollination. Comparisons between Types 2 and 3 revealed that the discouragement effect of floral color change on successive probes accelerated in plants with a large display size. Overall, the floral color change strategy contributed to reduce geitonogamous pollination, but its effectiveness was highly sensitive to display size and pollinator frequency.     

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

Flower visitors learn to avoid food-deceptive plants and to prefer rewarding ones by associating floral cues to rewards. As co-occurring plant species have different phenologies, cue-reward associations vary over time. It is not known how these variations affect flower visitors’ foraging costs and learning. We trained bumblebees of two colonies to forage in a community of deceptive and rewarding artificial inflorescences whose flower colours were either similar or dissimilar. We then modified the community composition by turning the rewarding inflorescences into unrewarding and adding rewarding inflorescences of a novel flower colour. In the short term, bees trained to similar rather than dissimilar inflorescences experienced higher costs of foraging (decreased foraging speed and accuracy) in the novel community. The colonies differed in their speed-accuracy trade-off. In the longer term, bees adapted their foraging behaviour to the novel community composition by increasingly visiting the novel rewarding inflorescences.     

Density-dependent and frequency-dependent selection by bumblebees Bombus terrestris (L.) (Hymenoptera: Apidae)

The behaviour of bumblebee workers foraging on arrays of artificial flowers of two colour morphs was observed. Experiments were conducted on arrays of varying morph frequencies and at three different total flower densities. Bumblebees consistently showed a preference for the commonest colour morph, and this behaviour was not significantly affected by changing density. In contrast, frequency-independent preferences changed significantly with density. At low densities, there was a strong bias towards the more conspicuous colour, whereas at higher densities there was no overall colour bias. Flight distances between flowers decreased significantly at high density. Bumblebees also visited flowers of similar colours sequentially, but this behaviour was not density-dependent. It is suggested that as densities increase, there is an increased probability that bumblebees detect yellow flowers, which were probably less conspicuous compared with blue flowers, and that this might be caused by changes in flight speed with flight distance. Where there is a positive relationship between pollinator visitation and the relative fitness of a floral morph, the observed behaviour would induce positive frequency-dependent selection on a plant population with two corolla colour morphs on which the bumblebees were foraging, which would result in stabilizing selection for a single corolla colour, irrespective of density. There was no indication that rare colour morphs would be preferred at high density. The probability of different corolla colour morphs going to fixation would, however, be affected by density.     

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.     

Pollination Biology of Hosta sieboldiana (Lodd.) Engler and H. sieboldii (Paxton) J. Ingram (Liliaceae)

Abstract The pollination biology of Hosta sieboldiana and H. sieboldii is investigated comparatively in Central Japan. Both species have homogamous, one-day flowers pollinated by bumblebees. The abdomens of the bees touch the stigma on the extended style when they land on the anthers inside the herkogamous flower, and autogamy is effectively prevented. However, the flowers are fairly self-compatible, and geitonogamy may occur rather frequently because two or more flowers on a scape very often bloom at the same time and many ramets are contiguous. The pollen/ovule ratios suggest that these species are facultative outbreeders. The flower of H. sieboldii seems completely suited to bumblebee pollination. In H. sieboldiana the stigma of the flower, whose style strongly protrudes, is not always touched by bumblebees, but frequent visitation of bumblebees results in pollination of almost all the flowers. Both species have similar pollination systems but seem reproductively isolated by blooming times and habitats. Their common pollinators, however, may sometimes cause introgressive hybridization in contiguous populations.     

Small but attractive: female‐biased nectar production and floral visitors in a dimorphic shrub

• In sexually dimorphic species, hermaphrodite flowers in gynodioecious species or male flowers in dioecious species are often larger and produce more nectar than their conspecific female flowers. As a consequence, hermaphrodite or male flowers frequently receive more pollinator visits.
• Sex ratio, flower size, floral display, nectar production and floral visits were evaluated in two natural populations of Fuchsia thymifolia, a morphologically gynodioecious but functionally subdioecious insect‐pollinated shrub.
• Sex ratio did not differ from the expected 1:1 in the two studied populations. As expected, hermaphrodite flowers were larger than female flowers, but in contrast to the general pattern, hermaphrodite flowers did not produce nectar or produced much less than female flowers. Flower visitors were flies (68%) and bumblebees (24%), both of which showed a preference for female flowers. No sex difference was detected in either flower longevity or floral display across the flowering season.
• Higher nectar production by females may attract more pollinators, and may be a strategy to enhance female reproductive success in this species. Finally, floral dimorphism and insect preferences did not seem to hamper the maintenance of sub‐dioecy or prevent the evolution of dioecy in F. thymifolia.

     

Pollinator Restriction in the Narrow-tube Flower Type of Mertensia ciliata (James) G. Don (Boraginaceae)

Abstract Mertensia ciliata (Boraginaceae) includes two flower types with different corolla tube widths, wide and narrow. The former is pollinated by both queens and worker bumblebees, while the latter type is pollinated exclusively by bumblebee workers. Morphological comparisons between the flowers and the bumblebees showed that the relationship between the width of the corolla tube mouth and the head width of the bumblebee is a primary factor restricting pollinators to workers in the narrow-tube type. Length of the proboscides and corolla tube are of secondary importance for this restriction, since some queens are not able to reach the bottom of a narrow corolla tube even if their proboscis is extended fully.