A bee’s eye view of remarkable floral colour patterns in the south-west Australian biodiversity hotspot revealed by false colour photography

Background and AimsColour pattern is a key cue of bee attraction selectively driving the appeal of pollinators. It comprises the main colour of the flower with extra fine patterns, indicating a reward focal point such as nectar, nectaries, pollen, stamens and floral guides. Such advertising of floral traits guides visitation by the insects, ensuring precision in pollen gathering and deposition. The study, focused in the Southwest Australian Floristic Region, aimed to spot bee colour patterns that are usual and unusual, missing, accomplished by mimicry of pollen and anthers, and overlapping between mimic-model species in floral mimicry cases.MethodsFloral colour patterns were examined by false colour photography in 55 flower species of multiple highly diverse natural plant communities in south-west Australia. False colour photography is a method to transform a UV photograph and a colour photograph into a false colour photograph based on the trichromatic vision of bees. This method is particularly effective for rapid screening of large numbers of flowers for the presence of fine-scale bee-sensitive structures and surface roughness that are not detectable using standard spectrophotometry.Key ResultsBee- and bird-pollinated flowers showed the expected but also some remarkable and unusual previously undetected floral colour pattern syndromes. Typical colour patterns include cases of pollen and flower mimicry and UV-absorbing targets. Among the atypical floral colour patterns are unusual white and UV-reflecting flowers of bee-pollinated plants, bicoloured floral guides, consistently occurring in Fabaceae spp., and flowers displaying a selective attractiveness to birds only. In the orchid genera (Diuris and Thelymitra) that employ floral mimicry of model species, we revealed a surprising mimicry phenomenon of anthers mimicked in turn by model species.ConclusionThe study demonstrates the applicability of ‘bee view’ colour imaging for deciphering pollinator cues in a biodiverse flora with potential to be applied to other eco regions. The technique provides an exciting opportunity for indexing floral traits on a biome scale to establish pollination drivers of ecological and evolutionary relevance.     

A Matter of Contrast: Yellow Flower Colour Constrains Style Length in Crocus species

Most flowers display distinct colour patterns comprising two different areas. The peripheral large-area component of floral colour patterns attracts flower visitors from some distance and the central small-area component guides flower visitors towards landing sites. Whereas the peripheral colour is largely variable among species, the central colour, produced mostly by anthers and pollen or pollen mimicking floral guides, is predominantly yellow and UV-absorbing. This holds also for yellow flowers that regularly display a UV bull’s eye pattern. Here we show that yellow-flowering Crocus species are a noticeable exception, since yellow-flowering Crocus species–being entirely UV-absorbing–exhibit low colour contrast between yellow reproductive organs and yellow tepals. The elongated yellow or orange-yellow style of Crocus flowers is a stamen-mimicking structure promoting cross-pollination by facilitating flower visitors’ contact with the apical stigma before the flower visitors are touching the anthers. Since Crocus species possess either yellow, violet or white tepals, the colour contrast between the stamen-mimicking style and the tepals varies among species. In this study comprising 106 Crocus species, it was tested whether the style length of Crocus flowers is dependent on the corolla colour. The results show that members of the genus Crocus with yellow tepals have evolved independently up to twelve times in the genus Crocus and that yellow-flowering Crocus species possess shorter styles as compared to violet- and white-flowering ones. The manipulation of flower visitors by anther-mimicking elongated styles in Crocus flowers is discussed.     

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.     

Comparative structure and pollen production of the stamens and pollinator-deceptive staminodes of Commelina coelestis and C. dianthifolia (Commelinaceae)

BACKGROUND AND AIMS: Flowers of Commelina coelestis and C. dianthifolia provide pollen alone as a floral reward, and rely on visual cues to attract pollinators. Three stamen types, all producing pollen, occur in each of these species: two cryptically coloured lateral stamens, a single cryptically coloured central stamen and three bright yellow staminodes that sharply contrast with the blue to purple corolla. The objective was to compare the stamen structure and pollen characteristics of each of the three stamen types, and to test the hypothesis that the staminodes are poor contributors of viable pollen for the siring of seed. The pollination roles of the three stamen types and the breeding systems of both species were also explored. Methods: Light, fluorescence and scanning electron microscopy were utilized to examine stamen morphology and pollen structure and viability. Controlled hand pollinations were used to explore the breeding system of each species. Filament and style lengths were measured to investigate herkogamy and autogamy. KEY RESULTS: Pollen from all stamen morphs is viable, but staminode pollen has significantly lower viability. Pollen polymorphism exists both (a) between the lateral and central stamens and the staminodes, and (b) within each anther. Lateral and central stamens have thicker endothecia with a greater number of secondary cell wall thickenings than the staminodes. CONCLUSIONS: Both species are entomophilous and facultatively autogamous. Lateral stamen pollen is important for cross-pollination, central stamen pollen is utilized by both species as a pollinator reward and for delayed autogamy in C. dianthifolia, and the staminodes mimic, by means of both colour and epidermal features, large amounts of pollen to attract insects to the flowers. Pollen from all three anther morphs is capable of siring seed, although staminode pollen is inferior. The thin staminode endothecium with fewer secondary thickenings retards staminode dehiscence.     

Colored floral organs influence pollinator behavior and pollen transfer in Commelina communis (Commelinaceae)

Visual floral guides such as colored anthers, lines, dots, and UV-absorption patterns on petals are commonly observed in insect-pollinated angiosperms. Floral guides that are known to enhance foraging efficiency of visitors on flowers thus promote return visits (foraging facilitation hypothesis, which predicts that visitors will discriminate against flowers with inferior floral guides). In this study, we experimentally examined the hypothesis that floral guides also prevent pollen-theft behavior by floral visitors (theft prevention hypothesis), which has rarely been tested. Nectarless flowers of Commelina communis have three types of brightly colored floral organs: large blue petals, rewarding yellow anthers, and nonrewarding yellow anthers. Colored floral organs were removed artificially from plants in two natural populations of C. communis. Removal of the nonrewarding yellow anthers diminished hoverings in front of flowers and tended to reduce the number of total floral visitor landings, supporting the foraging facilitation hypothesis. Additionally, removal of the rewarding yellow anther decreased the frequency of legitimate landings on flowers and the legitimate landing-to-total landing ratio, which is consistent with the theft prevention hypothesis. The nonrewarding anthers and the rewarding yellow anthers were shown to play an important role in increasing visitor landings and orienting floral visitors toward a landing point appropriate for pollination, respectively. We also showed that the absence of yellow anthers decreased both pollen dispatch from brown anthers and receipt by stigmas in C. communis. These findings support both the foraging facilitation hypothesis and the theft prevention hypothesis.     

稀有植物小丛红景天花部综合特征与繁育系统

对稀有物种生物学特征及繁育系统的研究将有利于我们对稀有物种的保育。该文通过野外定位观测稀有植物小丛红景天(Rhodiola dumulosa)的花部综合特征,并运用杂交指数、花粉-胚珠比的方法首次对其繁育系统进行初步测定。结果表明:该物种单花花期一般为5~6 d,开花过程中花柱逐渐伸长并向外弯曲,子房开裂并逐渐伸长,花药散粉具有先后顺序,一般外轮对萼花药先散粉,其后1 d左右对瓣花药开始散粉。单花花期依照其形态和散粉时间可分为6个阶段:花蕾期、内轮散粉期、内轮散粉末期、外轮散粉期、外轮散粉末期和凋谢期。而种群花期一般可持续30 d以上,不同海拔观测地点有所不同,海拔2 202 m处的观测地点B开花物候最为滞后。由于其杂交指数不小于4,花粉-胚珠比在700~1 000之间, 根据Dafni(1992)和Cruden(1977)的标准,初步判定该物种的繁育系统属于异交为主,部分自交亲和,传粉过程需要传粉者。     

天仙子的花部特征及延迟自交机制

通过实验观察和野外控制授粉等方法,对天仙子的自交亲和能力和自交传粉机制进行了研究。结果显示:(1)天仙子的花不完全雌性先熟,开花进程中雄蕊伸长是维持其混合交配系统的重要花部特征。(2)野外控制授粉实验证明天仙子的自交亲和性高,具有主动自交能力,主动自交发生的时间集中在晚花期,与花药和柱头接触的时间吻合。(3)在花粉活力和柱头可授期内,花药与柱头的接触能够发生自花授粉,这种依赖花药与柱头接触发生的自花授粉机制属于典型的延迟自交类型。研究表明,天仙子不仅在花结构上首先选择了适于异交的特征,而且还利用雄蕊伸长成功实现自花授粉,通过异交与延迟自交混合的交配系统为该物种提供了灵活的遗传与繁殖保障。     

Is There ‘Anther-Anther Interference’ within a Flower? Evidences from One-by-One Stamen Movement in an Insect-Pollinated Plant

The selective pressure imposed by maximizing male fitness (pollen dispersal) in shaping floral structures is increasingly recognized and emphasized in current plant sciences. To maximize male fitness, many flowers bear a group of stamens with temporally separated anther dehiscence that prolongs presentation of pollen grains. Such an advantage, however, may come with a cost resulting from interference of pollen removal by the dehisced anthers. This interference between dehisced and dehiscing anthers has received little attention and few experimental tests to date. Here, using one-by-one stamen movement in the generalist-pollinated Parnassia palustris, we test this hypothesis by manipulation experiments in two years. Under natural conditions, the five fertile stamens in P. palustris flowers elongate their filaments individually, and anthers dehisce successively one-by-one. More importantly, the anther-dehisced stamen bends out of the floral center by filament deflexion before the next stamen''s anther dehiscence. Experimental manipulations show that flowers with dehisced anther remaining at the floral center experience shorter (1/3–1/2 less) visit durations by pollen-collecting insects (mainly hoverflies and wasps) because these ‘hungry’ insects are discouraged by the scant and non-fresh pollen in the dehisced anther. Furthermore, the dehisced anther blocks the dehiscing anther''s access to floral visitors, resulting in a nearly one third decrease in their contact frequency. As a result, pollen removal of the dehiscing anther decreases dramatically. These results provide the first direct experimental evidence that anther-anther interference is possible in a flower, and that the selection to reduce such interferences can be a strong force in floral evolution. We also propose that some other floral traits, usually interpreted as pollen dispensing mechanisms, may function, at least partially, as mechanisms to promote pollen dispersal by reducing interferences between dehisced and dehiscing anthers.     

Pollination adaptations of group-by-group stamen movement in a meadow plant with temporal floral closure

Floral sexual organ (stamen and pistil) movements are selective adaptations that have different functions in male-female reproduction and the evolution of flowering plants. However, the significance of stamen movements in the spatial–temporal function and separation of male and female organs has not been experimentally determined in species exhibiting floral temporal closure. The current study investigated the role of slow stamen (group-by-group) movement in male-female sexual function, and the effect of stamen movement on pollen removal, male-male and male-female interference, and mating patterns of Geranium pratense, a plant with temporal floral closure. This species uses stamen group-by-group movement and therefore anther-stigma spatial–temporal separation. Spatial separation (two whorls of stamen and pistil length) was shown to be stronger than temporal separation. We found that stamen movements to the center of the flower increase pollen removal, and the most common pollinators visited more frequently and for longer durations during the male floral stage than during the female floral stage. Petal movements increased both self-pollen deposition rate and sexual interference in G. pratense. The fruit and seed set of naturally and outcrossed pollinated flowers were more prolific than those of self-pollinated flowers. Group-by-group stamen movement, dehiscence of stamens, pistil movement, and male-female spatial–temporal functional separation of G. pratense before floral temporal closure may prevent male-female and stamen-stamen interference and pollen discounting, and may increase pollen removal and cross-pollination.     

濒危植物长柄双花木的花部综合特征与繁育系统

 通过野外观察,运用杂交指数、花粉-胚珠比、人工授粉和套袋实验及等位酶电泳等方法,对长柄双花木(Disanthus cercidifolius Maxim. var. longipes H. T. Chang)自然种群和人工种群的开花状态、繁育系统进行了研究。结果如下：该种单花花期一般6～7 d,开花过程中柱头始终高于花药的位置,花药散粉具有先后顺序,一般2花药先散粉,其余3花药滞后1～2 d。单花花期依其形态和散粉时间可分为5个时期：即散粉前期、散粉初期、散粉盛期、凋谢期。种群开花一般历时49～55 d,但不同地点、年份之间有所差异,推测开花持续时间不同主要是环境条件所致。由于其杂交指数大于4,花粉-胚珠比等于1 250,结合人工套袋和授粉实验以及等位酶电泳结果可以确定该种的繁育系统属于异交为主,部分自交亲和,传粉过程需要传粉者。花粉竞争可能是导致该种濒危的主要的生殖生物学原因。     

Visual detection of diminutive floral guides in the bumblebee <Emphasis Type="Italic">Bombus terrestris</Emphasis> and in the honeybee <Emphasis Type="Italic">Apis mellifera</Emphasis>

Many flowers display colour patterns comprising a large peripheral colour area that serves to attract flower visitors from some distance, and a small central, contrastingly coloured area made up by stamens or floral guides. In this study, we scaled down the size of floral guides to detect the minimal size bumblebees (Bombus terrestris) and honeybees (Apis mellifera) require for guidance. We analyzed the approach and the precise contact of the antennal tips with the floral guide of artificial flowers which precedes landing and inspection. Both bumblebees and honeybees were able to make antennal contact with circular floral guides which were 2 mm in diameter; bumblebees performed better than honeybees and antennated also at floral guides smaller than 2 mm. In discrimination experiments with bumblebees, a minimum floral guide size of 2 mm was required for discrimination between artificial flowers with and without floral guides. With increasing experience bumblebees targeted close to the site of reward instead of making antennal contact with the floral guide, whereas honeybees did not alter their initial behaviour with growing experience. Bumblebees and honeybees spontaneously target diminutive floral guides to achieve physical contact with flowers by means of their antennae which helps them to inspect flowers.     

Pollination biology and sexual differentiation ofOsyris alba (Santalaceae) in the Mediterranean region

Osyris alba L. is a widespread dioecious hemiparasitic shrub of S Europe, N Africa, and SW Asia. Male inflorescences are multiflowered whereas each female inflorescence is reduced to a single flower with persistent enlarged bracts. Pollination is a prerequisite for fruit and seed development and wind is unlikely to be an effective means of pollen spread. In southern Italy pollen is transported by small unspecialized flies and beetles. Both male and female flowers produce an indistinguishable sweet odour. Male flowers are produced in large numbers and over a larger period than the females and provide pollen, nectar, and staminal hairs as rewards for pollinators. The presence and function of staminal hairs with tip cells inOsyris alba has been reported for the first time. Female flowers are rewardless, producing neither mature pollen, nectar nor staminal hairs, but possess three modified yellow indehiscent anthers containing no viable pollen which may provide a strong visual feeding stimulus for pollinators. It is suggested that pollinators are attracted by deceit to female flowers by mimicry of the males and the floral mimicry is, therefore, intraspecific and intersexual. The floral characteristics and flowering phenology of male and female plants are consistent with this kind of mimicry. The female flower possesses a tricarpellary ovary with three ovules of which only one develops. The single seed, containing a small embryo and a large, rich endosperm, is borne in a red fleshy bird-dispersed fruit. The reduction in seed number per flower to one highly nutrient-invested seed, together with a reduction of the multiflowered inflorescence to a solitary flower and the sequential production of ripe fruits over an extended fruiting season, suggest that the female function is markedly resource-limited. It is suggested that, although all the reproductive characteristics present inOsyris alba, as well as hemiparasitism, had probably evolved before the end of the tropical Tertiary, they are of adaptive advantage in the nutrient and water-limited environment of the Mediterranean maquis.     

How to look like a mallow: evidence of floral mimicry between Turneraceae and Malvaceae

Abundant, many-flowered plants represent reliable and rich food sources for animal pollinators, and may even sustain guilds of specialized pollinators. Contrastingly, rare plants need alternative strategies to ensure pollinators' visitation and faithfulness. Flower mimicry, i.e. the sharing of a similar flower colour and display pattern by different plant species, is a means by which a rare species can exploit a successful model and increase its pollination services. The relationship between two or more rewarding flower mimic species, or Müllerian mimicry, has been proposed as mutualistic, in contrast to the unilaterally beneficial Batesian floral mimicry. In this work, we show that two different geographical colour phenotypes of Turnera sidoides ssp. pinnatifida resemble co-flowering Malvaceae in colour as seen by bees' eyes, and that these pollinators do not distinguish between them when approaching flowers in choice tests. Main pollinators of T. sidoides are bees specialized for collecting pollen in Malvaceae. We demonstrate that the similarity between at least one of the geographical colour phenotypes of T. sidoides and co-flowering Malvaceae is adaptive, since the former obtains more pollination services when growing together with its model than when growing alone. Instead of the convergent evolution pattern attributed to Müllerian mimicry, our data rather suggest an advergent evolution pattern, because only T. sidoides seems to have evolved to be more similar to its malvaceous models.     

Relative impact of mate versus pollinator availability on pollen limitation and outcrossing rates in a mass‐flowering species

Plant mating systems are driven by several pre‐pollination factors, including pollinator availability, mate availability and reproductive traits. We investigated the relative contributions of these factors to pollination and to realized outcrossing rates in the patchily distributed mass‐flowering shrub Rhododendron ferrugineum. We jointly monitored pollen limitation (comparing seed set from intact and pollen‐supplemented flowers), reproductive traits (herkogamy, flower size and autofertility) and mating patterns (progeny array analysis) in 28 natural patches varying in the level of pollinator availability (flower visitation rates) and of mate availability (patch floral display estimated as the total number of inflorescences per patch). Our results showed that patch floral display was the strongest determinant of pollination and of the realized outcrossing rates in this mass‐flowering species. We found an increase in pollen limitation and in outcrossing rates with increasing patch floral display. Reproductive traits were not significantly related to patch floral display, while autofertility was negatively correlated to outcrossing rates. These findings suggest that mate limitation, arising from high flower visitation rates in small plant patches, resulted in low pollen limitation and high selfing rates, while pollinator limitation, arising from low flower visitation rates in large plant patches, resulted in higher pollen limitation and outcrossing rates. Pollinator‐mediated selfing and geitonogamy likely alleviates pollen limitation in the case of reduced mate availability, while reduced pollinator availability (intraspecific competition for pollinator services) may result in the maintenance of high outcrossing rates despite reduced seed production.     

Evidence for reductions in floral attractants with increased selfing rates in two heterandrous species

Although theoretical models predict low allocation to attractive structures with increased selfing in animal-pollinated plants, empirical measurement of the reproductive costs and benefits is complicated. Here, floral sex allocation was compared in two nectarless heterandrous species with different mating systems: Monochoria korsakowii (Pontederiaceae), which has moderate outcrossing rates, and Monochoria vaginalis, a predominant selfer. In both species, mirror-image flowers have one large dark-purple anther and five small yellow anthers. Experimental evidence is provided for functional differences between the two sets of anthers using data on pollinator visitation, pollen removal and deposition, and seed set after hand pollinations. Flower manipulations in bee-pollinated M. korsakowii demonstrated different functions of the two sets of anthers: the yellow (feeding) anthers function to attract pollinators, but have similar pollen performance to the purple (pollinating) anthers. Furthermore, a disproportional reduction in pollen production of the feeding anthers in the selfing species was found. This differential allocation between feeding and pollinating anthers in heterandrous species has not been recognized before. The finding of reduced allocation to attractive structures with an increase in the rate of self-fertilization supports the theory of sex allocation.     

Reduced visitation to buzz‐pollinated Cyanella hyacinthoides in the presence of other pollen sources in the hyperdiverse Cape Floristic Region

Many plant species have floral morphologies that restrict access to floral resources, such as pollen or nectar, and only a subset of floral visitors can perform the handling behaviors required to extract restricted resources. Due to the time and energy required to extract resources from morphologically complex flowers, these plant species potentially compete for pollinators with co‐flowering plants that have more easily accessible resources. A widespread floral mechanism restricting access to pollen is the presence of tubular anthers that open through small pores or slits (poricidal anthers). Some bees have evolved the capacity to remove pollen from poricidal anthers using vibrations, giving rise to the phenomenon of buzz‐pollination. These bee vibrations that are produced for pollen extraction are presumably energetically costly, and to date, few studies have investigated whether buzz‐pollinated flowers may be at a disadvantage when competing for pollinators’ attention with plant species that present unrestricted pollen resources. Here, we studied Cyanella hyacinthoides (Tecophilaeaceae), a geophyte with poricidal anthers in the hyperdiverse Cape Floristic Region of South Africa, to assess how the composition and relative abundance of flowers with easily accessible pollen affect bee visitation to a buzz‐pollinated plant. We found that the number of pollinator species of C. hyacinthoides was not influenced by community composition. However, visitation rates to C. hyacinthoides were reduced when the relative abundances of flowers with more accessible resources were high. Visitation rates were strongly associated with petal color, showing that flower color is important in mediating these interactions. We conclude that buzz‐pollinated plants might be at a competitive disadvantage when many easily accessible pollen sources are available, particularly when competitor species share its floral signals.     

Insect colour preference compared to flower colours in the Australian Alps

An apparent predominance of plant taxa with pale flowers in the alpine floras of Australia and New Zealand may be due to the prevalence of insects, such as flies, that prefer pale colours and the absence of other types of potential pollinators that are attracted to bright colours such as social bees and birds. In this study, the diversity of flower colours, and the preference of insects for different colours were examined for the largest contiguous alpine area in Australia, around Mt Kosciuszko. Out of an alpine flora of 204 taxa, 127 species were found to have large showy flowers. The most common flower colour among these taxa was white (53.5%), then yellow (21.3%), followed by pink (6.3%), and cream (6.3%). Only a handful of taxa had red, blue, brown, green, orange or purple flowers. When the colour preference of insects was tested using five different coloured traps (white, yellow, orange, red and purple), the most successful traps were white then yellow, with these two colours accounting for 66% of all individual insects collected. Diptera were the most common insects caught (576 insects greater than 4 mm in length, 31 morphotaxa) showing an apparent preference for white and yellow coloured traps over others. Therefore, the results add some support to the proposition that the 'white' flora of the Australian Alps may be associated with the colour preference of flies, which have previously been found to be the most common type of pollinators in the Kosciuszko alpine zone.     

Factors affecting pollinator movement and plant fitness in a specialized pollination system

The rate of pollen exchange within and among flowers may depend on pollinator attraction traits such as floral display size and flowering plant density. Variations in these traits may influence pollinator movements, pollen receipt, and seed number. To assess how floral display size and flowering plant density affect parameters of pollinator visitation rate, pollen receipt per flower, seed number per fruit and the between-plant pollinator movements, we studied the self-incompatible plant, Nierembergia linariifolia. Per-flower pollinator visitation rate and bout length increased linearly with increasing floral display size. Pollen receipt per flower increased linearly with increasing flowering plant density. For seed number per fruit, a polynomial model describing an increased seed number per fruit at low density and a decreased seed number per fruit at high density provided a significant fit. Per-flower pollinator visitation rate was not associated with pollen receipt per flower and seed number per fruit. Bees visited plants located near to the center of the population more frequently than plants located at the periphery. Increases in both floral display size and flowering plant density led to an increased chance of a plant being chosen as the center of the pollinator foraging area. These results suggest that even though large floral displays and high flowering plant density are traits that attract more pollinators, they may also reduce potential mate diversity by restricting pollen movement to conspecific mates that are closely located.     

Bumblebees require visual pollen stimuli to initiate and multimodal stimuli to complete a full behavioral sequence in close‐range flower orientation

Flower visits are complex encounters, in which animals are attracted by floral signals, guided toward the site of the first physical contact with a flower, land, and finally take up floral rewards. At close range, signals of stamens and pollen play an important role to facilitate flower handling in bees, yet the pollen stimuli eliciting behavioral responses are poorly known. In this study, we test the response of flower‐naive bumblebees (Bombus terrestris) toward single and multimodal pollen stimuli as compared to natural dandelion pollen. As artificial pollen stimuli, we used the yellow flavonoid pigment quercetin, the scent compound eugenol, the amino acid proline, the monosaccharide glucose, and the texture of pollen‐grain‐sized glass pellets as a tactile stimulus. Three test stimuli, dandelion pollen, one out of various uni‐ and multimodal stimulus combinations, and a solvent control were presented simultaneously to individual bumblebees, whose response was recorded. The results indicate that bumblebees respond in an irreversible sequence of behavioral reactions. Bumblebees approached the visual stimulus quercetin as often as natural dandelion pollen. An additional olfactory stimulus resulted in slightly more frequent landings. The multimodal stimulus combinations including visual, olfactory, gustatory, and tactile stimuli elicited approaches, antennal contacts, and landings as often as natural pollen. Subsequent reactions like proboscis extension, mandible biting, and buzzing were more often but not regularly observed at dandelion pollen. Our study shows that visual signals of pollen are sufficient to trigger initial responses of bumblebees, whereas multimodal pollen stimuli elicit full behavioral response as compared to natural pollen. Our results suggest a major role of pollen cues for the attraction of bees toward flowers and also explain, why many floral guides mimic the visual signals of pollen and anthers, that is, the yellow and UV‐absorbing color, to direct bumblebees toward the site where they access the floral rewards.