Flowers bear the function of filters supporting the attraction of pollinators as well as the deterrence of floral antagonists. The effect of epidermal cell shape on the visual display and tactile properties of flowers has been evaluated only recently. In this study we quantitatively measured epidermal cell shape, gloss and spectral reflectance of flowers pollinated by either bees or birds testing three hypotheses: The first two hypotheses imply that bee-pollinated flowers might benefit from rough surfaces on visually-active parts produced by conical epidermal cells, as they may enhance the colour signal of flowers as well as the grip on flowers for bees. In contrast, bird-pollinated flowers might benefit from flat surfaces produced by flat epidermal cells, by avoiding frequent visitation from non-pollinating bees due to a reduced colour signal, as birds do not rely on specific colour parameters while foraging. Moreover, flat petal surfaces in bird-pollinated flowers may hamper grip for bees that do not touch anthers and stigmas while consuming nectar and thus, are considered as nectar thieves. Beside this, the third hypothesis implies that those flower parts which are vulnerable to nectar robbing of bee- as well as bird-pollinated flowers benefit from flat epidermal cells, hampering grip for nectar robbing bees. Our comparative data show in fact that conical epidermal cells are restricted to visually-active parts of bee-pollinated flowers, whereas robbing-sensitive parts of bee-pollinated as well as the entire floral surface of bird-pollinated flowers possess on average flat epidermal cells. However, direct correlations between epidermal cell shape and colour parameters have not been found. Our results together with published experimental studies show that epidermal cell shape as a largely neglected flower trait might act as an important feature in pollinator attraction and avoidance of antagonists, and thus may contribute to the partitioning of flower-visitors.
It is accepted that the papilionaceous corolla of the Fabaceae evolved under the selective pressure of bee pollinators. Morphology and function of different parts of Coronilla emerus L. flowers were related to their role in the pollination mechanism. The corolla has a vexillum with red nectar lines, a keel hiding stamens and pistil, and two wing petals fasten to the keel with two notched folds. Pollinators land on the complex of keel and wings, trigger the protrusion of pollen and finally of the stigma from the keel tip. Data on pollen viability and stigma receptivity prove that flowers are proterandrous. The results of hand-pollination experiments confirmed that insects are fundamental to set seed. Interaction with pollinators allows not only the transport of pollen but also the rupture of the stigmatic cuticle, necessary to achieve both allogamy and autogamy. Field observations showed that Hymenoptera, Lepidoptera, and Diptera visited the flowers. Only some of the Hymenoptera landed on the flowers from the front and elicited pollination mechanisms. Most of the insects sucked the nectar from the back without any pollen transfer. Finally, morphological and functional characteristics of C. emerus flowers are discussed in terms of floral larceny and reduction in pollination efficiency.
Genetic crossing is an essential tool in both forward and reverse genetic approaches to understand the biological functions of genes. For Medicago truncatula (barrel medic) various crossing techniques have been used which differ in the methods used to dissect the female parent’s unopened flower bud to remove immature anthers for prevention of self-pollination. Previously described methods including front, side or back incision methods may damage the flower bud, impeding successful fertilization and/or seed development because they may allow pollen to dislodge and floral organs to desiccate after crossing, all of which diminish the success rates of crossing.
We report the keel petal incision method for genetic crossing in M. truncatula ecotype R108 and demonstrate successful crosses with two other M. truncatula ecotypes, A17 and A20. In the method presented here, an incision is made along the central line of the keel petal from the bottom 1/3rd of the female parent’s flower bud to its distal end. This allows easy removal of anthers from the flower bud and access for cross-pollination. After pollination, the stigma and the deposited pollen from the male donor are covered by the keel petal, wing petals and standard petal, forming a natural pouch. The pouch prevents dislodging of deposited pollen from the stigma and protects the internal floral organs from drying out, without using cling-film or water-containing chambers to maintain a humid environment. The keel petal incision method showed an approximate 80% success rate in the M. truncatula R108 ecotype and also in other ecotypes including Jemalong A17 and A20.
Our keel petal incision protocol shows marked improvement over existing methods with respect to the ease of crossing and the percentage of successful crosses. Developed for the M. truncatula R108 ecotype, the protocol has been demonstrated with A17 and A20 ecotypes and is expected to work with other ecotypes. Investigators of varying experience have achieved genetic crosses in M. truncatula using this method.
Legume; Genetic crossing; Barrel medic; Medicago truncatula; Artificial hybridization; Keel petal
An adaptive role of corolla shape has been often asserted without an empirical demonstration of how natural selection acts on this trait. In generalist plants, in which flowers are visited by diverse pollinator fauna that commonly vary spatially, detecting pollinator-mediated selection on corolla shape is even more difficult. In this study, we explore the mechanisms promoting selection on corolla shape in the generalist crucifer Erysimum mediohispanicum Polatschek (Brassicaceae). We found that the main pollinators of E. mediohispanicum (large bees, small bees and bee flies) discriminate between different corolla shapes when offered artificial flowers without reward. Importantly, different pollinators prefer different shapes: bees prefer flowers with narrow petals, whereas bee flies prefer flowers with rounded overlapping petals. We also found that flowers with narrow petals (those preferred by bees) produce both more pollen and nectar than those with rounded petals. Finally, different plant populations were visited by different faunas. As a result, we found spatial variation in the selection acting on corolla shape. Selection favoured flowers with narrow petals in the populations where large or small bees are the most abundant pollinator groups. Our study suggests that pollinators, by preferring flowers with high reward, exert strong selection on the E. mediohispanicum corolla shape. The geographical variation in the pollinator-mediated selection on E. mediohispanicum corolla shape suggests that phenotypic evolution and diversification can occur in this complex floral trait even without specialization.
corolla shape evolution; pollinator preference; spatial variation; geometric morphometrics; nectar; pollen
Background and Aims
Pollinators together with other biotic and some abiotic factors can select for floral traits. However, variation in pollinator abundance over time and space can weaken such selection. In the present study, the variation in pollinator abundance over time and space was examined in populations of the Rocky Mountain columbine. The variation in three floral traits is described and correlations between pollinator type, functional pollinator groups or altitude and floral traits are examined.
Pollinator observations took place in six Aquilegia coerulea populations over 1–4 years and spur length, flower colour and sepal length were measured in 12 populations. Pollinator abundance, measured as visits per flower per hour, was compared among populations and years. Pollinators were grouped into two functional groups: pollen or nectar collectors. The following associations were examined: annual presence of hawkmoths and whiter flowers with longer spurs; the presence of Sphinx vashti and longer spurs; and higher altitudes and whiter flowers. The study looked at whether an increase in the proportion of hawkmoths in a population was associated with whiter and larger flowers with longer spurs.
The abundance of different pollinator groups varied over time and space. Floral traits varied among populations. Higher altitude was correlated with bluer flowers. Whiter flowers were associated with the annual presence of hawkmoths. Populations visited by Sphinx vashti had longer spurs than populations visited only by Hyles lineata. Populations with greater percentage of nectar-collecting pollinators did not have whiter, larger flowers with longer spurs.
Despite the large variation in pollinator abundance over time and space, one species of bumble-bee or hawkmoth tended to predominate in each population each year. Future studies of Aquilegia coerulea should examine the specific influences of pollinators and the environment on flower colour and of hawkmoth species on spur length.
Aquilegia coerulea; columbine; pollinator abundance; bumble-bee; hawkmoth, flower colour; spur length; functional pollinator group; altitude; floral trait
Distinct floral pollination syndromes have emerged multiple times during the diversification of flowering plants. For example, in western North America, a hummingbird pollination syndrome has evolved more than 100 times, generally from within insect-pollinated lineages. The hummingbird syndrome is characterized by a suite of floral traits that attracts and facilitates pollen movement by hummingbirds, while at the same time discourages bee visitation. These floral traits generally include large nectar volume, red flower colour, elongated and narrow corolla tubes and reproductive organs that are exerted from the corolla. A handful of studies have examined the genetic architecture of hummingbird pollination syndrome evolution. These studies find that mutations of relatively large effect often explain increased nectar volume and transition to red flower colour. In addition, they suggest that adaptive suites of floral traits may often exhibit a high degree of genetic linkage, which could facilitate their fixation during pollination syndrome evolution. Here, we explore these emerging generalities by investigating the genetic basis of floral pollination syndrome divergence between two related Penstemon species with different pollination syndromes—bee-pollinated P. neomexicanus and closely related hummingbird-pollinated P. barbatus. In an F2 mapping population derived from a cross between these two species, we characterized the effect size of genetic loci underlying floral trait divergence associated with the transition to bird pollination, as well as correlation structure of floral trait variation. We find the effect sizes of quantitative trait loci for adaptive floral traits are in line with patterns observed in previous studies, and find strong evidence that suites of floral traits are genetically linked. This linkage may be due to genetic proximity or pleiotropic effects of single causative loci. Interestingly, our data suggest that the evolution of floral traits critical for hummingbird pollination was not constrained by negative pleiotropy at loci that show co-localization for multiple traits.
Penstemon; pollination syndrome; QTL; genetics of adaptation; phenotypic correlation
The sequential separation of male and female function in flowers of dichogamous species allows for the evolution of differing morphologies that maximize fitness through seed siring and seed set. We examined staminate- and pistillate-phase flowers of protandrous Saponaria officinalis for dimorphism in floral traits and their effects on pollinator attraction and seed set. Pistillate-phase flowers have larger petals, greater mass, and are pinker in color, but due to a shape change, pistillate-phase flowers have smaller corolla diameters than staminate-phase flowers. There was no difference in nectar volume or sugar content one day after anthesis, and minimal evidence for UV nectar guide patterns in staminate- and pistillate-phase flowers. When presented with choice arrays, pollinators discriminated against pistillate-phase flowers based on their pink color. Finally, in an experimental garden, in 2012 there was a negative correlation between seed set of an open-pollinated, emasculated flower and pinkness (as measured by reflectance spectrometry) of a pistillate-phase flower on the same plant in plots covered with shade cloth. In 2013, clones of genotypes chosen from the 2012 plants that produced pinker flowers had lower seed set than those from genotypes with paler flowers. Lower seed set of pink genotypes was found in open-pollinated and hand-pollinated flowers, indicating the lower seed set might be due to other differences between pink and pale genotypes in addition to pollinator discrimination against pink flowers. In conclusion, staminate- and pistillate-phase flowers of S. officinalis are dimorphic in shape and color. Pollinators discriminate among flowers based on these differences, and individuals whose pistillate-phase flowers are most different in color from their staminate-phase flowers make fewer seeds. We suggest morphological studies of the two sex phases in dichogamous, hermaphroditic species can contribute to understanding the evolution of sexual dimorphism in plants without the confounding effects of genetic differences between separate male and female individuals.
Iridescence is a form of structural coloration, produced by a range of structures, in which hue is dependent on viewing angle [1, 2, 3, 4]. One of these structures, the diffraction grating, is found both in animals (for example, beetles ) and in plants (on the petals of some animal pollinated flowers ). The behavioral impacts of floral iridescence and its potential ecological significance are unknown [6, 7, 8, 9]. Animal-pollinated flowers are described as “sensory billboards” , with many floral features contributing to a conspicuous display that filters prospective pollinators. Yet floral iridescence is more subtle to the human eye than that of many animal displays because the floral diffraction grating is not perfectly regular [5, 6, 7, 8, 9]. This presents a puzzle: if the function of petals is to attract pollinators, then flowers might be expected to optimize iridescence to increase showiness. On the other hand, pollinators memorize floral colors as consistent advertisements of reward quality, and iridescence might corrupt flower color identity. Here we tested the trade-off between flower detectability and recognition, requiring bumblebees (Bombus terrestris) to identify artificial flowers that varied in pigmentation and degree of iridescence. We find that iridescence does increase target detectability but that “perfect” iridescence (produced by an artificial diffraction grating) corrupts target identity and bees make many mistakes. However, “imperfect” floral iridescence does not lead to mistaken target identity, while still benefitting flower detectability. We hypothesize that similar trade-offs might be found in the many naturally “imperfect” iridescence-producing structures found in animal-animal, as well as other plant-animal, interactions.
•Iridescence can increase object detectability•Iridescence can increase the disruption of accurate color identification•Detectability and disruption are influenced by variation in iridescent structures•Floral iridescence is an optimal trade-off between detectability and identification
Some animal-pollinated flowers are iridescent, but this iridescence is subtle when compared to bolder animal iridescence. Whitney et al. show that iridescence could make flowers more detectable to bees. However, subtlety may be beneficial to flowers as bolder iridescence also disrupts the ability of bees to identify colored targets.
Here, we report on the results of an experimental study that assessed the visitation frequency of wild bees to conspecific flowers with different sized floral guides. UV absorbent floral guides are ubiquitous in Angiosperms, yet surprisingly little is known about conspecific variation in these guides and very few studies have evaluated pollinator response to UV guide manipulation. This is true despite our rich understanding about learning and color preferences in bees. Historical dogma indicates that flower color serves as an important long-range visual signal allowing pollinators to detect the flowers, while floral guides function as close-range signals that direct pollinators to a reward. We initiated the work presented here by first assessing the population level variation in UV absorbent floral guides for conspecific flowers. We assessed two species, Rudbeckia hirta and R. fulgida. We then used several petal cut-and-paste experiments to test whether UV floral guides can also function to attract visitors. We manipulated floral guide size and evaluated visitation frequency. In all experiments, pollinator visitation rates were clearly associated with floral guide size. Diminished floral guides recruited relatively few insect visitors. Exaggerated floral guides recruited more visitors than smaller or average sized guides. Thus, UV floral guides play an important role in pollinator recruitment and in determining the relative attractiveness of conspecific flower heads. Consideration of floral guides is therefore important when evaluating the overall conspicuousness of flower heads relative to background coloration. This work raises the issue of whether floral guides serve as honest indicators of reward, since guide size varies in nature for conspecific flowers at the same developmental stage and since preferences for larger guides were found. To our knowledge, these are the first cut-and-paste experiments conducted to examine whether UV absorbent floral guides affect visitation rates and pollinator preference.
Bee; Rudbeckia; Flower; Pollination; Opsin; Vision; Pollinator
Background and Aims
Studies of the effects of pollination on floral scent and bee visitation remain rare, particularly in agricultural crops. To fill this gap, the hypothesis that bee visitation to flowers decreases after pollination through reduced floral volatile emissions in highbush blueberries, Vaccinium corymbosum, was tested. Other sources of variation in floral emissions and the role of floral volatiles in bee attraction were also examined.
Pollinator visitation to blueberry flowers was manipulated by bagging all flowers within a bush (pollinator excluded) or leaving them unbagged (open pollinated), and then the effect on floral volatile emissions and future bee visitation were measured. Floral volatiles were also measured from different blueberry cultivars, times of the day and flower parts, and a study was conducted to test the attraction of bees to floral volatiles.
Open-pollinated blueberry flowers had 32 % lower volatile emissions than pollinator-excluded flowers. In particular, cinnamyl alcohol, a major component of the floral blend that is emitted exclusively from petals, was emitted in lower quantities from open-pollinated flowers. Although, no differences in cinnamyl alcohol emissions were detected among three blueberry cultivars or at different times of day, some components of the blueberry floral blend were emitted in higher amounts from certain cultivars and at mid-day. Field observations showed that more bees visited bushes with pollinator-excluded flowers. Also, more honey bees were caught in traps baited with a synthetic blueberry floral blend than in unbaited traps.
Greater volatile emissions may help guide bees to unpollinated flowers, and thus increase plant fitness and bee energetic return when foraging in blueberries. Furthermore, the variation in volatile emissions from blueberry flowers depending on pollination status, plant cultivar and time of day suggests an adaptive role of floral signals in increasing pollination of flowers.
Vaccinium corymbosum; honey bees; bumble bees; volatile organic compounds; diurnal rhythm; nectar production; site of emission
Abundance and visitation of pollinator assemblages tend to decrease with altitude, leading to an increase in pollen limitation. Thus increased competition for pollinators may generate stronger selection on attractive traits of flowers at high elevations and cause floral adaptive evolution. Few studies have related geographically variable selection from pollinators and intraspecific floral differentiation. We investigated the variation of Trollius ranunculoides flowers and its pollinators along an altitudinal gradient on the eastern Qinghai-Tibet Plateau, and measured phenotypic selection by pollinators on floral traits across populations. The results showed significant decline of visitation rate of bees along altitudinal gradients, while flies was unchanged. When fitness is estimated by the visitation rate rather than the seed number per plant, phenotypic selection on the sepal length and width shows a significant correlation between the selection strength and the altitude, with stronger selection at higher altitudes. However, significant decreases in the sepal length and width of T. ranunculoides along the altitudinal gradient did not correspond to stronger selection of pollinators. In contrast to the pollinator visitation, mean annual precipitation negatively affected the sepal length and width, and contributed more to geographical variation in measured floral traits than the visitation rate of pollinators. Therefore, the sepal size may have been influenced by conflicting selection pressures from biotic and abiotic selective agents. This study supports the hypothesis that lower pollinator availability at high altitude can intensify selection on flower attractive traits, but abiotic selection is preventing a response to selection from pollinators.
Background and Aims
Convergent floral traits hypothesized as attracting particular pollinators are known as pollination syndromes. Floral diversity suggests that the Australian epacrid flora may be adapted to pollinator type. Currently there are empirical data on the pollination systems for 87 species (approx. 15 % of Australian epacrids). This provides an opportunity to test for pollination syndromes and their important morphological traits in an iconic element of the Australian flora.
Data on epacrid–pollinator relationships were obtained from published literature and field observation. A multivariate approach was used to test whether epacrid floral attributes related to pollinator profiles. Statistical classification was then used to rank floral attributes according to their predictive value. Data sets excluding mixed pollination systems were used to test the predictive power of statistical classification to identify pollination models.
Floral attributes are correlated with bird, fly and bee pollination. Using floral attributes identified as correlating with pollinator type, bird pollination is classified with 86 % accuracy, red flowers being the most important predictor. Fly and bee pollination are classified with 78 and 69 % accuracy, but have a lack of individually important floral predictors. Excluding mixed pollination systems improved the accuracy of the prediction of both bee and fly pollination systems.
Although most epacrids have generalized pollination systems, a correlation between bird pollination and red, long-tubed epacrids is found. Statistical classification highlights the relative importance of each floral attribute in relation to pollinator type and proves useful in classifying epacrids to bird, fly and bee pollination systems.
Epacridaceae (epacrids); Ericaceae; multivariate analysis; plant–pollinator interactions; pollination syndromes; Random Forests; statistical classification; Styphelioideae
•Background and Aims Animal-pollinated angiosperms have evolved a variety of signalling mechanisms to attract pollinators. Floral scent is a key component of pollinator attraction, and its chemistry modulates both pollinator behaviour and the formation of plant–pollinator networks. The neotropical orchid genus Gongora exhibits specialized pollinator associations with male orchid bees (Euglossini). Male bees visit orchid flowers to collect volatile chemical compounds that they store in hind-leg pouches to use subsequently during courtship display. Hence, Gongora floral scent compounds simultaneously serve as signalling molecules and pollinator rewards. Furthermore, because floral scent acts as the predominant reproductive isolating barrier among lineages, it has been hypothesized that chemical traits are highly species specific. A comparative analysis of intra- and inter-specific variation of floral scent chemistry was conducted to investigate the evolutionary patterns across the genus.
•Methods Gas chromatography–mass spectrometry (GC-MS) was used to analyse the floral scent of 78 individuals belonging to 28 different species of Gongora from two of the three major lineages sampled across the neotropical region. Multidimensional scaling and indicator value analyses were implemented to investigate the patterns of chemical diversity within and among taxonomic groups at various geographic scales. Additionally, pollinator observations were conducted on a sympatric community of Gongora orchids exhibiting distinct floral scent phenotypes.
•Key Results A total of 83 floral volatiles, mainly terpenes and aromatic compounds, were detected. Many of the identified compounds are common across diverse angiosperm families (e.g. cineole, eugenol, β-ocimene, β-pinene and terpinen-4-ol), while others are relatively rare outside euglossine bee-pollinated orchid lineages. Additionally, 29 volatiles were identified that are known to attract and elicit collection behaviour in male bees. Floral scent traits were less variable within species than between species, and the analysis revealed exceptional levels of cryptic diversity. Gongora species were divided into 15 fragrance groups based on shared compounds. Fragrance groups indicate that floral scent variation is not predicted by taxonomic rank or biogeographic region.
Gongora orchids emit a diverse array of scent molecules that are largely species specific, and closely related taxa exhibit qualitatively and quantitatively divergent chemical profiles. It is shown that within a community, Gongora scent chemotypes are correlated with near non-overlapping bee pollinator assemblies. The results lend support to the hypothesis that floral scent traits regulate the architecture of bee pollinator associations. Thus, Gongora provides unique opportunities to examine the interplay between floral traits and pollinator specialization in plant–pollinator mutualisms.
Euglossine bees; floral scent; orchid genus Gongora; plant–pollinator mutualism; Euglossa
Background and Aims
The extreme complexity of asclepiad flowers (Asclepiadoideae–Apocynaceae) has generated particular interest in the pollination biology of this group of plants especially in the mechanisms involved in the pollination processes. This study compares two South American species, Morrenia odorata and Morrenia brachystephana, with respect to morphology and anatomy of flower structures, dynamic aspects of the pollination mechanism, diversity of visitors and effectiveness of pollinators.
Floral structure was studied with fresh and fixed flowers following classical techniques. The pollination mechanism was studied by visiting fresh flowers in the laboratory with artificial pollinator body parts created with an eyelash. Morphometric and nectar measurements were also taken. Pollen transfer efficiency in the flowers was calculated by recording the frequency of removed and inserted pollinia. Visitor activity was recorded in the field, and floral visitors were captured for subsequent analysis of pollen loads. Finally, pollinator effectiveness was calculated with an index.
The detailed structure of the flowers revealed a complex system of guide rails and chambers precisely arranged in order to achieve effective pollinaria transport. Morrenia odorata is functionally specialized for wasp pollination, and M. brachystephana for wasp and bee pollination. Pollinators transport chains of pollinaria adhered to their mouthparts.
Morrenia odorata and M. brachystephana present differences in the morphology and size of their corona, gynostegium and pollinaria, which explain the differences in details of the functioning of the general pollination mechanism. Pollination is performed by different groups of highly effective pollinators. Morrenia species are specialized for pollination mainly by several species of wasps, a specialized pollination which has been poorly studied. In particular, pompilid wasps are reported as important pollinators in other regions outside South Africa. A putative new function of nectar in asclepiads is presented, as it would be contributing to the pollination mechanism.
Morrenia odorata; Morrenia brachystephana; asclepiads; functional morphology; pollination mechanism; wasps; pollinator effectiveness
Background and Aims
Dimorphism among floral traits can evolve through variation in selection intensity between female and male performance, especially when sex functions are separated between flowers on a plant (monoecy), or between individuals (dioecy). In animal-pollinated species, male floral traits are predicted to be larger because competition for pollinators should favour larger displays. Floral dimorphism may be greater in dioecious than monoecious populations because of trade-offs between female and male function and opportunities for selfing in hermaphrodites.
These predictions were tested by surveying flower size, total flowers per inflorescence and daily display size in the insect-pollinated Sagittaria latifolia (Alismataceae). This species is useful for comparative analysis because populations are mostly either monoecious or dioecious. We examined floral dimorphism in 13 monoecious and 16 dioecious populations in eastern North America.
Male flowers were significantly larger than female flowers in monoecious and dioecious populations, but there was no evidence for greater flower size dimorphism in dioecious populations despite their larger flower sizes overall. Although inflorescences in both dioecious and monoecious populations produced more male flowers, daily floral displays were significantly larger for female than male function due to more synchronous female flower opening. Daily floral display dimorphism was significantly greater in dioecious populations, due to greater female daily floral displays. There was a positive relationship between mean flower size and total flowers per inflorescence for both sexes in dioecious populations, but no relationship for either sex function in monoecious populations. Flower size dimorphism was positively correlated with the frequencies of females in dioecious populations.
The increased size and number of male flowers and protracted male floral displays in S. latifolia are probably shaped by sexual selection for more effective pollen dispersal.
Sexual dimorphism; flower size; daily floral display; sexual selection; sex ratios; monoecy; dioecy; Sagittaria latifolia
Background and Aims
The underlying evolutionary processes of pollinator-driven floral diversification are still poorly understood. According to the Grant–Stebbins model speciation begins with adaptive local differentiation in the response to spatial heterogeneity in pollinators. Although this crucial process links the micro- and macroevolution of floral adaptation, it has received little attention. In this study geographical phenotypic variation was investigated in Patagonian Calceolaria polyrhiza and its pollinators, two oil-collecting bee species that differ in body size and geographical distribution.
Patterns of phenotypic variation were examined together with their relationships with pollinators and abiotic factors. Six floral and seven vegetative traits were measured in 45 populations distributed across the entire species range. Climatic and edaphic parameters were determined for 25 selected sites, 2–16 bees per site of the most frequent pollinator species were captured, and a critical flower–bee mechanical fitting trait involved in effective pollination was measured. Geographical patterns of phenotypic and environmental variation were examined using uni- and multivariate analyses. Decoupled geographical variation between corolla area and floral traits related to the mechanical fit of pollinators was explored using a Mantel test.
The body length of pollinators and the floral traits related to mechanical fit were strongly correlated with each other. Geographical variation of the mechanical-fit-related traits was decoupled from variation in corolla size; the latter had a geographical pattern consistent with that of the vegetative traits and was mainly affected by climatic gradients.
The results are consistent with pollinators playing a key role in shaping floral phenotype at a geographical scale and promoting the differentiation of two floral ecotypes. The relationship between the critical floral-fit-related trait and bee length remained significant even in models that included various environmental variables and an allometric predictor (corolla area). The abiotic environment also has an important role, mainly affecting floral size. Decoupled geographical variation between floral mechanical-fit-related traits and floral size would represent a strategy to maintain plant–pollinator phenotypic matching in this environmentally heterogeneous area.
Abiotic environmental gradients; bee morphology; Calceolaria; floral ecotypes; geographical range; local adaptation; oil-collecting bees; oil-offering flowers; Patagonia; phenotypic covariance; specialized pollination; speciation; vegetative morphology
Foraging insect pollinators such as bees must find and identify flowers in a complex visual environment. Bees use skylight polarization patterns for navigation [1–3], a capacity mediated by the polarization-sensitive dorsal rim area (DRA) of their eye [4, 5]. While other insects use polarization sensitivity to identify appropriate habitats , oviposition sites, and food sources , to date no nonnavigational functions of polarization vision have been identified in bees. Here we investigated the ability of bumblebees (Bombus terrestris) to learn polarization patterns on artificial “flowers” in order to obtain a food reward. We show that foraging bumblebees can learn to discriminate between two differently polarized targets, but only when the target artificial “flower” is viewed from below. A context for these results is provided by polarization imaging of bee-pollinated flowers, revealing the potential for polarization patterns in real flowers. Bees may therefore have the ability to use polarization vision, possibly mediated by their polarization-sensitive DRA, both for navigation and to learn polarization patterns on flowers, the latter being the first nonnavigational function for bee polarization vision to be identified.
•Bumblebees (Bombus terrestris) learn polarization patterns on artificial “flowers”•Polarization patterns were only learned from downward-facing, pendant “flowers”•Polarization vision in bumblebees is not restricted to sun-compass navigation•Polarization patterns of petals may be a component of floral signaling
Foraging bumblebees (Bombus terrestris) learn polarization patterns on downward-facing artificial “flowers” to find food, demonstrating that their polarization vision is not restricted to sun-compass navigation. Polarization patterns occur on the petals of real flowers and may be a, hitherto overlooked, component of floral signaling.
For self-pollinating plants to reproduce, male and female organ development must be coordinated as flowers mature. The Arabidopsis transcription factors AUXIN RESPONSE FACTOR 6 (ARF6) and ARF8 regulate this complex process by promoting petal expansion, stamen filament elongation, anther dehiscence, and gynoecium maturation, thereby ensuring that pollen released from the anthers is deposited on the stigma of a receptive gynoecium. ARF6 and ARF8 induce jasmonate production, which in turn triggers expression of MYB21 and MYB24, encoding R2R3 MYB transcription factors that promote petal and stamen growth. To understand the dynamics of this flower maturation regulatory network, we have characterized morphological, chemical, and global gene expression phenotypes of arf, myb, and jasmonate pathway mutant flowers. We found that MYB21 and MYB24 promoted not only petal and stamen development but also gynoecium growth. As well as regulating reproductive competence, both the ARF and MYB factors promoted nectary development or function and volatile sesquiterpene production, which may attract insect pollinators and/or repel pathogens. Mutants lacking jasmonate synthesis or response had decreased MYB21 expression and stamen and petal growth at the stage when flowers normally open, but had increased MYB21 expression in petals of older flowers, resulting in renewed and persistent petal expansion at later stages. Both auxin response and jasmonate synthesis promoted positive feedbacks that may ensure rapid petal and stamen growth as flowers open. MYB21 also fed back negatively on expression of jasmonate biosynthesis pathway genes to decrease flower jasmonate level, which correlated with termination of growth after flowers have opened. These dynamic feedbacks may promote timely, coordinated, and transient growth of flower organs.
Perfect flowers have both male organs that produce and release pollen and female organs that make and harbor seeds. Flowers also often attract pollinators using visual or chemical signals. So that male, female, and pollinator attraction functions occur at the right time, flower organs must grow and mature in a coordinated fashion. In the model self-pollinating plant Arabidopsis, a transcriptional network regulates genes that ensure coordinated growth of different flower organs, as well as pollen release and gynoecium (female) competence to support pollination. This network also regulates nectary development and production of volatile chemicals that may attract or repel insects. We have studied growth, chemical signal levels, and gene expression in mutants affected in components of this network, in order to determine how flower growth is controlled. Several plant hormones act in a cascade that promotes flower maturation. Moreover, regulatory feedback loops affect the timing and extent of developmental steps. Positive feedbacks may ensure that the development of different flower organs is coordinated and rapid, whereas negative feedbacks may allow growth to cease once flowers have opened. Our results provide a framework to understand how flower opening and reproduction are coordinated in Arabidopsis and other flowering plants.
Interactions with pollinators are proposed to be one of the major drivers of diversity in angiosperms. Specialised interactions with pollinators can lead to specialised floral traits, which collectively are known as a pollination syndrome. While it is thought that specialisation to a pollinator can lead to either an increase in diversity or in some cases a dead end, it is not well understood how transitions among specialised pollinators contribute to changes in diversity. Here, we use evolutionary trait reconstruction of bee-pollination and bird-pollination syndromes in Australian egg-and-bacon peas (Mirbelieae and Bossiaeeae) to test whether transitions between pollination syndromes is correlated with changes in species diversity. We also test for directionality in transitions that might be caused by selection by pollinators or by an evolutionary ratchet in which reversals to the original pollination syndrome are not possible.
Trait reconstructions of Australian egg-and-bacon peas suggest that bee-pollination syndrome is the ancestral form and that there has been replicated evolution of bird-pollination syndromes. Reconstructions indicate potential reversals from bird- to bee-pollination syndromes but this is not consistent with morphology. Species diversity of bird-pollination syndrome clades is lower than that of their bee-pollination syndrome sisters.
We estimated the earliest transitions from bee- to bird-pollination syndrome occurred between 30.8 Ma and 10.4 Ma. Geographical structuring of pollination syndromes was found; there were fewer bird-pollination species in the Australian southeast temperate region compared to other regions of Australia.
A consistent decrease in diversification rate coincident with switches to bird pollination might be explained if greater dispersal by bird pollinators results in higher levels of connectivity among populations and reduced chances of allopatric speciation.
The earliest transitions overlap with the early diversification of Australian honeyeaters – the major lineage of pollinating birds in Australia. Our findings are consistent with the idea that environment and availability of pollinators are important in the evolution of pollination syndromes. Changes in flower traits as a result of transitions to bird-pollination syndrome might also limit reversals to a bee-pollination syndrome.
Pollination syndrome; Adaptive radiation; Ancestral state reconstruction; Diversification
American mayapple and Himalayan mayapple are a pair of sister species with disjunct distribution between eastern Asia and eastern North America, which the former was considered to be self-incompatible but the later to be self-compatible. We are interested in the diversification of breeding systems in the two species, particularly a usual mode of self pollination in Himalayan mayapple (Podophyllum hexandrum) which is achieved by movement of the pistil as a previous study suggested. By contrast, our observations and flower manipulations show that delayed selfing was facilitated by petals closing and stamens moving simultaneously to contact the stigma, and bees were effective pollinators although they were few.
Recent molecular phylogenetics have indicated that American mayapple (mainly self-incompatible, SI) and Himalayan mayapple, which was considered to be self-compatible (SC), are sister species with disjunct distribution between eastern Asia and eastern North America. We test a hypothesis that the persistence of this early spring flowering herb in the Himalayan region is attributable to the transition from SI to SC, the capacity for selfing in an unpredictable pollination environment. Pollinator observations were conducted in an alpine meadow with hundreds of Himalayan mayapple (Podophyllum hexandrum Royle) individuals over 2 years. To examine autogamy, seed set under different pollination treatments was compared. To clarify whether automatic self-pollination is achieved by movement of the pistil as a previous study suggested, we measured incline angles of the pistil and observed flower movement during anthesis using video. Floral visitors to the nectarless flowers were very rare, but solitary bees and honeybees could be potential pollinators. Seed set of bagged flowers was not significantly different from that of open-pollinated, self- or cross-pollinated flowers. However, removal of petals or stamens lowered seed yield. The angles of inclination of pistils did not change during the process of pollination. Automatic self-pollination was facilitated by petals closing and stamens moving simultaneously to contact the stigma. Stigmatic pollen load increased little during the day time, in contrast to a sharp increase when the flowers closed during the night-time. These observations indicated that Himalayan mayapple was SC and delayed self-pollination was facilitated by the movement of petals rather than the pistil. Compared with SI American mayapple, no obvious inbreeding depression in SC Himalayan mayapple may contribute its existence in the uplifting zone. A scarcity of pollinators may have driven the shift to delayed selfing in P. hexandrum.
Autogamy; Baker's law; petal movement; Podophyllum hexandrum; Podophyllum peltatum; pollinator limitation; self-compatible; stigmatic pollen load.
Floral traits that correlate with nectar availability or are linked functionally to nectar production carry the potential to enable remote assessment of energy rewards by pollinators. Such floral traits can be considered “honest” in the sense that they convey information about the quality or profitability of a flower to a pollinator. Recently a new sensory channel used in plant-pollinator interactions was identified. We demonstrated that evaporation of water from the nectar itself and the petals create local humidity gradients above Oenothera cespitosa (Onagraceae) flowers. Since these humidity gradients are directly linked to nectar volume, they convey reliable information about nectar rewards to hawkmoth pollinators (Sphingidae). Several studies document a variety of sensory cues that constitute honest signaling between plants and pollinators, and shed light on the central question of when the two parties should communicate honestly. In the following sections, I will comment on different honest signals mediating plant-pollinator interactions, with a special emphasis on our recent findings about floral humidity gradients.
humidity gradient; nectar; floral profitability; floral display; vision; olfaction; hygroreception; honest signaling; transient rewardlessness
Different pollinators can exert different selective pressures on floral traits, depending on how they fit with flowers, which should be reflected in the patterns of variation and covariation of traits. Surprisingly, empirical evidence in support of this view is scarce. Here, we have studied whether the variation observed in floral phenotypic integration and covariation of traits in Narcissus species is associated with different groups of pollinators. Phenotypic integration was studied in two style dimorphic species, both with dimorphic populations mostly visited by long-tongued pollinators (close fit with flowers), and monomorphic populations visited by short-tongued insects (loose fit). For N. papyraceus, the patterns of variation and correlation among traits involved in different functions (attraction and fit with pollinators, transfer of pollen) were compared within and between population types. The genetic diversity of populations was also studied to control for possible effects on phenotypic variation. In both species, populations with long-tongued pollinators displayed greater phenotypic integration than those with short-tongued pollinators. Also, the correlations among traits involved in the same function were stronger than across functions. Furthermore, traits involved in the transfer of pollen were consistently more correlated and less variable than traits involved in the attraction of insects, and these differences were larger in dimorphic than monomorphic populations. In addition, population genetic parameters did not correlate with phenotypic integration or variation. Altogether, our results support current views of the role of pollinators in the evolution of floral integration.
adaptation; genetic diversity; style dimorphism; phenotypic selection; plasticity; pollinator-mediated selection
Background and Aims
The effect of pollination on flower life span has been widely studied, but so far little attention has been paid to the reproductive consequences of delayed pollination in plants with long floral life spans. In the present study, Polygala vayredae was used to answer the following questions. (1) How does male and female success affect the floral longevity of individual flowers? (2) How does delaying fertilization affect the female fitness of this species?
Floral longevity was studied after experimental pollinations involving male and/or female accomplishment, bagging and open pollination. The reproductive costs of a delay in the moment of fertilization were evaluated through fruit set, seed–ovule ratio and seed weight, after pollination of flowers that had been bagged for 2–18 d.
Senescence of the flowers of P. vayredae was activated by pollen reception on the stigmatic papillae, while pollen removal had no effect on floral longevity. Nonetheless, a minimum longevity of 8 d was detected, even after successful pollination and pollen dissemination. This period may be involved with the enhancement of male accrual rates, as the female accomplishment is generally achieved after the first visit. Floral life span of open-pollinated flowers was variable and negatively correlated with pollinator visitation rates. Delayed pollination had a major impact on the reproductive success of the plant, with fruit set, seed–ovule ratio and seed weight being significantly diminished with the increase of flower age at the moment of fertilization.
A strong relationship between pollination and floral longevity was observed. Flowers revealed the ability to extend or reduce their longevity, within some limits, in response to the abundance of efficient pollinators (i.e. reproductive fulfilment rates). Furthermore, with scarce or unpredictable pollinators, a long floral life span could maintain the opportunity for fertilization but would also have reproductive costs on production of offspring. Reduced female fitness late in the flower's life could shift the cost–benefit balance towards a shorter life span, partially counteracting the selection for longer floral life span potentially mediated by scarce pollination services.
Delayed pollination; endemic species; flower longevity; life span; pollen limitation; pollination; pollinator scarcity; Polygala vayredae; Polygalaceae; reproductive consequences; secondary pollen presentation
Background and Aims
Unrelated plants pollinated by the same group or guild of animals typically evolve similar floral cues due to pollinator-mediated selection. Related plant species, however, may possess similar cues either as a result of pollinator-mediated selection or as a result of sharing a common ancestor that possessed the same cues or traits. In this study, visual and olfactory floral cues in Lysimachia species exhibiting different pollination strategies were analysed and compared, and the importance of pollinators and phylogeny on the evolution of these floral cues was determined. For comparison, cues of vegetative material were examined where pollinator selection would not be expected.
Floral and vegetative scents and colours in floral oil- and non-floral oil-secreting Lysimachia species were studied by chemical and spectrophotometric analyses, respectively, compared between oil- and non-oil-secreting species, and analysed by phylogenetically controlled methods.
Vegetative and floral scent was species specific, and variability in floral but not vegetative scent was lower in oil compared with non-oil species. Overall, oil species did not differ in their floral or vegetative scent from non-oil species. However, a correlation was found between oil secretion and six floral scent constituents specific to oil species, whereas the presence of four other floral compounds can be explained by phylogeny. Four of the five analysed oil species had bee-green flowers and the pattern of occurrence of this colour correlated with oil secretion. Non-oil species had different floral colours. The colour of leaves was similar among all species studied.
Evidence was found for correlated evolution between secretion of floral oils and floral but not vegetative visual and olfactory cues. The cues correlating with oil secretion were probably selected by Macropis bees, the specialized pollinators of oil-secreting Lysimachia species, and may have evolved in order to attract these bees.
Colour hexagon; oil secretion; correlated evolution; flower and vegetative scent; headspace analysis; GC-MS; Lysimachia; multidimensional scaling; oil-bee Macropis; phylogeny; spectral photometry
Background and aims
A South American cactus species, Echinopsis ancistrophora (Cactaceae), with dramatic among-population variation in floral traits is presented.
Eleven populations of E. ancistrophora were studied in their habitats in northern Argentina, and comparisons were made of relevant floral traits such as depth, stigma position, nectar volume and sugar concentration, and anthesis time. Diurnal and nocturnal pollinator assemblages were evaluated for populations with different floral trait combinations.
Remarkable geographical variations in floral traits were recorded among the 11 populations throughout the distribution range of E. ancistrophora, with flower lengths ranging from 4·5 to 24·1 cm. Other floral traits associated with pollinator attraction also varied in a population-specific manner, in concert with floral depth. Populations with the shortest flowers showed morning anthesis and those with the longest flowers opened at dusk, whereas those with flowers of intermediate length opened at unusual times (2300–0600 h). Nectar production varied non-linearly with floral length; it was absent to low (population means up to 15 µL) in short- to intermediate-length flowers, but was high (population means up to 170 µL) in the longest tubed flowers. Evidence from light-trapping of moths, pollen carriage on their bodies and moth scale deposition on stigmas suggests that sphingid pollination is prevalent only in the four populations with the longest flowers, in which floral morphological traits and nectar volumes match the classic expectations for the hawkmoth pollination syndrome. All other populations, with flowers 4·5–15 cm long, were pollinated exclusively by solitary bees.
The results suggest incipient differentiation at the population level and local adaptation to either bee or hawkmoth (potentially plus bee) pollination.
Pollination; floral biology; Echinopsis ancistrophora; cactus; Cactaceae; hawkmoth; bee