Animal-pollinated Angiosperms Research Articles

How many animal-pollinated angiosperms are nectar-producing?

The diversity of plant-pollinator interactions is grounded in floral resources, with nectar considered one of the main floral rewards plants produce for pollinators. However, a global evaluation of the number of animal-pollinated nectar-producing angiosperms and their distribution world-wide remains elusive. We compiled a thorough database encompassing 7621 plant species from 322 families to estimate the number and proportion of nectar-producing angiosperms reliant on animal pollination. Through extensive sampling of plant communities, we also explored the interplay between nectar production, floral resource diversity, latitudinal and elevational gradients, contemporary climate, and environmental characteristics. Roughly 223 308 animal-pollinated angiosperms are nectar-producing, accounting for 74.4% of biotic-pollinated species. Global distribution patterns of nectar-producing plants reveal a distinct trend along latitudinal and altitudinal gradients, with increased proportions of plants producing nectar in high latitudes and altitudes. Conversely, tropical communities in warm and moist climates exhibit greater floral resource diversity and a lower proportion of nectar-producing plants. These findings suggest that ecological trends driven by climate have fostered the diversification of floral resources in warmer and less seasonal climates, reducing the proportion of solely nectar-producing plants. Our study provides a baseline for understanding plant-pollinator relationships, plant diversification, and the distribution of plant traits.

Regional plant abundance explains patterns of host use by pollen-specialist bees in eastern North America.

Specialist insect herbivores make up a substantial fraction of Earth's biodiversity; however, they exploit a minority of plant lineages. For instance, in the eastern United States and Canada, ~25% of bee species are pollen specialists, but they are hosted by a small fraction of the native, animal-pollinated angiosperms in the region: Only 6% of plant genera and 3% of families support pollen-specialist bees. It is unclear why some plant lineages host specialist bees while others do not. We know that at least some specialist bees use plant taxa that are avoided by generalists, suggesting that specialist bees favor plants with low-quality pollen, potentially as a strategy to escape competition or obtain protection from natural enemies. There is also evidence that specialist bees prefer superabundant host plants. Here we investigate whether pollen quality and plant abundance predict patterns of host use by specialist bees in eastern North America. Through field observations, we find that plants hosting specialist bees are frequent sources of pollen for generalists, suggesting that their pollen is not generally avoided by bees due to poor pollen quality. In addition, our analysis of a large citizen-science data set shows that regional abundance strongly predicts which plant genera in the eastern United States host pollen-specialist bees. Our results show that bees specialize on regionally abundant-but not necessarily low-quality-plant lineages. These plant lineages may provide more opportunities for the evolution of specialists and lower likelihood of specialist extinction.

Pollen production per flower increases with floral display size across animal-pollinated flowering plants.

The number of open flowers on a plant (i.e., floral display size) can influence plant fitness by increasing pollinator attraction. However, diminishing marginal fitness returns with increasing floral display are expected as pollinators tend to visit more flowers per plant consecutively. An extended flower visitation sequence increases the fraction of ovules disabled by self-pollination (ovule discounting) and reduces the fraction of a plant's own pollen that is exported to sire seeds in other plants (pollen discounting). Hermaphroditic species with a genetic system that prevents self-fertilization (self-incompatibility) would avoid ovule discounting and its fitness cost, whereas species without such a genetically based barrier would not. Contrarily, pollen discounting would be an unavoidable consequence of a large floral display irrespective of selfing barriers. Nevertheless, the increasing fitness costs of ovule and pollen discounting could be offset by respectively increasing ovule and pollen production per flower. We compiled data on floral display size and pollen and ovule production per flower for 1241 animal-pollinated, hermaphroditic angiosperm species, including data on the compatibility system for 779 species. We used phylogenetic general linear mixed models to assess the relations of pollen and ovule production to floral display size. Our findings provide evidence of increasing pollen production, but not of ovule production, with increasing display size irrespective of compatibility system and even after accounting for potentially confounding effects like flower size and growth form. Our comparative study supports the pollen-discount expectation of an adaptive link between per-flower pollen production and floral display across animal-pollinated angiosperms.

On the function of flower number: disentangling fertility from pollinator-mediated selection.

In animal-pollinated angiosperms, the 'male-function' hypothesis claims that male reproductive success (RS) should benefit from large floral displays, through pollinator attraction, while female RS is expected to be mainly limited by resource availability. As appealing as this theory might be, studies comparing selection strength on flower number in both sexes rarely document the expected asymmetry. This discrepancy could arise because flower number impacts both pollinator attraction and overall gamete number. In this study, we artificially manipulate floral displays to disentangle the fertility versus pollinator attraction components of selection, both in terms of mating and RS. In females, flower number was under strong fertility selection, as predicted in the absence of pollen limitation. By contrast, in males, flower number was mainly under sexual selection, which in turn increased male RS. However, these selection patterns were not different in males with artificially increased floral displays. This suggests that sexual selection acting on flower number in males does not occur because flower number increases pollinator attraction, but rather because more pollen is available to disperse on more mates. Our study illustrates the power of disentangling various components of selection with potentially sex-specific effects for understanding the evolution of sexual dimorphism.

Conical petal epidermal cells, regulated by the MYB transcription factor MIXTA, have an ancient origin within the angiosperms.

Conical epidermal cells occur on the tepals (perianth organs, typically petals and/or sepals) of the majority of animal-pollinated angiosperms, where they play both visual and tactile roles in pollinator attraction, providing grip to foraging insects, and enhancing colour, temperature, and hydrophobicity. To explore the evolutionary history of conical epidermal cells in angiosperms, we surveyed the tepal epidermis in representative species of the ANA-grade families, the early-diverging successive sister lineages to all other extant angiosperms, and analysed the function of a candidate regulator of cell outgrowth from Cabomba caroliniana (Nymphaeales). We identified conical cells in at least two genera from different families (Austrobaileya and Cabomba). A single SBG9 MYB gene was isolated from C. caroliniana and found to induce strong differentiation of cellular outgrowth, including conical cells, when ectopically expressed in Nicotiana tabacum. Ontogenetic analysis and quantitative reverse transcription-PCR established that CcSBG9A1 is spatially and temporally expressed in a profile which correlates with a role in conical cell development. We conclude that conical or subconical cells on perianth organs are ancient within the angiosperms and most probably develop using a common genetic programme initiated by a SBG9 MYB transcription factor.

Evolution and diversity of floral scent chemistry in the euglossine bee-pollinated orchid genus Gongora.

•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.•Conclusions 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.

Sterile flowers increase pollinator attraction and promote female success in the Mediterranean herb Leopoldia comosa

Large floral displays have opposing consequences for animal-pollinated angiosperms: they attract more pollinators but also enable elevated among-flower self-pollination (geitonogamy). The presence of sterile flowers as pollinator signals may enhance attraction while allowing displays of fewer open fertile flowers, limiting geitonogamy. The simultaneous contributions of fertile and non-fertile display components to pollinator attraction and reproductive output remain undetermined. The simultaneous effects of the presence of sterile flowers and fertile-flower display size in two populations of Leopoldia comosa were experimentally assessed. Pollinator behaviour, pollen removal and deposition, and fruit and seed production were compared between intact plants and plants with sterile flowers removed. The presence of sterile flowers almost tripled pollinator attraction, supplementing the positive effect of the number of fertile flowers on the number of bees approaching inflorescences. Although attracted bees visited more flowers on larger inflorescences, the number visited did not additionally depend on the presence of sterile flowers. The presence of sterile flowers improved all aspects of plant performance, the magnitude of plant benefit being context dependent. During weather favourable to pollinators, the presence of sterile flowers increased pollen deposition on stigmas of young flowers, but this difference was not evident in older flowers, probably because of autonomous self-pollination in poorly visited flowers. Total pollen receipt per stigma decreased with increasing fertile display size. In the population with more pollinators, the presence of sterile flowers increased fruit number but not seed set or mass, whereas in the other population sterile flowers enhanced seeds per fruit, but not fruit production. These contrasts are consistent with dissimilar cross-pollination and autonomous self-pollination, coupled with the strong predispersal inbreeding depression exhibited by L. comosa populations. Sterile flowers enrich pollination quality by promoting pollen export and import, while limiting the mating costs of geitonogamy associated with large fertile displays.

Does pollen aerodynamics correlate with pollination vector? Pollen settling velocity as a test for wind versus insect pollination among cycads (Gymnospermae: Cycadaceae: Zamiaceae)

Studies of cycad pollination globally have revealed obligate pollination mutualisms with insects, typically hostspecific beetles. Some cycads in the genus Cycas have floating seeds allowing oceanic dispersal, and have colonized remote islands such as Fiji, Guam, and Madagascar. This seems to contradict the expected requirement that specific beetle pollinators be present in order for cycads to establish in remote localities. We therefore postulated that these ‘island’ cycads are wind pollinated. We tested for adaptations associated with wind pollination in a laboratory study of pollen aerodynamics. The pollen from a range of (non-cycad) wind-pollinated plants was not relatively ‘buoyant’: the settling velocities of wind-pollinated species exceeded those of insect-pollinated cycads and some animal-pollinated angiosperms. We attributed this result to settling velocity being, in part, correlated with pollen size, as cycad pollen was consistently smaller. A better predictor for pollination vector was the tendency of pollen to aggregate during a vertical fall. Pollen of wind-pollinated plants separated into single grains, whereas cycad pollen and pollen of animal-pollinated angiosperms adhered in large aggregations, the settling velocity of which increased rapidly with aggregate size. The pollen of cycads known to be insect pollinated was similar in morphology, settling speed, and clumping behaviour to pollen of ‘island’ cycads of unknown pollination biology. Based on these aerodynamics, we predict that cycad species on oceanic islands have insect pollinators. More broadly, we propose that pollen aggregation during a vertical fall provides a sound test for wind versus animal pollination when the pollination vector is unknown.

Dependency on floral resources determines the animals’ responses to floral scents

Animal-pollinated angiosperms either depend on cross-pollination or may also reproduce after self-pollination – the former are thus obligately, the latter facultatively dependent on the service of animal-pollinators. Analogously, flower visitors either solely feed on floral resources or complement their diet with these, and are hence dependent or not on the flowers they visit. We assume that obligate flower visitors evolved abilities that enable them to effectively forage on flowers including mechanisms to bypass or tolerate floral defences such as morphological barriers and repellent / deterrent secondary metabolites. Facultative flower visitors, in contrast, are supposed to lack these adaptations and are often prevented to consume floral resources by defence mechanisms. In cases where obligate flower visitors are mutualists and facultative ones are antagonists, this dichotomy provides a solution for the plants’ dilemma to attract pollinators and simultaneously repel exploiters. In a meta-analysis, we recently supported this hypothesis: obligate flower visitors are attracted to floral scents, while facultative ones are repelled. Here, we add empirical evidence to these results: bumblebees and ants, obligate and facultative flower visitors, respectively, responded as predicted by the results of the meta-analysis to synthetic floral scent compounds.

Pollinator-mediated selfing in two deceptive orchids and a review of pollinium tracking studies addressing geitonogamy

Among the factors thought to have favoured the evolution of deception (rewardlessness) in orchids is the reduction of pollinator-mediated selfing when unrewarded pollinators visit fewer flowers per inflorescence. We obtained data on natural levels of geitonogamy in the deceptive orchids Dactylorhiza sambucina and Himantoglossum hircinum by monitoring the dispersal and receipt of colour-coded pollinia. As donors, we marked 185 flowers of D. sambucina and 956 flowers of H. hircinum. In D. sambucina, 30% of the pollinator-visited flowers and 62% of the marked inflorescences experienced geitonogamous pollination events. In H. hircinum, the respective percentages were 36 and 71%. The furthest pollen transport distance in the Andrena-pollinated H. hircinum was 6.9 m (median 1.27 m), while the furthest transport in the bumblebee-pollinated D. sambucina was 176 m (median 1.23 m), a record in Orchidaceae. An analysis of pollen-tracking studies in orchids revealed geitonogamy levels of around 40% (based on individuals; 19-37% based on flowers) in both rewardless species and rewarding ones. This is similar to geitonogamy levels in other animal-pollinated angiosperms, although the data basis for comparison may still be too small. So far, however, it is not evident that rewardless orchids experience particularly low levels of geitonogamy.

Control of cell and petal morphogenesis by R2R3 MYB transcription factors

Petals of animal-pollinated angiosperms have adapted to attract pollinators. Factors influencing pollinator attention include colour and overall size of flowers. Colour is determined by the nature of the pigments, their environment and by the morphology of the petal epidermal cells. Most angiosperms have conical epidermal cells, which enhance the colour intensity and brightness of petal surfaces. The MYB-related transcription factor MIXTA controls the development of conical epidermal cells in petals of Antirrhinum majus. Another gene encoding an R2R3 MYB factor very closely related to MIXTA, AmMYBML2, is also expressed in flowers of A. majus. We have analysed the roles of AmMYBML2 and two MIXTA-related genes, PhMYB1 from Petunia hybrida and AtMYB16 from Arabidopsis thaliana, in petal development. The structural similarity between these genes, their comparable expression patterns and the similarity of the phenotypes they induce when ectopically expressed in tobacco, suggest they share homologous functions closely related to, but distinct from, that of MIXTA. Detailed phenotypic analysis of a phmyb1 mutant confirmed the role of PhMYB1 in the control of cell morphogenesis in the petal epidermis. The phmyb1 mutant showed that epidermal cell shape affects petal presentation, a phenotypic trait also observed following re-examination of mixta mutants. This suggests that the activity of MIXTA-like genes also contributes to petal form, another important factor influencing pollinator attraction.

Pollen-size comparisons among animal-pollinated angiosperms with different pollination characteristics

Pollen volume varies among angiosperm species over five orders of magnitude, presumably because the functional advantages of pollen size depend on each species» particular pollination and fertilization conditions. This paper reports two studies that assess whether animal-pollinated species with different pollination systems differ correspondingly in pollen size, as would be expected if pollen size affected pollen transport. Analysis of ninePedicularisspecies detected significant interspecific variation in pollen size; however, the overall mean pollen volume of species pollinated primarily by nectar-collecting bees did not differ significantly from that of species pollinated by pollen-collecting bees. Similarly, comparison of bee- and bird-pollinated congeners in 16 genera (nine families) from Australia and North America found considerable variation in pollen diameter within and between genera, but this variation was not associated consistently with differences in primary pollinator type (bee>bird for three genera, bee≈bird for five genera, bee<bird for eight genera). These results imply that pollen-transport conditions likely play a minor role in the evolution of pollen size, at least for bee- and bird-pollinated species. Hence, interspecific pollen-size variation more probably reflects differences in conditions for pollen germination, pollen-tube growth and ovule fertilization.

Pollen-size comparisons among animal-pollinated angiosperms with different pollination characteristics

Pollen volume varies among angiosperm species over five orders of magnitude, presumably because the functional advantages of pollen size depend on each species» particular pollination and fertilization conditions. This paper reports two studies that assess whether animal-pollinated species with different pollination systems differ correspondingly in pollen size, as would be expected if pollen size affected pollen transport. Analysis of ninePedicularisspecies detected significant interspecific variation in pollen size; however, the overall mean pollen volume of species pollinated primarily by nectar-collecting bees did not differ significantly from that of species pollinated by pollen-collecting bees. Similarly, comparison of bee- and bird-pollinated congeners in 16 genera (nine families) from Australia and North America found considerable variation in pollen diameter within and between genera, but this variation was not associated consistently with differences in primary pollinator type (bee>bird for three genera, bee≈bird for five genera, bee<bird for eight genera). These results imply that pollen-transport conditions likely play a minor role in the evolution of pollen size, at least for bee- and bird-pollinated species. Hence, interspecific pollen-size variation more probably reflects differences in conditions for pollen germination, pollen-tube growth and ovule fertilization.

Mating cost of large floral displays in hermaphrodite plants

HERMAPHRODITISM comprises outcrossing whenever the proximity of male and female organs allows self-fertilization1 and interference between sexual functions2. Many floral traits of animal-pollinated angiosperms encourage cross-fertilization3, as recognized by Darwin4-6; however, these characteristics may also allow pollination between flowers on the same individual (geitonogamous self-pollination) 7,8. Simultaneous display of many flowers exemplifies this conflict. Although large floral displays promote outcrossing through enhanced pollinator attraction9, they could be costly in terms of lost mating opportunities10,11 if geitonogamy decreased outcrossed siring success by reducing pollen transfer between plants (pollen discounting12). We report here that, after manipulating the flower number of bee-pollinated Eichhornia paniculata plants, we observed the predicted higher selfing and lower outcrossed siring success for larger inflorescences. Given the reduced fitness resulting when pollen receipt by one flower interferes with pollen export by another, we propose broadening traditional interpretations of floral design and display to recognize their roles in reducing geitonogamous pollen discounting.

Abiotic pollination: an evolutionary escape for animal-pollinated angiosperms

Early botanists considered abiotic pollination to be primitive in angiosperms. But we now deduce from studies of palaeoecology and of extant ‘prim itive’ angiosperms that animal pollination was concom itant with the rise of the angiosperms. Recent studies of wind and w ater pollination in angiosperms also show these systems to be highly sophisticated. If entomophily contributed to the rise of the early angiosperms, why should many of their descendants have later evolved abiotic pollination systems? Although entomophily was initially advantageous to the early angiosperms, abiotic pollination systems may be superior in areas of low species diversity, newly colonized habitats, and places with extremely short growing seasons or other adverse climatic conditions. Abiotically pollinated plants are not constrained by the range of animal pollinators, and as a result are spectacularly successful in long-distance dispersal. Abiotic pollination also offers an escape from deleterious sexual selection and from dependency on pollinators that are climatically limited in their distribution in space or time and vulnerable to extinction. Because evolution of abiotic pollination frequently leads to dicliny or dichogamy, it is largely irreversible. This evolutionary irreversibility coupled with lowered rates of extinction and speciation give wind- or water-pollinated taxa unique phylogenetic profiles. As a large quantity of pollen is wasted by anemophilous plants, it is surprising that so many vigorous species of this kind abounding with individuals should still exist in any part of the w orld; for if they had been rendered entomophilous, their pollen would have been transported by the aid of the senses and appetites of insects with incomparably greater safety than by the w ind... It seems at first sight a still more surprising fact that plants, after having been once rendered entomophilous, should ever have again become anemophilous. (Darwin 1876, p. 407)

Female-predominant sex ratios in angiosperms

A model is presented which expresses the seed production of dioecious and gynodioecious animal-pollinated Angiosperms in terms of the relative seed-fecundity of the sexes, the number of pollinator visits to each flower and the sex ratio. The model predicts that the maximum seed set occurs when females predominate, providing the pollinators visit each flower more than once and the seed set of males is not high. There is strong evidence that a marked preponderance of females in species of four genera is due to more frequent fertilisation by female-determining pollen nuclei than by male-determining nuclei. Two hypotheses have been proposed to explain this differential fertilisation. Several objections are raised to the hypothesis of Lewis (1942), Mulcahy (1967) and Kaplan (1972) that female-predominant sex ratios have been selected because they maximise the total seed production of populations. It is considered that the hypothesis of Smith (1963) that the differential fertilisation is a consequence of the genetic differentiation of sex chromosomes offers a more likely explanation of female-predominant sex ratios.