Floral trait evolution associated with shifts between insect and wind pollination in the dioecious genus Leucadendron (Proteaceae)

Transitions between animal and wind pollination have occurred in many lineages and have been linked to various floral modifications, but these have seldom been assessed in a phylogenetic framework. In the dioecious genus Leucadendron (Proteaceae), transitions from insect to wind pollination have occurred at least four times. Using analyses that controlled for relatedness among Leucadendron species, we investigated how these transitions shaped the evolution of floral structural and signaling traits, including the degree of sexual dimorphism in these traits. Pollen grains of wind‐pollinated species were found to be smaller, more numerous, and dispersed more efficiently in wind than were those of insect‐pollinated species. Wind‐pollinated species also exhibited a reduction in spectral contrast between showy subtending leaves and background foliage, reduced volatile emissions, and a greater degree of sexual dimorphism in color and scent. Uniovulate flowers and inflorescence condensation are conserved ancestral features in Leucadendron and likely served as exaptations in shifts to wind pollination. These results offer insights into the key modifications of male and female floral traits involved in transitions between insect and wind pollination.     

Pollination in Geonoma macrostachys and Three Congeners,G. acaulis,G. gracilis,and G. interrupta

A continuous 15 month study of the floral ecology of four syntopic understorey palm species of Genoma was conducted in Amazonian Peru lowland rainforest. The spicate inflorescences of G. macrostachys, G. acaulis and G. gracilis are strictly protandrous and the plants are functionally dioecious. Data suggest that in G. macrostachys and G. acaulis pollination is based on a mimicry system, the pistillate flowers mimicking the staminate ones in colour, shape and scent. Pollen-collecting meliponine bees (Hymenoptera, Apidae, Meliponinae) and pollen-feeding syrphid flies (Diptera, Syrphidae) which visit inflorescences during both sexual stages are the pollinators of G. macrostachys. Geonoma acaulis is pollinated by small pollen-feeding weevils (Coleoptera, Curculionidae, Derelomini) that visit male and female spikes. Additionally, in G. macrostachys another pollinator type, viz. euglossine bees (Hymenoptera, Apidae, Euglossinae), which are attracted and rewarded by both types of flowers may account for long-distance pollination. The palm G. gracilis shows a very distinct pollination system. Although opportunistic insect visitors are attracted to the inflorescences of this species it seems to be mainly anemophilous because pollen becomes powdery during an thesis. The branched inflorescences of G. interrupta are also protandrous, but unlike the other species of Geonoma observed, staminate and pistillate anthesis of individual flowers are, for the most, overlapping. A broad spectrum of visitors is attracted (bees, wasps, flies, and beetles), which all may act as pollinators. Outcrossing is especially encouraged during the purely female phase at the end of the flowering cycle when there are no more staminate flowers in the inflorescence. Effects on the reproductive biology and population structure of different pollination systems and breeding system are discussed.     

Thrips pollination of the dioecious ant plant Macaranga hullettii (Euphorbiaceae) in Southeast Asia

Discussion about thrips (Thysanoptera) as main pollinators has been controversial in the past because thrips do not fit the preconception of an effective pollinator. In this study, we present evidence for thrips pollination in the dioecious pioneer tree genus Macaranga (Euphorbiaceae). Macaranga hullettii is pollinated predominantly by one thrips species, Neoheegeria sp. (Phlaeothripidae, Thysanoptera). As a reward for pollinators, the protective floral bracteoles function as breeding sites for thrips and trichomal nectaries on the adaxial surface of the floral bracteoles provide alimentation. Flowering phenology of both staminate and pistillate trees was highly synchronized within 3-4 wk periods. In contrast to pistillate trees, staminate trees start to breed the thrips inside the developing inflorescences ～2 wk before anthesis. Breeding of Neoheegeria sp. in the laboratory indicates that the thrips development is completed within ～17 d. Thus, staminate trees offer breeding sites for one thrips generation until the onset of pollen presentation. Intraspecific pollen transfer by thrips was proved by pollen loads of thrips taken from receptive pistillate inflorescences of M. hullettii. Bagging experiments of different mesh sizes showed that seed set reached almost the level of open-pollinated flowers when exclusively tiny insects like thrips were able to enter the net bags, but no apomictic seed set occurred when no insect access was given to the flowers.     

Attalea phalerata and Bactris glaucescens (Arecaceae, Arecoideae): Phenology and pollination ecology in the Pantanal, Brazil

We compared the reproductive and vegetative phenology and pollination ecology of sympatric Attalea phalerata and Bactris glaucescens palms (Arecaceae) in the Pantanal, Brazil, in a riparian forest area subject to periodic flooding. Attalea phalerata has a solitary stem and produces staminate, pistillate and rarely bisexuals inflorescences that open during the day. Bactris glaucescens has multiple stems and has bisexual flowers with crepuscular/nocturnal anthesis. Both species present bud break and leaf-budding during the year. Attalea phalerata shows continual annual flowering with ripening of fruits during the dry season. For B. glaucescens flowering occurs simultaneously with fruiting for about seven months, and fruit production can be influenced by temperature and level of flooding. The difference in the timing of anthesis of the flowers ensures production of floral resources during both day and night when both species of palms are flowering. The floral structures of both species have morphological characteristics associated with pollination by insects (mainly beetles), such as the presence of odor, stigmatic secretion, heat production, and adhesive substances (“pollenkitt”) in the pollen. In A. phalerata, the main pollinators were Mystrops sp. (Nitidulidae) and Madarini (Curculionidae). Derelomus sp. (Curculionidae) and Paratenetus sp. (Tenebrionidae) beetles visited B. glaucescens during the day and could have pollinated the flowers at these occasions.     

Reproductive biology and pollination ecology of Triplaris gardneriana (Polygonaceae): a case of ambophily in the Brazilian Chaco

• Triplaris gardneriana (Polygonaceae) is a dioecious pioneer tree reported as insect‐pollinated, despite possessing traits related to anemophily. Here, we analyse the possible roles of insects and wind on the pollination of this species to establish whether the species is ambophilous.
• We carried out observations of floral biology, as well as on the frequency and behaviour of pollinators visiting flowers in a population of T. gardneriana in the Chaco vegetation of Brazil. We conducted experimental pollinations to determine the maternal fertility of female plants and whether they were pollen‐limited, and we also conducted aerobiological experiments to provide evidence of how environmental factors influence atmospheric pollen dispersal.
• The population comprised an area of approximately 152.000 m² and was composed of 603 female and 426 male plants (sex ratio = 0.59:0.41). We observed 48 species of insects visiting flowers of T. gardneriana, of which the bees Scaptotrigona depilis and Apis mellifera scutellata were the most effective pollinators. We recorded pollen grains dispersed by wind on 74% of the glass slides placed on females, located at different distances (1–10 m) from male plants.
• Airborne pollen concentration was negatively correlated with relative humidity and positively correlated with temperature. Our observations and experimental results provide the first evidence that T. gardneriana is an ambophilous species, with pollen dispersal resulting from both animal and wind pollination. This mixed pollination strategy may be adaptive in T. gardneriana providing reproductive assurance during colonisation of sites with different biotic and abiotic conditions.

     

Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees

Background and Aims

Pollen-collecting bees are among the most important pollinators globally, but are also the most common pollen thieves and can significantly reduce plant reproduction. The pollination efficiency of pollen collectors depends on the frequency of their visits to female(-phase) flowers, contact with stigmas and deposition of pollen of sufficient quantity and quality to fertilize ovules. Here we investigate the relative importance of these components, and the hypothesis that floral and inflorescence characteristics mediate the pollination role of pollen collection by bees.

Methods

For ten Aloe species that differ extensively in floral and inflorescence traits, we experimentally excluded potential bird pollinators to quantify the contributions of insect visitors to pollen removal, pollen deposition and seed production. We measured corolla width and depth to determine nectar accessibility, and the phenology of anther dehiscence and stigma receptivity to quantify herkogamy and dichogamy. Further, we compiled all published bird-exclusion studies of aloes, and compared insect pollination success with floral morphology.

Key Results

Species varied from exclusively insect pollinated, to exclusively bird pollinated but subject to extensive pollen theft by insects. Nectar inaccessibility and strong dichogamy inhibited pollination by pollen-collecting bees by discouraging visits to female-phase (i.e. pollenless) flowers. For species with large inflorescences of pollen-rich flowers, pollen collectors successfully deposited pollen, but of such low quality (probably self-pollen) that they made almost no contribution to seed set. Indeed, considering all published bird-exclusion studies (17 species in total), insect pollination efficiency varied significantly with floral shape.

Conclusions

Species-specific floral and inflorescence characteristics, especially nectar accessibility and dichogamy, control the efficiency of pollen-collecting bees as pollinators of aloes.     

Contrasting pollination ecology of Disepalum species (Annonaceae): evolutionary loss of the floral chamber and partial breakdown of protogyny associated with a shift in pollination system

Disepalum comprises two monophyletic sister subgenera, Enicosanthellum and Disepalum, with strikingly different floral morphologies: the former has two whorls of unfused sepals, forming a partially enclosed floral chamber, whereas the latter possesses a single whorl of congenitally fused petals and lacks a floral chamber. The pollination ecologies of representative species are reported, including assessments of floral phenology, pollinators and floral thermogenesis. Disepalum pulchrum (subgenus Enicosanthellum) has hermaphroditic flowers with a pollination chamber and is protogynous with prolonged anthesis; it is pollinated by nitidulid beetles and drosophilid flies. Disepalum anomalum (subgenus Disepalum) is also hermaphroditic with prolonged anthesis, but has incomplete protogyny due to overlapping pistillate and staminate phases; it is pollinated by meliponine bees, which are attracted by the pollen, but which are only able to transfer pollen to receptive stigmas during the overlap phase. Alternative evolutionary hypotheses are evaluated, including the possibility that the ancestor of the subgenus Disepalum lineage may have experienced a profound genetic mutation, possibly involving genes responsible for organ merism and fusion, resulting in the loss of the pollination chamber and hence favouring different floral visitors. The breakdown in protogyny required for effective pollination is likely to have had significant ramifications on population genetic diversity.     

Reproductive biology of Syagrus coronata (Arecaceae): sex‐biased insect visitation and the unusual case of scent emission by peduncular bracts

• Several monoecious species of palms have developed complex strategies to promote cross‐pollination, including the production of large quantities of floral resources and the emission of scents that are attractive to pollinators. Syagrus coronata constitutes an interesting model with which to understand the evolution of plant reproductive strategies in a monoecious species adapted to seasonally dry forests.
• We monitored blooming phenology over 1 year, during which we also collected and identified floral visitors and putative pollinators. We identified potential floral visitor attractants by characterizing the scent composition of inflorescences as well as of peduncular bracts, during both male and female phases, and the potential for floral thermogenesis.
• Syagrus coronata produces floral resources throughout the year. Its inflorescences are predominantly visited by a diverse assortment of small‐sized beetles, whose richness and abundance vary throughout the different phases of anthesis. We did not find evidence of floral thermogenesis. A total of 23 volatile compounds were identified in the scent emitted by the inflorescences, which did not differ between male and female phases; whereas the scent of the peduncular bracts was composed of only 4‐methyl guaiacol, which was absent in inflorescences.
• The composition of floral scent chemistry indicates that this palm has evolved strategies to be predominantly pollinated by small‐sized weevils. Our study provides rare evidence of a non‐floral scent emitting structure involved in pollinator attraction, only the second such case specifically in palms. The peculiarities of the reproductive strategy of S. coronata might play an important role in the maintenance of pollination services and pollen dispersion.

     

Diversity of pollination ecology in the Schismatoglottis Calyptrata Complex Clade (Araceae)

• Field studies integrating pollination investigations with an assessment of floral scent composition and thermogenesis in tropical aroids are rather few. Thus, this study aimed to investigate the pollination biology of nine species belonging to Schismatoglottis Calyptrata Complex Clade. The flowering mechanism, visiting insect activities, reproductive system, thermogenesis and floral scent composition were examined.
• Anthesis for all species started at dawn and lasted 25–29 h. Colocasiomyia (Diptera, Drosophilidae) are considered the main pollinators for all the investigated species. Cycreon (Coleoptera, Hydrophilidae) are considered secondary pollinators as they are only present in seven of the nine host plants, despite the fact that they are the most effective pollen carrier, carrying up to 15 times more pollen grains than Colocasiomyia flies. However, the number of Colocasiomyia individuals was six times higher than Cycreon beetles. Chaloenus (Chrysomelidae, Galeuricinae) appeared to be an inadvertent pollinator. Atheta (Coleoptera, Staphylinidae) is considered a floral visitor in most investigated species of the Calyptrata Complex Clade in Sarawak, but a possible pollinator in S. muluensis. Chironomidae midges and pteromalid wasps are considered visitors in S. calyptrata.
• Thermogenesis in a biphasic pattern was observed in inflorescences of S. adducta, S. calyptrata, S. giamensis, S. pseudoniahensis and S. roh. The first peak occurred during pistillate anthesis; the second peak during staminate anthesis. Inflorescences of all investigated species of Calyptrata Complex Clade emitted four types of ester compound, with methyl ester‐3‐methyl‐3‐butenoic acid as a single major VOC (volatile organic compound). The appendix, pistillate zone, staminate zone and spathe emitted all these compounds.
• A mixed fly–beetle pollination system is considered an ancestral trait in the Calyptrata Complex Clade, persisting in Sarawak taxa, whereas the marked reduction of interpistillar staminodes in taxa from Peninsular Malaysia and especially, Ambon, Indonesia, is probably linked to a shift in these taxa to a fly‐pollinated system.

     

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

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

     

Reproductive Biology of the Monoecious Understory Palm Prestoea schultzeana in Amazonian Ecuador1

Prestoea schultzeana is a monoecious, protandrous palm in the forest understory of Amazonian Ecuador. We studied its leaf production, population density, sexual expression, phenology, pollination, and the specificity of the floral visitors. On average, 1.4 leaves and 0.9 inflorescences are produced per individual per year. The number of staminate flowers per inflorescence is relatively constant compared with the number of pistillate flowers which varies greatly. Flowering occurs in staminate and pistillate phases of approximately 19 and 0–7 days duration, respectively. Flowers open in the morning, and staminate flowers abscise in the afternoon of the same day whereas pistillate flowers last for two days. Flowers are whitish-yellow with a sweet odor and produce nectar. They were visited by Coleoptera (Chrysomelidae, Curculionidae, Nitidulidae, Ptiliidae, Staphylinidae), Hemiptera, Diptera (Drosophilidae, Syrphidae, Ceratopogonidae), Lepidoptera (Nymphalidae), and Hymenoptera (Formicidae, Halictidae). All examined individuals of the syrphid fly Copestylum sp. visiting pistillate flowers carried 100–500 grains of P. schultzeana pollen. Pollen occurred on all body parts, but especially on the legs, and this makes Copestylum sp. the most important pollinator. Most floral visitors were also frequent on the flowers of co-occurring plant species; notably the palm Hyospathe elegans shared most visitor species with P. schultzeana.     

Insect-induced wind pollination of the palm Chamaedorea pinnatifrons and pollination in the related Wendlandiella sp.

In Peruvian Amazonia pollination ecology of two palms, Chamaedorea pinnatifrons (Jacq.) Oerst. and Wendlandiella sp. was studied from October 1988 to January 1990. Both palms are dioecious understory species that form locally dense populations.In C. pinnatifrons both sexes flower synchronously during the dry season. Prior to anthesis, the pendulous male inflorescence is inhabited by numerous thrips (Thysanoptera) and Ptiliidae (Coleoptera). Staminate flowers open by a small basal slit between the petals. At anthesis pollen is shed and the movements of the insects inside the flowers trigger pollen release in small clouds. Thus, the powdery pollen becomes airborne and finally air currents act as a vector, carrying pollen to the inconspicuous female plants, which usually are not visited by insects. The term insect induced wind pollination is suggested for this pollination mode. Wendlandiella flowers during four months in the dry season. Male and female plants were not visited by insects. The dry condition of the pollen indicates that anemophily is the pollination mode in Wendlandiella. Fructification is rare but the plants show intense vegetative propagation.The significance of anemophily in the tropical lowland rain forest is discussed.     

Dioecy and the evolution of pollination systems inSchiedea and Alsinidendron (Caryophyllaceae:Alsinoideae) in the Hawaiian Islands

The transition from biotic to wind pollination and the consequencesof this transition for the evolution of dioecious breeding systems wereinvestigated in Schiedea and Alsinidendron(Caryophyllaceae: Alsinoideae), genera endemic to the Hawaiian Islands. The potential for wind pollination was studied for five species ofSchiedea using a wind tunnel. Morphological correlates of windpollination for these species were then used to infer the presence orabsence of wind pollination in the remaining Schiedea species. Hermaphroditic Alsinidendron and Schiedea species,which occur in mesic to wet forests, or less commonly in dry habitats,show little or no indication of wind pollination. These species had lowpollen:ovule ratios, large relative pollen size, diffuse inflorescences,substantial nectar production in several cases, and appear to bebiotically pollinated or autogamous. Sexually dimorphic species, whichall occur in dry habitats, are wind pollinated, based on wind tunnelresults or morphological adaptations indicating the potential for windpollination. These adaptations include high pollen:ovule ratios, smallpollen size, moderately to highly condensed inflorescences, and reducednectaries and nectar production. Shifts to wind pollination anddimorphism are strongly correlated in Schiedea, suggesting theclose functional relationship of the twophenomena.     

Pollen vectors and inflorescence morphology in four species of Salix

 Many plant species exhibit inflorescence morphologies intermediate between pollination syndromes and may therefore employ generalist pollination strategies. We studied how wind and insect pollination are related to inflorescence morphology in the floodplain species Salix alba, S. elaeagnos, S. daphnoides and S. triandra. Insect exclusion experiments showed that all four species were primarily pollinated by insects, but were capable of some seed set when wind was the only pollen vector. Such a generalist pollination system may provide reproductive assurance in these pioneer species. High wind pollination success was associated with slender and divided stigmatic lobes and low ovule number per catkin, which may enhance filtering capacity for airborne pollen. In contrast, species that relied more on insect pollination had robust stigmata and many ovules per catkin, which may reduce the number of insect visits necessary for pollination. Received April 18, 2002; accepted July 23, 2002 Published online: November 28, 2002 Addresses of authors: S. Karrenberg (e-mail: karrenberg@bio.indiana.edu), Department of Biology, Indiana University, Jordan Hall, 1001 East Third Street, Bloomington, IN 47405, USA. P. J. Edwards, Geobotanical Institute, ETH, Zürichbergstrasse 38, CH-8044 Zürich, Switzerland. J. Kollmann, Department of Ecology, Royal Veterinary and Agricultural University, Rolighedsvej 21, DK-1958 Frederiksberg, Denmark.     

THE EVOLUTION OF INSECT-MEDIATED SELF-POLLINATION FROM AN OUTCROSSING SYSTEM IN CALYPTRIDIUM (PORTULACACEAE)

Calyptridium monospermum (Portulacaceae) comprises two biological races visited by different groups of insects. One race, pollinated by a bumblebee, Bombus vosnesenskii (Apidae), is outcrossing, while the other race is pollinated casually by a variety of other insects whose visits result in insect-mediated self-pollination and geitonogamy within the inflorescence. Insect-mediated selfing is also the mode of pollination in the closely related species, C. umbellatum. While all plants of both species are self-compatible, insect visitation is necessary for good seed set. Selfing populations of C. monospermum exhibit many floral adaptations for insect-mediated self-pollination which parallel those of the selfing C. umbellatum, while retaining vegetative characteristics typical of C. monospermum. These floral traits involve flower color and odor, style and stamen orientation, size of stigmatic surfaces, number of pollen grains produced, density of open flowers on inflorescences, and presence or absence of protogyny. Artifical pollination experiments show that these floral adaptations are effective in increasing the probability of insect-mediated self-pollination. Insect-mediated selfing in C. umbellatum and in some populations of C. monospermum is encouraged and probably made necessary by the inconstant pollinating behavior of the insects which visit these plants, as shown by the large percentage of non-Calyptridium pollen recovered from the bodies of insects captured while visiting these plants.     

FUNCTIONAL DIOECY AND ANDROMONOECY IN SOLANUM

Field and laboratory studies of 19 diclinous species endemic to Australia help to clarify the nature and evolution of andromonoecy, androdioecy, and dioecy in the genus Solanum. Ten species are andromonoecious; typically these species bear inflorescences with a single, large basal hermaphroditic flower and 12–60 distal, smaller staminate flowers. We suggest that the andromonoecious condition was derived from hermaphroditic-flowered ancestors in part by hemisterilization of flowers but largely by addition of staminate flowers. The resultant larger inflorescences are hypothesized to serve both to attract and to entrain pollinators, yielding more or higher-quality seed set in hermaphroditic flowers and/or greater dispersion of pollen from staminate flowers. We suggest that andromonoecy may also serve to reduce selling. Nine other species are morphologically androdioecious but functionally dioecious. In these species, staminate flowers, like those of the andromonoecious species, bear anthers with copious tricolporate pollen and a highly reduced gynoecium. The morphologically hermaphroditic flowers are functionally pistillate and borne singly in inflorescences, and they bear anthers with inaperturate pollen. The inaperturate pollen, although viable, never germinates and is hypothesized to be retained in pistillate flowers as a reward to pollinators in the nectarless Solanum flowers. All other species of Solanum studied with pollen dimorphism in which one pollen morph is inaperturate are also best treated as functionally dioecious. We conclude that there is no evidence for androdioecy in Solanum. A review of other families suggests that there is little support for this unusual breeding system in any other angiosperm group either. Preliminary analyses suggest that andromonoecy and dioecy are polyphyletic in Solanum. Furthermore, dioecy is as likely to have arisen from hermaphroditic as from andromonoecious ancestors.     

The best of two worlds: ecology and evolution of ambophilous plants

Ambophily, the mixed mode of wind and insect pollination is still poorly understood, even though it has been known to science for over 130 years. While its presence has been repeatedly inferred, experimental data remain regrettably rare. No specific suite of morphological or ecological characteristics has yet been identified for ambophilous plants and their ecology and evolution remain uncertain. In this review we summarise and evaluate our current understanding of ambophily, primarily based on experimental studies. A total of 128 ambophilous species – including several agriculturally important crops – have been reported from most major habitat types worldwide, but this probably represents only a small subset of ambophilous species. Ambophilous species have evolved both from wind- and insect-pollinated ancestors, with insect-pollinated ancestors mostly representing pollination by small, generalist flower visitors. We compiled floral and reproductive traits for known ambophilous species and compared our results to traits of species pollinated either by wind or by small generalist insects only. Floral traits were found to be heterogeneous and strongly overlap especially with those of species pollinated by small generalist insects, which are also the prominent pollinator group for ambophilous plants. A few ambophilous species are only pollinated by specialised bees or beetles in addition to pollination by wind. The heterogeneity of floral traits and high similarity to generalist small insect-pollinated species lead us to conclude that ambophily is not a separate pollination syndrome but includes species belonging to different insect- as well as wind-pollination syndromes. Ambophily therefore should be regarded as a pollination mode. We found that a number of ecological factors promoted the evolution of ambophily, including avoidance of pollen limitation and self-pollination, spatial flower interference and population density. However, the individual ecological factors favouring the transition to ambophily vary among species depending on species distribution, habitat, population structure and reproductive system. Finally, a number of experimental studies in combination with observations of floral traits of living and fossil species and dated phylogenies may indicate evolutionary stability. In some clades ambophily has likely prevailed for millions of years, for example in the castanoid clade of the Fagaceae.     

SEX DIFFERENTIAL FLORAL LONGEVITY,NECTAR SECRETION,AND POLLINATOR FORAGING IN A PROTANDROUS SPECIES

Sex differential nectar production, floral longevity and pollinator foraging were examined in Lobelia cardinalis, a self-compatible, protandrous species that is hummingbird pollinated. The staminate phase of the flowers lasts significantly longer and produces significantly more nectar (total sugar) per day than the pistillate phase of the flowers. Additional pollen is presented throughout the staminate phase. Because inflorescences of L. cardinalis mature acropetally, the nectar reward on any given day is greatest at the top of the inflorescence (where staminate phase flowers are located). Hummingbirds appear to be sensitive to this pattern of nectar presentation as they most commonly began foraging in the middle of an inflorescence and proceeded upward. This foraging pattern tends to promote outcrossing and suggests that staminate phase flowers are visited more often than pistillate phase flowers. We conclude that L. cardinalis emphasizes the male function at anthesis. Others have hypothesized that the features of this species are a logical consequence of intrasexual selection, but further research is needed before we place great confidence in a sexual selection interpretation of our data.     

Intensified wind pollination mediated by pollen dimorphism after range expansion in an ambophilous biennial Aconitum gymnandrum

Pollination systems and associated floral traits generally differ between core and marginal populations of a species. However, such differences are rarely examined in plants with a mixed wind‐ and bumblebee‐pollination system, and the role of wind pollination during range expansion in ambophilous plants remains unclear. We compared floral traits and the contributions of bumblebee and wind pollination in refugium and marginal populations of the ambophilous plant Aconitum gymnandrum. We found that most floral traits differed between the two populations, and those traits associated with the shift to wind pollination were pronounced in the marginal population. Bumblebee visitation rates varied significantly, but were generally low in the marginal population. Wind pollination occurred in both populations, and the efficiency was lower than that of bumblebee pollination. Two types of pollen grains, namely round and fusiform pollen, were transported to a stigma by bumblebees and wind, but fusiform pollen contributed to wind pollination to a larger degree, especially in the marginal population. Our results suggest that wind pollination was enhanced by pollen dimorphism in the marginal population of A. gymnandrum, and wind pollination may provide reproductive assurance when bumblebee activity is unpredictable during range expansion, indicating that ambophily is stable in this species and shift in pollination system could be common when plants colonize new habitats.     

Geographic variation of reproductive traits and competition for pollinators in a bird‐pollinated plant

Geographic variation in the reproductive traits of animal‐pollinated plants can be shaped by spatially variable selection imposed by differences in the local pollination environment. We investigated this process in Babiana ringens (Iridaceae), an enigmatic species from the Western Cape region of South Africa. B. ringens has evolved a specialized perch facilitating cross‐pollination by sunbirds and displays striking geographic variation in perch size and floral traits. Here, we investigate whether this variation can be explained by geographic differences in the pollinator communities. We measured floral and inflorescence traits, and abiotic variables (N, P, C, and rainfall) and made observations of sunbirds in populations spanning the range of B. ringens. In each population, we recorded sunbird species identity and measured visitation rates, interfloral pollen transfer, and whether the seed set of flowers was pollen limited. To evaluate whether competition from co‐occurring sunbird‐pollinated species might reduce visitation, we quantified nectar rewards in B. ringens and of other co‐flowering bird‐pollinated species in local communities in which populations occurred. Variation in abiotic variables was not associated with geographical variation of traits in B. ringens. Malachite sunbirds were the dominant visitor (97% of visits) and populations with larger‐sized traits exhibited higher visitation rates, more between‐flower pollen transfer and set more seed. No sunbirds were observed in four populations, all with smaller‐sized traits. Sunbird visitation to B. ringens was not associated with local sunbird activity in communities, but sunbird visitation was negatively associated with the amount of B. ringens sugar relative to the availability of alternative nectar sources. Our study provides evidence that B. ringens populations with larger floral traits are visited more frequently by sunbirds, and we propose that visitation rates to B. ringens may be influenced, in part, by competition with other sunbird‐pollinated species.