Pollination systems in Pogonieae (Orchidaceae: Vanilloideae): A hypothesis of evolution among reward and rewardless flowers

The tribe Pogonieae of Vanilloideae (Orchidaceae) consists of six genera, including Pogoniopsis, a myco-heterotrophic taxon with morphological characteristics distinct from the remaining of the tribe. A hypothesis about the phylogeny of the tribe was inferred, involving all currently recognized genera, based on isolated and combined sequence data of 5.8S, 18S and 26S (nrDNA) regions using parsimony and Bayesian analyses. Phylogenetic analyses show that inclusion of Pogoniopsis turns the tribe Pogonieae paraphyletic. All analyses reveal that Pogoniopsis is closely related to members of Epidendroideae. The pantropical Vanilla is monophyletic if Dictyophyllaria is assumed as synonym of Vanilla. Members of Pogonieae are pollinated by several groups of solitary and social bees, two pollination systems being recognized: reward-producing and deceptive. The molecular phylogeny suggests that ancestrals related to Pogonieae gave rise to two evolutionary lines: a tropical one with reward production of flowers, and a predominantly temperate regions invading line with deceptive flowers. Reward-producing flowers characterize the South and Central American clade (=Cleistes), while deceptive pollination is prominent in the clade that includes North American-Asiatic taxa plus the Amazonian genus Duckeella.     

Flower color change accelerated by bee pollination in Tibouchina (Melastomataceae)

Floral color changes are common among Melastomataceae and have been interpreted as a warning mechanism for bees to avoid old flowers, albeit increasing long-distance flower display. Here the reproductive systems of Tibouchina pulchra and T. sellowiana were investigated by controlled pollinations. Their pollinators were identified, and experiments on floral color and fragrance changes were conduced to verify if those changes affect the floral visitation. Both Tibouchina species are self compatible. The flowers lasted three days or more, and the floral color changed from white in the 1st day to pink in the following days. Pollen deposition on stigma induced floral color change. The effectiveness of the pollination is dependent on bees’ size; only large bees were regarded as effective pollinators. In experimental tests, the bees in T. pulchra preferred the natural white flowers while the visitors of T. sellowiana were attracted by both natural and mimetic 1st-day flowers (2nd-day flowers with experimentally attached 1st-day flower petals). During the experiments on floral fragrance, the bees visited both natural and mimetic 1st-day flowers (2nd-day flowers with 1st-day flower scents). In both experiments, the bees avoided natural 2nd-day flowers, but seldom visited modified 2nd-day flowers. The attractiveness of T. pulchra and T. sellowiana flowers cannot be attributed exclusively to the color or the fragrance separately, both factors seemingly act together.     

Does bee or wasp mimicry by orchid flowers also deter herbivores?

General visual bee mimicry and specific chemical mimicry by flowers to solitary female bees or wasps are well known in several orchid genera, for example, the Mediterranean genus Ophrys, the Australian genera Cryptostylis and Chiloglottis, and the South-African Disa. This mimicry has been shown to attract solitary male bees or wasps, which are their species-specific pollinators. The visual and chemical signals are considered to be a type of deceptive pollination mechanism based on mimicry for the exploitation of perceptual biases of animals. We propose that in addition to this unique pollination mechanism, these plants exhibit another, rarely mentioned and practically forgotten, non-exclusive function of bee or wasp mimicry (Batesian mimicry). This mimicry may deter large mammalian herbivores, and possibly also insects from the plants and especially from their flowers by a type of visual and olfactory deceptive aposematism. While visiting the flowers, bees and wasps may add a Müllerian effect to this defense. We extend this hypothesis to many other rewarding flowers that are bee or wasp pollinated and propose that abundance of pollinating bees or wasps may deter herbivorous mammals and insects from the plants during their peak flowering season.     

Notes on the pollination mechanisms ofMoraea inclinata andM. brevistyla (Iridaceae)

Individual flowers ofMoraea inclinata are nectariferous and last about six hours. They appear to be pollinated largely by bees in the familyHalictidae (Lasioglossum spp.,Nomia spp.,Zonalictus) and to a lesser extent by bees in the familyAnthophoridae (Amegilla). The mechanism of bee-pollination inM. inclinata is the Iris type; i.e., each flower consists of three pollination units (an outer tepal, a partly exserted anther, and the opposed style branch which terminates in a pair of petal-like crests). Bees rarely visit more than one pollination unit per flower. Transferral of pollen to the bee is passive and nototribic although all bees collected on the flowers were female and 55% of the bees carried pollen loads with 2–5 pollen taxa in their scopae.Moraea brevistyla flowers are nectariferous but lack scent and last two days. They are visited infrequently by bees and only one femaleLasioglossum spec. carried the pollen ofM. brevistyla. Unlike flowers ofM. inclinata those ofM. brevistyla deposit pollen only on the head and thorax. Bee-mediated autogamy in both species is avoided due to the erratic foraging patterns of the bees and the flexibility of each stigma lobe as the bee backs out of the flower. Approximately 2–4 flowers in the inflorescences of both species (6–8 flowers/infloresence) develop into capsules.     

Specialized pollination by carpenter bees in Calanthe striata (Orchidaceae), with a review of carpenter bee pollination in orchids

Calanthe striata has nectarless flowers that are self‐compatible, but pollinator dependent. Field observations showed that the flowers were pollinated exclusively by the carpenter bee Xylocopa appendiculata circumvolans, although the bees occasionally wasted pollen by delivering to the stigmatic surface pollinaria that retained their anther caps. Fruit set ratios at the population level varied spatiotemporally, but were generally low (8.3–17.3%). Calanthe striata blooms in spring when post‐overwintering carpenter bees have not yet started foraging for brood production. It can therefore exploit an abundance of opportunistic/naïve foragers. This timing may also increase the possibility of pollinator visits, because no rewarding co‐flowering plants are available in the orchid habitats. A literature review of Orchidaceae pollinated by carpenter bees revealed that at least 14 species of Orchidoideae and Epidendroideae have evolved flowers specialized for carpenter bee pollination. They typically have shallow pink/magenta flowers with a foothold for pollinators; pollinaria are attached to the head, ventral thorax or base of the middle legs of carpenter bees when they insert their heads and/or proboscises into flowers; pollination success is generally low, a probable consequence of the deceptive pollination systems. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 730–743.     

Pollination ecology of the Cerrado species Eschweilera nana (Lecythidaceae subfam. Lecythidoideae)

Eschweilera nana is pollinated by a guild of pollinators consisting of mostly bees. Effective pollinators are large bees able to force their way into the closed androecium to access nectar. The morphology of the flowers diminishes self pollination and promotes cross-pollination. Although many pollinators make diurnal visits to the flowers, fruit set was very low in comparison with the number of flowers produced. Breeding system tests yielded only two fruits, one produced by xenogamy and another one in the control test. The results of this study are consistent with studies of other Cerrado plants pollinated by guilds of insects and support the conclusion of other pollination studies of Lecythidaceae that fruit set is low in comparison with the high numbers of flowers produced.     

Variation in style length and anther–stigma distance in Ixiolirion songaricum (Amaryllidaceae)

Variation in style length and anther–stigma distance (ASD) was investigated in 18 populations of Ixiolirion songaricum, an early-spring ephemeral perennial herb in northern Xinjiang. The effect of ASD on autonomous self-pollen deposition and seed set was assessed using bagging experiments. Seed production under autonomous self-pollination, cross-pollination and natural pollination was determined by manual pollination experiments. Stigmas of multiple flowers within an individual were sandwiched between two separate anther levels, and no individuals possessed approach or reverse herkogamy. Style length varied continuously among flowers, resulting in a wide range of variation in ASD. There were fewer flowers with a small ASD than with a large ASD in populations. ASD was negatively correlated with autonomous self-pollen deposition and seed set, but it was positively correlated with natural pollination seed set. Seed production under natural pollination was higher than that under autonomous self-pollination, but it was smaller than that under cross-pollination. Variation in style length and ASD among flowers was not caused by style or stamen elongation in I. songaricum, which differ from other species reported in literature that have continuous variation in style length and ASD.     

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

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

Reproductive biology of Alpinia blepharocalyx (Zingiberaceae): another example of flexistyly

The floral biology and breeding system of Alpinia blepharocalyx were studied in Yunnan province, southwest China. Our results indicate that populations of A. blepharocalyx have two floral morphs, which differ in flowering behaviour: the cataflexistylous morph in which the stigma is held erect above the dehiscent anther when anthesis begins in the morning and becomes curved under the anther at afternoon, and the anaflexistylous morph in which the receptive stigma is curved under the indehiscent anther first and moves into a reflexed superior position above the anther as it begins to shed pollen in the afternoon; the flowering period of both floral morphs is 12 hours; the stylar movements in the two floral morphs are synchronous, and they have similar traits to those found in other Alpinia species previously reported. Also, on average, cataflexistylous flowers are larger than anaflexistylous flowers, especially the labellum and corolla tube length; moreover, the P/O ratio of the two floral morphs is significantly different: the cataflexistylous morph has more pollen grains and fewer ovules than the anaflexistylous morph; the evolutionary significance of this comparison is discussed. Cataflexistylous flowers were observed to produce a lower concentration of nectar than that of anaflexistylous flowers before 11:00 a.m., but they then have higher nectar concentration; cataflexistylous flowers always have more nectar than anaflexistylous flowers. Flowers of A. blepharocalyx were visited by fewer insects at a lower frequency, including honey bees (Apis cerana cerana) and two species of carpenter bees (Xylocopa spp.). No significant differences were found in the fruit set among the hand-pollination treatments regardless of selfing (geitonogamy and autogamy) or crossing (intermorph and intramorph); but all hand-pollination treatments exhibited much higher fruit set than the controls; meanwhile, no fruit set occurred in the unpollinated bagged plants. Pollen tube growth was examined using fluorescence microscopy following self, intramorph, and intermorph hand pollinations at different times of the day; the pollen tubes of both floral morphs have the same growth rate and the capability to reach the ovary. Both the results of pollen tube growth and fruit sets under different pollination conditions show that A. blepharocalyx is self-compatible and dependent upon insects for pollination. The distinctive flexistyly mechanism of A. blepharocalyx is likely a floral mechanism that promotes effective intermorph pollen transfer.     

Intersexual mimicry and flowering phenology facilitate pollination in a dioecious habitat specialist species, <Emphasis Type="Italic">Myristica fatua</Emphasis> (Myristicaceae)

Myristica fatua is a dioecious specialist species restricted to the endangered, freshwater Myristica swamp forests in the Western Ghats, India. Earlier studies have alluded to pollination by deception in members of the Myristica genus, and thus we examined the pollination ecology comprising floral biology, flower production, flower visitors, and reproductive success in M. fatua and inferred the potential strategies that could permit such deception in this habitat specialist tree. Male flowers provide pollen rewards for an extended period of time while female flowers are rewardless and both sexes are visited by generalist insects, mainly by honeybees and stingless bees. Bee visits were significantly more frequent and longer on male than on female flowers as bees collected pollen from male flowers. We found that flower production patterns create a preponderance of males compared to females in the swamp populations. Using a model of honeybee color vision, we found the distance between the color loci of male and female flowers and based on minimum visual angle subtended by these flowers, we suggest that the two floral sexes cannot be discriminated by bees. Bees are likely deceived by the perceptual similarity of rewardless female flowers to pollen-offering male flowers and pollination is the consequence of foraging errors made by pollinators that encounter largely male–rarely female flower mosaics as they forage among clump-distributed M. fatua trees in the swamp habitat.     

Floral specialization for different pollinators and divergent use of the same pollinator among co‐occurring Impatiens species (Balsaminaceae) from Southeast Asia

Floral variation among closely related species is thought to often reflect differences in pollination systems. Flowers of the large genus Impatiens are characterized by extensive variation in colour, shape and size and in anther and stigma positioning, but studies of their pollination ecology are scarce and most lack a comparative context. Consequently, the function of floral diversity in Impatiens remains enigmatic. This study documents floral variation and pollination of seven co‐occurring Impatiens spp. in the Southeast Asian diversity hotspot. To assess whether floral trait variation reflects specialization for different pollination systems, we tested whether species depend on pollinators for reproduction, identified animals that visit flowers, determined whether these visitors play a role in pollination and quantified and compared key floral traits, including floral dimensions and nectar characteristics. Experimental exclusion of insects decreased fruit and seed set significantly for all species except I. muscicola, which also received almost no visits from animals. Most species received visits from several animals, including bees, birds, butterflies and hawkmoths, only a subset of which were effective pollinators. Impatiens psittacina, I. kerriae, I. racemosa and I. daraneenae were pollinated by bees, primarily Bombus haemorrhoidalis. Impatiens chiangdaoensis and I. santisukii had bimodal pollination systems which combined bee and lepidopteran pollination. Floral traits differed significantly among species with different pollination systems. Autogamous flowers were small and spurless, and did not produce nectar; bee‐pollinated flowers had short spurs and large floral chambers with a wide entrance; and bimodally bee‐ and lepidopteran‐pollinated species had long spurs and a small floral chamber with a narrow entrance. Nectar‐producing species with different pollination systems did not differ in nectar volume and sugar concentration. Despite the high frequency of bee pollination in co‐occurring species, individuals with a morphology suggestive of hybrid origin were rare. Variation in floral architecture, including various forms of corolla asymmetry, facilitates distinct, species‐specific pollen‐placement on visiting bees. Our results show that floral morphological diversity among Impatiens spp. is associated with both differences in functional pollinator groups and divergent use of the same pollinator. Non‐homologous mechanisms of floral asymmetry are consistent with repeated independent evolution, suggesting that competitive interactions among species with the same pollination system have been an important driver of floral variation among Impatiens spp.     

Domestication of cardamom (Elettaria cardamomum) in Western Ghats, India: divergence in productive traits and a shift in major pollinators

Background and Aims

Elettaria cardamomum, a highly priced spice, is native to the Western Ghats of South India. Wild populations still occur in isolated patches in their natural habitats; however, much of today''s commercial product comes from cultivated sources. There is no information on domestication-related traits of this species; the main objective of this study was to compare wild and cultivated populations of cardamom in terms of vegetative and reproductive features in order to identify domestication syndromes and to examine whether the two populations have developed reproductive barriers.

Methods

Two wild populations and five cultivated plantations were used for the present study. Vegetative and floral traits, flowering phenology, pollination biology and breeding systems of wild and cultivated populations were compared. Effective pollinators amongst floral visitors were identified by confirming pollen transfer as well as by fruit set following their visit to virgin flowers. Manual pollinations were carried out in order to study the breeding systems of the two populations and reproductive barriers, if any, between them.

Key Results

Several productive traits including the number of branches, number of inflorescences, and total number of flowers per clump, number of flowers that open each day, the duration of flowering, the length of the flower and the amount of nectar per flower are significantly greater in cultivated cardamom. The principal pollinators in wild cardamom are solitary bees, Megachile sp. and two species of Amegilla, whereas those in cultivated cardamom are the social bees Apis dorsata, A. cerana and Trigona iridipennis. Both the wild and cultivated populations are self-compatible and there are no reproductive barriers between the two populations.

Conclusions

Domestication in cardamom has brought about significant changes in vegetative and reproductive traits and a shift in effective pollinators from native solitary bees to social bees. The shift in pollinators seems to be due to the availability of a large number of flowers for prolonged periods in cultivated cardamom that can attract and sustain social bees, rather than due to co-evolution of the flower and the pollinator.Key words: Elettaria cardamomum, wild cardamom, domestication, Amegilla sp., Apis cerana, Apis dorsata, Megachile sp., pollination efficiency, solitary bees, social bees     

Low legitimate pollen flow in distylic Turnera hermannioides (Passifloraceae) and its consequences on fruit and seed set

Turnera hermannioides is a ruderal distylic subshrub, native to NE-Brazil. In the Catimbau National Park, situated within the semi-arid Caatinga region, we studied the pollination ecology of this species, emphasizing (1) effective pollinators; (2) characteristics of short- and long-styled flowers; (3) intra- and intermorph pollen flow; and (4) fruit and seed set. Short and long-styled morphs differ in pollen size and ornamentation, stigmatic surface, style and stamen length and nectar production. The flowers are obligate intermorphic outcrossers and depend on animals for pollination. The flowers of T. hermannioides attracted insect visitors of 25 species, among them butterflies, beetles, but mainly bees. Polylectic bees, such as Apis mellifera, stingless bees, and solitary Callonychium brasiliense were the most frequent visitors and the principal pollinators. The frequency of visits, however, was very low (on average 1.9 visits/flower/day), resulting in a low and unbalanced legitimate pollen flow, i.e. a much lower number of pollen grains from short-styled flowers reaching stigmas of long-styles than vice versa, which in turn compromised fruit and seed set. Surprisingly, Protomeliturga catimbaui and P. turnerae, both oligolectic on flowers of the Turneraceae-clade of the Passifloraceae s.l., were very rare flower visitors and did not contribute significantly to the pollination of Turnera hermannioides. We discuss how the low visitation rate and the inefficiency of pollinators (i.e. inefficiency in promoting legitimate pollination) compromise pollen flow and, consequently, fruit and seed set in this species.     

Three pollination guilds and variation in floral characteristics of Bornean gingers (Zingiberaceae and Costaceae)

The pollinators of 29 ginger species representing 11 genera in relation to certain floral morphological characteristics in a mixed-dipterocarp forest in Borneo were investigated. Among the 29 species studied, eight were pollinated by spiderhunters (Nectariniidae), 11 by medium-sized Amegilla bees (Anthophoridae), and ten by small halictid bees. These pollination guilds found in gingers in Sarawak are comparable to the pollination guilds of neotropical Zingiberales, i.e., hummingbird-, and euglossine-bee-pollinated guilds. Canonical discriminant analysis revealed that there were significant correlations between floral morphology and pollination guilds and suggests the importance of plant–pollinator interactions in the evolution of floral morphology. Most species in the three guilds were separated on the plot by the first and second canonical variables. Spiderhunter-pollinated flowers had longer floral tubes, while Amegilla-pollinated flowers had wider lips than the others, which function as a platform for the pollinators. Pistils and stamens of halictid-pollinated flowers were smaller than the others. The fact that gingers with diverse morphologies in a forest with high species diversity were grouped into only three pollination guilds and that the pollinators themselves showed low species diversity suggests that many species of rare understory plants have evolved without segregating pollinators in each pollination guild.     

Pollination of Sarcandra glabra (Chloranthaceae) in Natural Populations in Japan

Sarcandra glabra was investigated in its natural habitat in Japan. Flowers were protogynous and stigma receptivity dropped off significantly following anther dehiscence. Female-stage and bisexual-stage flowers were visited by beetles, bees, hemiptera, flies, and rarely ants that foraged for pollen and/or small droplets of liquid that occasionally were secreted by the carpels and inflorescence axes. At least the beetles, bees, and hemiptera commonly touched the stigmas and likely effected pollination. Flowers were self-compatible, and automatic selfing sometimes occurred when pollen fell from apical flowers onto the stigmas of lower flowers. Received 8 June 2001/ Accepted in revised form 18 September 2001     

Phylogeny and radiation of pollination systems in DISA (Orchidaceae)

We studied the patterns of adaptive radiation in Disa, a large orchid genus in southern Africa. A cladogram for 27 species was constructed using 44 morphological characters. Pollination systems were then mapped onto the phylogeny in order to analyze pathways of floral evolution. Shifts from one pollination system to another have been a major feature of the evolutionary diversification of Disa. Unlike many plant genera that are pollinated mainly by a single group of insects, radiation in Disa has encompassed nearly all major groups of pollinating insects; in all, 19 different specialized pollination systems have been found in the 27 species included in this analysis. Another striking pattern is the repeated evolution of broadly similar pollination systems in unrelated clades. For example, butterfly-pollinated flowers have evolved twice; showy deceptive flowers pollinated by carpenter bees, twice; long-spurred flowers pollinated by long-tongued flies, four times; night-scented flowers pollinated by moths, three times; and self-pollination, three times. This suggests that a few dominant pollinator species in a region may be sufficient to generate diversification in plants through repeated floral shifts that never retrace the same pathways.     

Adaptive radiation of the putrid perianth: Ferraria (Iridaceae: Irideae) and its unusual pollinators

Field studies of 13 of the estimated 17 species of the southern African geophytic genus Ferraria (Iridaceae: Iridoideae) identified four distinct pollination systems. Ferraria flowers are radially symmetric and cupped with a large, mostly pale or dull-colored perianth. Perigonal nectaries secrete hexose dominant (fructose and glucose) nectar. Most species are pollinated by Diptera of four families, apparently attracted by strong floral odors, mostly putrid or fermenting, but sometimes apparently sweet, and a large perianth mottled and edged with dark color. Concentrated sugary secretions are produced on the tepal claws that form a shallow floral cup. In contrast, flowers of F. ferrariola have a deep, narrow floral cup, a pale blue or yellow perianth, and a spicy scent and are pollinated by bees in the family Apidae, rewarded by nectar of moderate sugar concentration. Ferraria divaricata and F. variabilis have dull-colored, darkly speckled or streaked perianths and produce ample, highly dilute nectar pooled at the base of the floral cup and are pollinated by eumenid and masarine wasps (Vespidae). Lastly, F. uncinata has flowers with a narrow floral cup and dull violet tepals with brown margins. They are visited only by meloid and melyrid beetles. All pollen transfers from the anther of a Ferraria flower to an insect’s body are passive, regardless of pollinator. Pollen load analyses suggests that all pollinators show a high degree of faithfulness to Ferraria flowers.     

Effect of bumble bee (Hymenoptera: Apidae) pollination intensity on the quality of greenhouse tomatoes

Laboratory studies were conducted to assess tomato, Lycopersicon esculentum Mill. (Solanaceae), quality in relation to the level of buzz-pollination by bumble bees. Studies were conducted in commercial tomato greenhouses in the Leamington, Ontario, area to categorize bruising of tomato anther cones by bumble bees into five levels of bruising. The number of pollen grains per stigma was determined for each bruising level, and the bruising level was found to be a good predictor of stigmatic pollen load. Experimental flowers were pollinated by bumble bees and assigned to bruising levels based on the degree of anther cone discoloration. Fruit set, tomato weight, minimum diameter, the number of days until ripe, roundness, weight, percentage sugars, and number of seeds were assessed and compared among bruising level. Fruit set in flowers receiving no pollination visits was 30.2%, whereas, 83.3, 84.4, 81.2, and 100% of the flowers set fruit in bruising levels 1, 2, 3, and 4, respectively. Minimum diameter, number of seeds, and tomato weight all increased from no bruising to different levels of bruising. There was no increase in weight or diameter above a bruising level of 1, and no increase in the number of seeds per fruit after a bruising level of 2. We found that pollination of tomato flowers greater than a bruising level of 2 (corresponding to approximately one to two bee visits) did not result in a significant increase in quality.     

Functional Monoecy Due to Delayed Anther Dehiscence: A Novel Mechanism in Pseuduvaria mulgraveana (Annonaceae)

Unlike most genera in the early-divergent angiosperm family Annonaceae, Pseuduvaria exhibits a diversity of floral sex expression. Most species are structurally andromonoecious (or possibly androdioecious), although the hermaphroditic flowers have been inferred to be functionally pistillate, with sterile staminodes. Pseuduvaria presents an ideal model for investigating the evolution of floral sex in early-divergent angiosperms, although detailed empirical studies are currently lacking. The phenology and pollination ecology of the Australian endemic species Pseuduvaria mulgraveana are studied in detail, including evaluations of floral scent chemistry, pollen viability, and floral visitors. Results showed that the flowers are pollinated by small diurnal nitidulid beetles and are protogynous. Pollen from both hermaphroditic and staminate flowers are shown to be equally viable. The structurally hermaphroditic flowers are nevertheless functionally pistillate as anther dehiscence is delayed until after petal abscission and hence after the departure of pollinators. This mechanism to achieve functional unisexuality of flowers has not previously been reported in angiosperms. It is known that protogyny is widespread amongst early-divergent angiosperms, including the Annonaceae, and is effective in preventing autogamy. Delayed anther dehiscence represents a further elaboration of this, and is effective in preventing geitonogamy since very few sexually mature flowers occur simultaneously in an individual. We highlight the necessity for field-based empirical interpretations of functional floral sex expression prior to evaluations of evolutionary processes.     

Pollination ecology in sympatric winter flowering Helleborus (Ranunculaceae)

We studied biotic and abiotic factors that influence pollination in two sympatric winter flowering species. Helleborus foetidus and Helleborus bocconei flower simultaneously in winter. Although climatic conditions are not favorable for biotic pollination both species rely mainly on large bees of the genus Bombus. At the beginning of flowering, harsh climatic conditions are restrictive for insect visits. As flowering continues and temperatures rise, pollinator activity increases. The two plant species share pollinators that visit them indiscriminately. The flowers of the two species differ in form and insects visit H. foetidus by inserting their heads and H. bocconei ventrally: pollen load on insects is highly specialized. With the arrival of spring, many other species start to bloom and in spite of the large number of flowers still on the plants insects abandon Helleborus species. At the end of spring increasing biotic interactions take away pollinators from the Helleborus species.