Is the nectar redox cycle a floral defense against microbial attack?

Many angiosperms use a remarkable reproductive strategy that relies on attracting animals (insect, avian or mammalian pollinators) to transfer pollen between plants. Relying on other organisms for sexual reproduction seems evolutionarily untenable, but the great diversity of angiosperms illustrates how highly successful this strategy is. To attract pollinators, plants offer a variety of rewards. Perhaps the primary floral reward is floral nectar. Plant nectar has long been considered a simple sugar solution but recent work has demonstrated that nectar is a complex biological fluid containing significant and important biochemistry with the potential function of inhibiting microbial growth. These results lead the way to novel insights into the mechanisms of floral defense and the co-evolution of angiosperms and their pollinators.     

Notes on the colour of pollen

The spectral reflection of pollen in 67 plant species out of 28 families was measured by means of mass recording of pollen grains. Various types of spectral reflection curves were found, but 75% belonged to two categories: 1. Human-yellow pollen with strong reflection in the green and red, and low reflection in the ultraviolet and blue range of wavelengths. 2. Human-whitish pollen with strong reflection in the green and red and additional reflection of shorter wavelengths. It is shown that it is important to have information about the mode of the visual pollen display — crypsis or colour contrast against the corolla, pollen advertisement, or concealment — and the visual capabilities of the presumed pollinators in order to be able to discuss the signalling function of pollen colours.     

Stigmatic exudate in the Annonaceae: Pollinator reward,pollen germination medium or extragynoecial compitum?

Although “dry‐type” stigmas are widely regarded as ancestral in angiosperms, the early‐divergent family Annonaceae has copious stigmatic exudate. We evaluate three putative functions for this exudate: as a nutritive reward for pollinators; as a pollen germination medium; and as an extragynoecial compitum that enables pollen tube growth between carpels. Stigmatic exudate is fructose dominated (72.2%), but with high levels of glucose and sucrose; the dominance of hexose sugars and the diversity of amino acids observed, including many that are essential for insects, support a nutritive role for pollinators. Sugar concentration in pre‐receptive flowers is high (28.2%), falling during the peak period of stigmatic receptivity (17.4%), and then rising again toward the end of the pistillate phase (32.9%). Pollen germination was highest in sugar concentrations <20%. Sugar concentrations during the peak pistillate phase therefore provide optimal osmolarity for pollen hydration and germination; subsequent changes in sugar concentration during anthesis reinforce protogyny (in which carpels mature before stamens), enabling the retention of concentrated exudate into the staminate phase as a pollinator food reward without the possibility of pollen germination. Intercarpellary growth of pollen tubes was confirmed: the exudate therefore also functions as a suprastylar extragynoecial compitum, overcoming the limitations of apocarpy.     

Floral reward presentation favored the expression of male function in the pollen‐only flower Melastoma malabathricum

Abstract Animal‐pollinated plant species modulate the presentation of pollinator rewards to maximize reproductive success. In plants providing pollen as the only reward for pollinators, it is usually difficult to unravel the dual roles of reward presentation and the realization of male and female functions (pollen removal and deposition). Exploiting the two types of anther in the androecia of Melastoma malabathricum L., we examined whether the removal of pollen for reward is regulated primarily to favor male function or female function. Pollen removal by carpenter bees from the feeding and pollination anthers, as well as pollen deposition on the stigmas, were quantified during anthesis of M. malabathricum. There was no significant difference in pollen removal rates from the feeding and pollination anthers of M. malabathricum between the onset of anthesis and flower wilting. The stigmatic pollen loads exceeded the ovule number after three sonication bouts, and female function was satisfied earlier than male function. The results support the hypothesis that the presentation of pollination reward in this species is regulated primarily to favor the expression of male function, rather than female function, in agreement with the pollen‐donation hypothesis. A cooperative relationship between the feeding and pollination anthers was demonstrated in heterantherous flowers, which optimizes the balance in investments between pollinator rewards and “functional pollen” for gene transfer.     

The endangered Iris atropurpurea (Iridaceae) in Israel: honey-bees,night-sheltering male bees and female solitary bees as pollinators

Background and Aims

The coastal plain of Israel hosts the last few remaining populations of the endemic Iris atropurpurea (Iridaceae), a Red List species of high conservation priority. The flowers offer no nectar reward. Here the role of night-sheltering male solitary bees, honey-bees and female solitary bees as pollinators of I. atropurpurea is documented.

Methods

Breeding system, floral longevity, stigma receptivity, visitation rates, pollen loads, pollen deposition and removal and fruit- and seed-set were investigated.

Key Results

The main wild pollinators of this plant are male eucerine bees, and to a lesser extent, but with the potential to transfer pollen, female solitary bees. Honey-bees were found to be frequent diurnal visitors; they removed large quantities of pollen and were as effective as male sheltering bees at pollinating this species. The low density of pollen carried by male solitary bees was attributed to grooming activities, pollen displacement when bees aggregated together in flowers and pollen depletion by honey-bees. In the population free of honey-bee hives, male bees carried significantly more pollen grains on their bodies. Results from pollen analysis and pollen deposited on stigmas suggest that inadequate pollination may be an important factor limiting fruit-set. In the presence of honey-bees, eucerine bees were low removal–low deposition pollinators, whereas honey-bees were high removal–low deposition pollinators, because they removed large amounts into corbiculae and deposited relatively little onto receptive stigmas.

Conclusions

Even though overall, both bee taxa were equally effective pollinators, we suggest that honey-bees have the potential to reduce the amount of pollen available for plant reproduction, and to reduce the amount of resources available to solitary bee communities. The results of this study have potential implications for the conservation of this highly endangered plant species if hives are permitted inside reserves, where the bulk of Oncocyclus iris species are protected.     

Unidirectionality of floral colour changes

Many angiosperms have arranged their flowers in inflorescences forming a distinct signalling unit to flower visitors. In some species, the flowers of inflorescences undergo a temporal colour change corresponding exactly to a change in the reward status. Based on information obtained from the spectral reflection curves of pre-change and postchage colours of flower corollas and/or floral guides, it was possible to demonstrate that the colour phase associated with reward closely corresponds to the visual stimuli which trigger behavioural responses of inexperienced flower visitors, and that the colour phase associated with less reward corresponds to visual stimuli less attractive to naïve flower visitors. Reciprocal colour changes were not observed. It is to be assumed that the unidirectionality of floral colour changes is an adaptation of angiosperms aimed at the guidance of first-time flower visitors. Signalling reward to inexperienced flower visitors is an additional function of floral colour changes. The main function of floral colour changes, however, is to provide cues with which the flower visitors can learn to associate one colour phase with reward.     

贠建全:广东荷包岛维管束植物名录

以分布于秦岭的金花忍冬（Lonicera chrysantha Turcz.）、忍冬（L.japonica Thunb.）、葱皮忍冬（L.ferdinandii Franch.）和金银忍冬（L.maackii（Rupr.）Maxim.）为对象,通过定位观察、人工授粉实验、人为设置实验斑块的方法对忍冬属4种植物的开花生物学特性、繁育系统、花色变化现象、传粉过程进行了研究。结果表明,4种植物的单花花期、花部特征存在差异。人工授粉实验显示,4种植物均存在一定的花粉限制,自交不亲和。除葱皮忍冬外,其余3种植物随着花色由白变黄,花粉和花蜜报酬减少、雌雄生殖能力逐渐降低;葱皮忍冬花变色后花蜜量变化不显著,且仍保留较强的雌性生殖能力。变色花的保留被认为是植物的一种生殖策略,通过增大植物的花展示来扩大自身的吸引力,以吸引更多远距传粉者访花。人为控制白、黄花不同数量比的实验结果表明,大多数传粉者偏向访问白花（变色前的花）,且白花提供的报酬量和黄花（变色后的花）数量显著影响传粉者的访花频率,即当花蜜量减少或黄花数量增多时,传粉者访花频率随之降低。因此,我们认为忍冬属4种植物的花色变化可能除了增大植物对远距传粉者的吸引力外,对近距传粉者的访花行为也可能具有一定的影响。当传粉者接近植株时,变色后的花可能暗示其花蜜（花粉）报酬已经发生变化,并驱使昆虫离开并飞向同株或异株植物新开放的报酬丰富的白花,这既有利于提高传粉者的觅食效率,又能降低植物同株异花授粉的几率,对忍冬属植物及传粉者都具有重要意义,是植物长期与授粉昆虫相互适应的反映。     

The potential for selection on pollen colour dimorphisms in Nigella degenii: morph-specific differences in pollinator visitation, fertilisation success and siring ability

Two subspecies of Nigella degenii (Ranunculaceae) possess a dimorphism in pollen colour and vary extensively in frequency of the two morphs in natural populations. Here we investigate the role of selection on pollen colour during the pollination phase in the two subspecies and its potential contribution to the maintenance of this colour variation. In a combination of common garden experiments and field observations, we obtained data on pollinator visitation rates and explored the effect of pollen colour on fertilisation success and siring ability under conditions of low vs. high pollen competition. In experimental gardens, naïve pollinators responded differently to plants with different pollen colour, but the favoured morph varied between dates and locations, and colour morphs were not visited in a frequency-dependent manner. Donor plants with dark pollen had a reproductive advantage (higher seed set) in single-donor pollinations, but the realised siring ability (measured by progeny morph ratio) was highly variable between different two-donor crosses with no general bias towards the light or dark morph. Therefore, although the dark pollen type appears to have a general selective advantage in terms of fertilisation success, our data are also consistent with a scenario involving the maintenance of both colour morphs, particularly under conditions of high pollen competition, a variable genetic background and/or spatial or temporal variation in the pollinator fauna.     

Pseudopollen in Dendrobium unicum Seidenf. (Orchidaceae): Reward or Deception?

BACKGROUND AND AIMS: In 1987, Kjellsson and Rasmussen described the labellar trichomes of Dendrobium unicum Seidenf. and proposed that these hairs function as pseudopollen. Pseudopollen is a mealy material that superficially resembles pollen, is usually laden with food substances and is formed when labellar hairs either fragment into individual cells or become detached from the labellum. However, the trichomes of D. unicum are very different from pseudopollen-forming hairs found in other orchid genera such as Maxillaria and Polystachya. Moreover, Kjellsson and Rasmussen were unable to demonstrate the presence of food substances within these trichomes and argued that even in the absence of food substances, the hairs, in that they superficially resemble pollen, can still attract insects by deceit. The aim of this paper is to investigate whether the labellar trichomes of D. unicum contain food reserves and thus reward potential pollinators or whether they are devoid of foods and attract insects solely by mimicry. METHODS: Light microscopy, histochemistry and transmission electron microscopy. KEY RESULTS: Dendrobium unicum produces pseudopollen. Pseudopollen here, however, differs from that previously described for other orchid genera in that the pseudopollen-forming trichomes consist of a stalk cell and a 'head' of component cells that separate at maturity, in contrast to Maxillaria and some Polystachya spp. where pseudopollen is formed by the fragmentation of moniliform hairs. Moreover, the pseudopollen of Maxillaria and Polystachya largely contains protein, whereas in D. unicum the main food substance is starch. CONCLUSIONS: Flowers of D. unicum, rather than attracting insects solely by deceit may also reward potential pollinators.     

Generalized food deception: colour signals and efficient pollen transfer in bee‐pollinated species of Eulophia (Orchidaceae)

Non‐rewarding plants use a variety of ruses to attract their pollinators. One of the least understood of these is generalized food deception, in which flowers exploit non‐specific food‐seeking responses in their pollinators. Available evidence suggests that colour signals, scent and phenology may all play key roles in this form of deception. Here we investigate the pollination systems of five Eulophia spp. (Orchidaceae) lacking floral rewards. These species are pollinated by bees, notably Xylocopa (Anthophorinae, Apidae) or Megachile (Megachilidae) for the large‐flowered species and anthophorid (Anthophorinae, Apidae) or halictid (Halictidae) bees for the small‐flowered species. Spectra of the lateral petals and ultraviolet‐absorbing patches on the labella are strongly contrasting in a bee visual system, which may falsely signal the presence of pollen to bees. All five species possess pollinarium‐bending mechanisms that are likely to limit pollinator‐mediated self‐pollination. Flowering times extend over 3–4 months and the onset of flowering was not associated with the emergence of pollinators, some of which fly year round. Despite sharing pollinators with other plants and lacking rewards that would encourage fidelity, the Eulophia spp. exhibited relatively high levels of pollen transfer efficiency compared with other rewarding and deceptive orchids. We conclude that the study species employ generalized food deception and exploit food‐seeking bees. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 713–729.     

Floral colour change in Pedicularis monbeigiana (Orobanchaceae)

We examined the effects of the retention of colour-changed flowers on long- and short-distance attractiveness of bumblebees and the likelihood of successive flower visits by bumblebees in Pedicularis monbeigiana. The lower lip changed colour with age from white to purple. Hand geitonogamous pollination significantly reduced seed production. No pollen limitation occurred in this species. Purple-phase flowers contributed minimally to pollinator attractiveness at long distance. The combination of less reproductive flowers with a lower amount of reward and floral colour change enabled plants to direct pollinators to reproductive, highly rewarding white flowers at close range. A high percentage of purple-phase flowers in an inflorescence was associated with a marked reduction in the frequency of successive flower visits to individual plants. We suggest floral colour change in P. monbeigiana may serve as a mechanism for enhancing inter-individual pollen transfer and reducing intra-individual pollen transfer.     

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

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

Feeding friend and foe: ample pollen mitigates the effects of pollen theft for a gynodioecious plant,Polemonium foliosissimum (Polemoniaceae)

Background and AimsMost angiosperms rely on pollinators to transport pollen and effect fertilization. While some floral visitors are effective pollinators, others act as thieves, consuming pollen but effecting little pollination in return. The importance of pollen theft in male and female reproductive success has received little attention. Here, we examined if pollen consumption by flies altered pollen receipt and exacerbated pollen limitation for a bumblebee-pollinated plant, Polemonium foliosissimum (Polemoniaceae).MethodsTo examine the effect of pollen-thieving flies, we took a three-pronged approach. First, we used single-visit observations to quantify pollen removal and pollen deposition by flies and bumblebees. Second, we manipulated pollen in the neighbourhood around focal plants in two years to test whether pollen reduction reduced pollen receipt. Third, we combined pollen reduction with hand-pollination to test whether pollen thieving exacerbated pollen limitation. Polemonium foliosissimum is gynodioecious in most populations in the Elk Mountains of central Colorado, USA. Thus, we also tested whether pollen theft affected hermaphrodites and females differently.ResultsFlies removed significantly more pollen and deposited less pollen per visit than did bumblebees. Reduction of pollen in the neighbourhood around focal plants reduced pollen receipt in both years but only nearly significantly so in 2015. In 2016, plants were significantly pollen-limited; hand-pollination significantly increased seeds per fruit for both hermaphrodites and females. However, the reduction of pollen around focal plants did not exacerbate pollen limitation for either hermaphrodites or females.ConclusionsOur results suggest that plants tolerate significant consumption of pollen by thieves and pollinators by producing ample pollen to feed both and fertilize available ovules. Our results demonstrate that pollen limitation in P. foliosissimum is driven by lack of effective pollinators rather than lack of pollen. Teasing out these effects elucidates the relative importance of drivers of reproductive success and thus the expected response to selection by different floral visitors.     

Pollen advertisement: chemical contrasts between whole-flower and pollen odors

Odors of pollen and whole flowers were compared in taxonomically unrelated species that offer pollen as the only food reward to pollinators. Volatiles were collected using headspace adsorption and analyzed by gas chromatography and mass spectrometry. The odor of pollen was found to be chemically distinct from the total flower odor, and this pollen-odor distinctness varied among the three species. In Papaver rhoeas (Papaveraceae), the contrast between pollen and whole-flower odors was most subtle, with differences observed only in the proportions of individual volatiles (almost exclusively aliphatic hydrocarbons). In Filipendula vulgaris (Rosaceae), pollen volatiles were fewer than in the flowers (comprising mainly benzenoids and fatty-acid derivatives) and their relative proportions produced an odor dominated by 2-heptadecanone that contrasted strikingly with the flower odor dominated by 2-phenyl ethanol. In Lupinus polyphyllus (Fabaceae), the pollen odor contained fewer volatiles and in differing proportions than the flower fragrance (comprising almost exclusively isoprenoids). The findings add to earlier chemical evidence of odor contrasts between pollen and other flower parts in two other species. Drawing on information from pollination studies of these various species, it is suggested that pollen odor is used by pollen-foraging insects both to discriminate between plant species and to assess reward availability in individual flowers, and that it might in addition serve a protective function against destructive flower-feeding insects and pathogens.     

The coexistence of binucleate and trinucleate pollen in Mitrephora macclurei Weerasooriya & R. M. K (Annonaceae)

Pollen of angiosperms may be either binucleate or trinucleate at maturity. According to Schürhoff–Brewbaker law, the binucleate state is pleisomorphic occuring in about 70% of all angiosperms, while the trinucleate state is advanced occurring in about 30% of the angiosperms. The derivation of trinucleate pollen from binucleate pollen is irreversible, thus trinucleate or mixed pollen was considered uncommon in early lineage. In the present work, using conventional paraffin section method, the coexistence of both binucleate and trinucleate pollen in the same intact anther were observed in Mitrephora macclurei, a species belonging to the eumagnoliid family Annonaceae. The increasing number of plants with trinucleate or mixed pollen discovered in early lineages, as well as climatic introduced changes in nuclear number challenge analyses of ancestral state and evolution of pollen nuclear number in angiosperms.     

The Pollen Tube Pathway in Tasmannia insipida (Winteraceae): Homology of the Male Gametophyte Conduction Tissue in Angiosperms

Abstract: The pathway of the pollen tube in Tasmannia insipida (Winteraceae), an archaic angiosperm, is described. Visual observations and measurements of percentage sugar content from stigmatic exudate and the calyptra droplet were made. The droplet that forms on the calyptra of unopened flowers was artificially pollinated, but no pollen tubes appeared to grow through it to the gynoecium of female flowers. Calyptra droplets occur on both female and male (having reduced female structures) flowers of this dioecious plant. It is considered unlikely that a drop pollination mechanism, analogous to that found in some gymnosperms, is at work in T. insipida, and it is proposed that one possible droplet function is as a "reward" to potential pollinators in advance of flower opening. Pollen tubes were observed to grow almost exclusively along epidermal cells. Early thoughts on angiosperm transmission tissue are re-examined and built upon. It is proposed that the male gametophyte conduction tissue in angiosperms is homologous with epidermal tissue, and that pollen tube passage occurred originally solely along the surface of specialized epidermal cells, or possibly for short distances along unspecialized regions covered with exudate derived from these cells. Some earlier attempts to explain transmitting tissue homology and evolution are discussed.     

Pollen layering and male–male competition: Quantum dots demonstrate that pollen grains compete for space on pollinators

Premise

Almost nothing is known about what happens to pollen grains once they attach to pollinators, although some have postulated that pollen from different donors may form complex, two- or three-dimensional landscapes (e.g., layers or mosaics) that can facilitate male–male competition. For example, pollen that is already on pollinators may preclude the deposition of subsequent pollen grains.

Methods

Using quantum dots to mark the pollen of individual flowers, we explored the possibilities of layering and preclusion in a fly-pollinated iris, Moraea lurida.

Results and Conclusions

The proportion of labeled pollen from the last flower visited diminished in sequential pollen samples taken from the top to the bottom of the pollen load, representing the first empirical evidence for pollen layering. However, the consequences in terms of pollen preclusion were equivocal: Although the pre-existing pollen load size was not a good predictor of new pollen receipt, labeled pollen loads from the last flower visited were significantly smaller than pollen loads from the previous flower visited. Thus, pollen from the previous flower may preclude pollen placement from a subsequently visited flower, and pollen from different flowers may compete for space on pollinators.

     

Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators

An adaptive role of corolla shape has been often asserted without an empirical demonstration of how natural selection acts on this trait. In generalist plants, in which flowers are visited by diverse pollinator fauna that commonly vary spatially, detecting pollinator-mediated selection on corolla shape is even more difficult. In this study, we explore the mechanisms promoting selection on corolla shape in the generalist crucifer Erysimum mediohispanicum Polatschek (Brassicaceae). We found that the main pollinators of E. mediohispanicum (large bees, small bees and bee flies) discriminate between different corolla shapes when offered artificial flowers without reward. Importantly, different pollinators prefer different shapes: bees prefer flowers with narrow petals, whereas bee flies prefer flowers with rounded overlapping petals. We also found that flowers with narrow petals (those preferred by bees) produce both more pollen and nectar than those with rounded petals. Finally, different plant populations were visited by different faunas. As a result, we found spatial variation in the selection acting on corolla shape. Selection favoured flowers with narrow petals in the populations where large or small bees are the most abundant pollinator groups. Our study suggests that pollinators, by preferring flowers with high reward, exert strong selection on the E. mediohispanicum corolla shape. The geographical variation in the pollinator-mediated selection on E. mediohispanicum corolla shape suggests that phenotypic evolution and diversification can occur in this complex floral trait even without specialization.     

Floral Biology and Pollination Mechanisms in Two Viola Species—From Nectar to Pollen Flowers?

The genus Viola is represented by four related species in Brazil belonging to section Leptidium, one of the most primitive sections in the genus. Floral biology and pollination by bees were studied in Viola cerasifolia and V. subdimidiata in high-altitude areas in south-eastern Brazil. Flowers are zygomorphic and spurred. The five stamens are arranged in a cuff around the ovary, and pollen is released by means of apical connective projections, which form a cone surrounding the base of the style. The connective projections of the inferior stamens are elongated and curved to form a hook-shaped structure. Nectar-secreting tissue can occur in the basal connective appendages of the inferior stamens, which project into the spur. Flowers of V. subdimidiata secreted a mean volume of 0.14 micro l nectar over a 24-h period; approx. 40 % of flowers did not secrete any nectar. The main pollinators of these Viola species are female bees belonging to the genus Anthrenoides (Andrenidae), which search mainly for pollen. These bees seem to be oligolectic and obtain large amounts of pollen from Viola by vibrating the flowers or by moving the hook repeatedly back and forth. Males of Anthrenoides patrol Viola clusters and also feed on nectar, acting as secondary pollinators. The basic floral structure in the genus Viola fits that of 'nectar flowers'. The uncommon hook-shaped projections, scanty nectar production, and behaviour of pollinators suggest that V. cerasifolia and V. subdimidiata are shifting their reward for pollinators from nectar to pollen. Based on floral morphology, this shift may be widespread in Viola sect. Leptidium.     

Secondary pollen presentation: More than to increase pollen transfer precision

Pollination precision and efficiency have been deemed to be important driving forces in floral evolution. Herkogamy reduction is a main mechanism to increase pollination precision. Secondary pollen presentation (SPP), by which pollen is presented on other floral organs especially pistils, has been widely accepted as a special mechanism to increase pollen transfer precision through spatial reduction of the anther–stigma distance, that is, minimized herkogamy. This overlooks a potential driving force, that is expanding the pollination niche through converting pollen thieves and nectar robbers into effective pollinators. We selected two species as study models with typical pistillate SPP, Pavetta hongkongensis Bremek. (Rubiaceae) and Scaevola taccada (Gaertn.) Roxb. (Goodeniaceae). In both species, two distinct pollinator functional groups were recognized. Short-tongued bees and flies fed on pollen on stigmas but also stole pollen from anthers and robbed nectar, whereas long-tongued hawkmoths and butterflies only collected nectar. Emasculation had no influence on long-tongued pollinators, but significantly decreased the visitation frequency of short-tongued visitors and fruit set, compared to intact flowers, demonstrating short-tongued visitors did not effectively pollinate and acted merely as pollen thieves or nectar robbers when SPP was absent. Data from the two plant species clearly indicated pistillate SPP has additional adaptive advantages of converting ineffective visitors into pollinators and consequently widening the pollination niche, which could help plants overcome environmental stochasticity. Our results suggest that multiple selective forces drive the evolution of SPP and the minimization of herkogamy.