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One-by-one stamen movement in Parnassia palustris. The first stamen (%) elongates its filament slowly and its anther starts dehiscence after about one day later when the filament reached its maximum length (A). The filament deflexes about one day later and the stamen bends out of the floral center (filament angle "45u, indicated by the horizontal dash line); simultaneously the second stamen (&) begins its filament elongation (B). Similarly, the third (#), fourth ( N ), and fifth (e) stamens start their filament elongation only after the former stamen has moved out of the floral center (C, D, E). The number next to each stamen in (E) indicates the movement sequence (note that the dehisced anthers always abscise during the movement process). Shaded areas indicate night-time. doi:10.1371/journal.pone.0086581.g001
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The selective pressure imposed by maximizing male fitness (pollen dispersal) in shaping floral structures is increasingly recognized and emphasized in current plant sciences. To maximize male fitness, many flowers bear a group of stamens with temporally separated anther dehiscence that prolongs presentation of pollen grains. Such an advantage, howe...
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... palustris is distinct for its single slender stem with single flower on the top and five strikingly-branched staminodes with a nectary-like tip on each branch [22,23] (Fig. 1). The nectary-like tip has been proven to be attractant to pollinators [22]. There are five fertile stamens aggregating at the flower's center when the flower opens. These stamens become elevated, one-by-one through filament elongation, and then the anthers dehisce sequentially over the immature pistil [16]. Of greater significance is ...
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... group is easier and more accurate to record, and also because within each functional group members normally interacted with floral parts in a similar way [18,24,25]. Five functional groups were identified as floral visitors: hoverflies, ichneumon wasps, vespid wasps, flies, and ants. The main species of each functional group are shown in Fig. ...
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... the beginning of anthesis, all five fertile stamens were incurved and aggregated around the gynoecium. About 5 h after the flower had fully opened (286613 min in 2009 and 313612 min in 2012; N = 35 in each years), one stamen began to elongate its filament and to uplift its anther slowly above the gynoecium (Fig. 1A). It took approximately 24 h (1400 min) for the stamen to begin anther dehiscence after the start of filament elongation (Table 1). The anther dehiscence lasted for about 5 h (Table 1) after which the filament began to deflex and the filament angle increased as a result (Fig. 1B). It took about 24 h for the filament to finish its ...
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... its filament and to uplift its anther slowly above the gynoecium (Fig. 1A). It took approximately 24 h (1400 min) for the stamen to begin anther dehiscence after the start of filament elongation (Table 1). The anther dehiscence lasted for about 5 h (Table 1) after which the filament began to deflex and the filament angle increased as a result (Fig. 1B). It took about 24 h for the filament to finish its deflexion (Table 1), i.e. when the filament angle reached its maximum (Fig. 1C). The next stamen's filament elongation normally started only after the former stamen had moved out of the floral center (filament angle "45u) (Fig. 1), which was more than 3.5 hours after the start of the ...
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... to begin anther dehiscence after the start of filament elongation (Table 1). The anther dehiscence lasted for about 5 h (Table 1) after which the filament began to deflex and the filament angle increased as a result (Fig. 1B). It took about 24 h for the filament to finish its deflexion (Table 1), i.e. when the filament angle reached its maximum (Fig. 1C). The next stamen's filament elongation normally started only after the former stamen had moved out of the floral center (filament angle "45u) (Fig. 1), which was more than 3.5 hours after the start of the former stamen's anther dehiscence (Table 1). The five fertile stamens moved in an alternate sequence (as opposed to a clockwise or ...
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... began to deflex and the filament angle increased as a result (Fig. 1B). It took about 24 h for the filament to finish its deflexion (Table 1), i.e. when the filament angle reached its maximum (Fig. 1C). The next stamen's filament elongation normally started only after the former stamen had moved out of the floral center (filament angle "45u) (Fig. 1), which was more than 3.5 hours after the start of the former stamen's anther dehiscence (Table 1). The five fertile stamens moved in an alternate sequence (as opposed to a clockwise or an anti-clockwise sequence; Fig. 1E). For every movement stage there was no significant difference between the two years (P.0.055, Student's t- test; ...
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... filament elongation normally started only after the former stamen had moved out of the floral center (filament angle "45u) (Fig. 1), which was more than 3.5 hours after the start of the former stamen's anther dehiscence (Table 1). The five fertile stamens moved in an alternate sequence (as opposed to a clockwise or an anti-clockwise sequence; Fig. 1E). For every movement stage there was no significant difference between the two years (P.0.055, Student's t- test; Table ...
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... five insect functional groups on P. palustris flowers showed different forage preferences: hoverflies seek both nectar and pollen, vespid wasps only seek pollen, ichneumon wasps and ants feed only on nectar at the base of filament and flies mainly forage the nectar on the top of staminodes (Fig. S1). These insects differed in visitation rate and duration (Table 2), with hoverflies, flies and ants as the most common visitors to the flowers (Fig. 3) Control flowers (i.e. flowers with free movement of stamens) were visited by different groups of pollinators with high visitation rates and duration (Fig. 3). As a result, most pollen ...
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... at the floral center; (ii) the anther-dehisced stamen will bend out of the floral center before the next stamen's anther dehiscence. The stamens move very slowly, with filament elongation taking nearly a whole day to reach their maximum. Anther dehiscence lasts for approximately 5 h and finally, the filament deflexion lasts for another day (Fig. 1, Table 1). These movements are obviously much slower than in other taxa. In Loasaceae the stamens move from their original places (petals) to the floral center in only 2- 4 min [5,20] and in Rutaceae this movement takes less than 20 min [18]. The higher frequency of pollinator visits [5,18] and stamen movements can be triggered by floral ...
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... visitation durations (Fig. 3) and suppressed pollen dispersal of the dehiscing anther (Fig. 4). We therefore conclude that deflection of the anther-dehisced stamen from the flower's center in P. palustris flowers is likely a mechanism to avoid interference with late-dehiscing anthers. The alternate movement sequence of the five fertile stamens (Fig. 1E) and the abscission of the dehisced anther after moving out of the floral center ( Fig. 1D,E) may further decrease anther-anther interfer- ences. During this process, the stigma is getting mature and selfing is possible since this plant is self-compatible (Fig. 2). We speculated that the drop off of the dehisced anthers may also avoid ...
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... 4). We therefore conclude that deflection of the anther-dehisced stamen from the flower's center in P. palustris flowers is likely a mechanism to avoid interference with late-dehiscing anthers. The alternate movement sequence of the five fertile stamens (Fig. 1E) and the abscission of the dehisced anther after moving out of the floral center ( Fig. 1D,E) may further decrease anther-anther interfer- ences. During this process, the stigma is getting mature and selfing is possible since this plant is self-compatible (Fig. 2). We speculated that the drop off of the dehisced anthers may also avoid anther- stigma interferences (including selfing) and thus may be selectively advantageous. ...
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Citations
... Stamens of Saxifraga candelabrum exhibited a successive movement, a feature also found in the Parnassiaceae, Rutaceae, Tropaeolaceae, and Loasaceae [15]. The adaptive significance of such stamen movements has been proposed to reduce male-female and male-male interference [17], increase pollen deposition [16], promote pollen export [43], and achieve reproductive assurance [18]. In flowers of S. candelabrum, the staminate and carpellate phases are distinctively separated, which precludes male-female interactions and reproductive assurance via selfing. ...
... ex Wight & Arn. [17,18,43], all with successive stamen movement, our experiments also found the reproduction of S. candelabrum was pollen-limited, which highlights strong selection pressure to maximize pollen transfer. To consolidate the adaptiveness of successive stamen movement, it is ideal to compare pollen transfer and seed sired between flowers with such behaviors and those without. ...
... Nonetheless, a few studies have tried to fix mature stamens with threads or tapes from bending to the center or moving away in Parnassia spp. [17,43] and Ruta graveolens [18]. Their results showed that manipulations had either reduced pollen visitation or pollen transfer efficiency, resulting in fewer seed set. ...
Background
Successive stamen movement is a complex plant behavior involving successive uplift of stamens and pollen release, which plays a role in reducing sexual interference, increasing pollen deposition and promoting pollen export. Although reported from several taxa, studies on whether the movement can be influenced by abiotic and biotic factors are scarce.
Methods
In this study, we here for the first time described a pattern of successive stamen movement in Saxifraga candelabrum (Saxifragaceae). We then compared the rates of stamen movement in S. candelabrum under different weather and varying pollinator visits. Pollen packaging and presentation schedule of S. candelabrum were also investigated.
Results
The results showed that the number of stamens bent per day in sunny days was significantly higher than overcast and rain. Flowers that receive more pollinator visits (control treatment) had significantly higher number of stamen movement than those that received fewer (removal treatment) and none (bagging treatment). Throughout the staminate phase of a flower, there was a progressive increase in both pollen quantity of individual stamens and pollen presentation during each day.
Conclusion
Our research demonstrates that successive stamen movement in S. candelabrum was accelerated by favorable weather and increased pollinator visits, which may promote pollen export. Moreover, incremental pollen packaging is likely an adaptation to seasonal regularity in variations of sex ratio resulting from protandry.
... For example, some plants, such as some genera of Fabaceae (e.g., Medicago, Trifolium, Ulex), possess explosive pollen release mechanisms (reviewed by Aluri and Reddi, 1995) to rapidly release a vast proportion of the pollen from flowers during the first pollinator visit. Other plants dispense pollen by gradual maturation of anthers within a flower and present pollen from only a fraction of anthers at each moment (Ren and Bu, 2014). A similar goal, i.e., gradual pollen release, can also be reached by the pump mechanism employed, e.g., by most Asteraceae, where pollen is pumped out by gradual pistil growth through the flower tube (Erbar and Leins, 1995;Galloni et al., 2007). ...
Premise:
Animal-pollinated plants face a high risk of pollen loss during its transfer. To limit the negative effect of pollen losses by pollen consumption and heterospecific transfer, plant species may adjust and stratify their pollen availability during the day (i.e., "schedule" their pollen presentation) and attract pollinators in specific time frames.
Methods:
We investigated diurnal patterns of pollen availability and pollinator visitation in three coflowering plant species: Succisa pratensis with open flowers and accessible pollen, pollinated mainly by pollen-feeding hoverflies; Centaurea jacea with open flowers and less accessible pollen, pollinated mainly by pollen-collecting bees; and Trifolium hybridum with closed flowers and pollen accessible only after the active opening of the flower, pollinated exclusively by bees.
Results:
The three plant species differed in the peak pollen availability, tracked by the visitation activity of their pollinators. Succisa pratensis released all pollen in the morning, while pollinator activity was still low and peaked with a slight delay. In contrast, C. jacea and T. hybridum had distinct pollen presentation schedules, peaking in the early afternoon. The pollinator visitation to both of these species closely matched their pollen availability.
Conclusions:
Stratifying pollen availability to pollinators during the day may be one of several mechanisms that allow coflowering plants to share their pollinators and decrease the probability of heterospecific pollen transfer.
... To artificially interrupt the continuous herkogamy variation in E. fischeriana, the floral carpophore was delicately leaned, and the gynophore was immobilized with a white thread to prevent further deflexion. According to the manipulations conducted by Ren and Bu (2014), one end of the thread was attached to the floral carpophore and the other end was attached to the gynophore through the area between two opposed petals. We disguised the threads to keep them out of the route of pollinators in order to reduce potential disturbance during insect visits. ...
Continuous variation in herkogamy has been well reported, however, less attention has been paid to the phenomena that the consecutive expression of two types of herkogamy in the same flower. Euphorbia fischeriana, which have both vertical and lateral herkogamy, show vertical herkogamy during the female phase. However, their gynophores bend to one side with the male phase and show lateral herkogamy. In this study, we observed the effect of successive sexual organs movement on variation in herkogamy traits. By artificially manipulating the flower to present gynophore straightened in the floral center or bend to one side, we attempted to investigate whether herkogamy movement affects pollinator access efficiency, pollen removal and deposition, and seed set ratio. Furthermore, we conducted artificial pollination in the female phase to evaluate the effect of changes in pollination environment on the variations in herkogamy traits. The results showed that gynophore straightened in female phase favors pollen deposition, whereas gynophore bending in male phase was conducive to the removal of pollen. Visitation frequency, pollen deposition and removal, and seed set ratio decreased significantly when the gynophore movement was manipulated. Finally, the bending of gynophore was obviously promoted by pollination. Therefore, the continuous variation of herkogamy in the same flower of E. fischeriana caused by the bending of the gynophore could improve the accuracy of pollination and avoid the interference of the ovary with access efficiency. That may be an adaptive strategy when pollinators are scarce. Furthermore, our study also provides good support for the hypothesis that variations in herkogamy traits are strongly selected by differences in pollination environments.
... Parnassia L. consists of small, glabrous and rosulate perennial herbs, with several morphologically distinguishable traits, including a solitary, terminal, bisexual and pentamerous flower borne on an unbranched scape; five showy staminodes; and one-by-one stamen movement (Ku 1987;Ku and Hultgård 2001;Sandvik and Totland 2003;Ren 2010;Armbruster et al. 2014;Ren and Bu 2014). Species of Parnassia predominantly occur in arctic and alpine regions of Europe, Asia, and North America with a center of diversification in mountainous areas in Pan-Himalaya and southwest China (Phillips 1982;Ku 1987;Ku and Hultgård 2001;Wu et al. 2003;Simmons 2004;Wu 2005). ...
Based on investigation of populations of Parnassia guilinensis and P. xinganensis , examination of herbarium specimens (including types), as well as consultation of protologues and distributions, P. guilinensis is hereby reduced to a synonym of P. xinganensis . P. xinganensis is endemic to northeastern Guangxi Province of China and characterized by having elliptic to ovate leaves and staminodes 3–5-branched with globose glands. Field photographs and an updated morphological description of P. xinganensis are provided.
... Parnassia has two diagnostic traits, i.e. five showy staminodes (Gu and Hultgård 2001, Sandvik and Totland 2003, Wu 2005 and one-by-one stamen movement (Gris 1868, Hultgard 1987, Ren 2010, Armbruster et al. 2014, Ren and Bu 2014. The shape and branching of the staminodes are the most important traits for the taxonomic treatment of Parnassia (Gu 1987, Gu and Hultgård 2001, Wu 2005. ...
... The shape and branching of the staminodes are the most important traits for the taxonomic treatment of Parnassia (Gu 1987, Gu and Hultgård 2001, Wu 2005. The distinctive mode of one-by-one stamen movement associated with sequential maturation of the anthers is thought to be an adaptation to increase pollen outputs under low insect visitation rates (Ren and Tang 2012, Armbruster et al. 2014, Ren and Bu 2014. ...
... Finally, cascade movement mechanisms (whether thigmonastic or not) often occur in combination with subsequent autonomous movements to avoid anther-anther interference during pollination (e.g. Parnassia 43 ; Ruta graveolens 32 ). Moreover, in the latter case all stamens repeat their movement towards the style simultaneously at the end of anthesis to ensure pollination through selfing as a backup mechanism 32 . ...
Obvious movements of plant organs have fascinated scientists for a long time. They have been studied extensively, but few behavioural studies to date have dealt with them, and hardly anything is known about their evolution. Here, we present a large experimental dataset on the stamen movement patterns found in the Loasaceae subfam. Loasoideae (Cornales). An evolutionary transition from autonomous-only to a combination of autonomous and thigmonastic stamen movement with increased complexity was experimentally demonstrated. We compare the stamen movement patterns with extensive pollinator observations and discuss it in the context of male mating behavior. Thigmonastic pollen presentation via stamen movements appears to be a crucial component of floral adaptation to pollinator behaviour, evolving in concert with complex adjustments of flower signal, reward and morphology. We hypothesize that rapid adjustments of pollen presentation timing may play a significant role in the diversificationof this plant group, representing a striking example for the evolutionary significance of plant behaviour.
... Recently, researchers have paid more attention to the phenomenon of 'male-male' interference, i.e. when one set of anthers gets in the way of disseminating pollen from another set of anthers. Ren and Bu (2014) provided direct experimental evidence for 'anther-anther interference' in angiosperms and showed its role in driving the evolution of floral traits, which had previously been ascribed to pollen dispensing mechanisms. However, the effects of male-female interference, i.e. the pistil interferes with disseminating pollen from the anthers by preventing the anther from touching a pollinator, or perhaps the anther prevents pollinator from depositing outcross pollen on the stigma, have been less well studied. ...
... However, the effects of male-female interference, i.e. the pistil interferes with disseminating pollen from the anthers by preventing the anther from touching a pollinator, or perhaps the anther prevents pollinator from depositing outcross pollen on the stigma, have been less well studied. It is likely that male-female interference may act as a selective force and needs to be considered when interpreting floral adaptation and evolution (Ren and Bu 2014). As stamen movements tend to result in movement herkogamy, they may decrease male-female interference by decreasing self-fertilization and increasing outcrossing . ...
... As stamen movements tend to result in movement herkogamy, they may decrease male-female interference by decreasing self-fertilization and increasing outcrossing . Therefore, in most cases, slow stamen movement has an important influence on both pollen export and reception (Ren and Bu 2014). Indeed, slow stamen movement, along with herkogamy or dichogamy, alters the overall pattern of reproduction. ...
Approximately 80 % of angiosperm species produce hermaphroditic flowers, which face the problem of male–male sexual interference (one or more anthers gets in the way of disseminating pollen from other anthers) or male–female sexual interference (the pistil interferes with disseminating pollen from the anthers by preventing the anther from touching a pollinator, or the anther prevents pollinator from depositing outcross pollen on the stigma). Slow stamen movement in hermaphrodite flowers has been interpreted as an adaptation for reducing male–male sexual interference. Using slow stamen movement in Lychnis cognata (Caryophyllaceae), this study presents new evidence that this phenomenon can reduce both male–male and male–female sexual interference. Ten stamens in L. cognata flowers vertically elongated their filaments in two batches and displayed similar patterns in pollen dispensing. More importantly, 10 stamens bend out of the floral centre by curving the filament also in 2 batches and pollen grains located at the flower centre displayed the highest viability. Thus, three stages of stamen movement can be identified, comprising two male stages (M1 and M2) and one female stage (F). We found that the main pollinator for L. cognata, Bhutanitis yulongensis (Papilionodae) generally preferred M1 flowers. Manipulation experiments show that vertical stamen movement enabled the anthers to dehisce at different times to prolong the presentation of pollen grains. Horizontal movement of the stamen decreased both male–male and male–female interference. However, vertical stamen movement had a minor role in increasing amount of pollen received by the stigma. This study provides the first direct experimental evidence of concurrent male–male and male–female interference in a flower. We suggest that the selection pressure to reduce such interference might be a strong force in floral evolution. We also propose that other selective pressure, including pollen dispensing mechanisms, pollen longevity, pollinator behaviour and weather, might contribute to floral evolution.
... When a flower was found to have an uplifted anther in the floral centre, the stamen was immobilized with a white thread to prevent subsequent deflexion. One end of the thread was bound to the joint between the filament and anther, and the other end was tethered to the pedicel through the space between two opposite petals, according to the manipulations piloted by Ren and Bu (2014). To minimize possible interference during insect visitation, we camouflaged the thread and petal and kept it outside the path of the floral visitors. ...
... Such stamen movement is similar to that observed in other Parnassia species, i.e. P. palustris (Sandvik and Totland 2003;Ren and Bu 2014) and P. epunctulata (Armbruster et al. 2014). Successive stamen movement in P. wightiana is thus characterized by two features: staggered stamen maturation and movement herkogamy. ...
... A recent study in the Parnassia species P. palustris demonstrated that one-by-one stamen movement could decrease 'anther-anther' interference by reducing the amount of pollen wasted in anthers (Ren and Bu 2014). However, such interference was not found in our study because the pollen removal rate was similar when one or two anthers were presented at once. ...
Successive stamen movement directly controls pollen presentation schedules through sequential stamen maturation and changes the extent of herkogamy by altering the positions of sexual organs. However, the implications of such movements in terms of pollination are not well understood. Pollen presentation theory predicts that staggered pollen presentation should be favoured when plants are subject to diminishing returns on pollen transfer. Herkogamy on the other hand, has been interpreted as an adaptive trait that reduces sexual interference in hermaphrodite flowers. In this study, we conducted floral manipulations to determine the function of successive stamen movement in pollen transfer. By artificially manipulating the flowers to present two anthers simultaneously in the floral centre, we attempted to investigate whether changes in the anther presentation strategy affect pollen removal, deposition and the efficiency of pollinators. Compared with the natural treatment, the pollen transfer efficiency of halictid bees decreased significantly when the flowers were manipulated to present two anthers simultaneously. Although the presentation of two anthers simultaneously led to a similar pollen removal rate, there was a significant reduction in pollen deposition on neighbouring stigmas. To evaluate the effect of movement herkogamy on pollen export and deposition and seed set, the flowers were manipulated with or without the movement of stamen bending out from the floral centre. Pollen export decreased significantly when the central anther was moved away from the pistil, and pollen deposition and seed set declined significantly when the five spent anthers were retained on the pistil. Our study provides good support for the pollen presentation theory and provides direct experimental evidence that successive stamen movement could increase pollen transfer efficiency by sequential stamen maturation. Moreover, movement herkogamy promotes pollen export, deposition and seed set, and could therefore be regarded as an effective mechanism to reduce interference between male and female functions.
... Many plants respond to external mechanical stimuli associated mainly to touch and vibration, which may occur in different parts of the plant (Braam 2005). On the flowers, these stimuli happen mainly on the stamens (Jaffe et al. 1977;Schlindwein and Wittmann 1997a, b;Ren and Bu 2014) and staminodia (Claßen-Bockhoff and Pischtschan 2000), and may affect the reproductive capacity of a plant (Braam 2005). In many flowers, the external stimuli are induced mainly by pollinators and the movement of these structures may induce co-adaptive processes involving touch-sensitive organs (thigmonastic or thigmotropic movement) and the behavior of the effective pollinators (see Romero and Nelson 1986;Schlindwein and Wittmann 1997a, b;Braam 2005;Cota-Sánchez et al. 2013). ...
Inducement to stamen movement by oligolectic bees has been reported for some Loasaceae species; however, detailed research studies on the pollination ecology of species in the genus Aosa are absent. In this study, we analyzed the floral biology and breeding system of Aosa rupestris (Hook.) Weigend, focusing on the role of pollinators in inducing stamens’ movements. We described the anthesis, the behavior of floral visitors, and carried out reproductive experiments in a population in a dry forest (“caatinga”) area in Northeastern Brazil. We carried out four experiments and one control to establish whether the interval between the movements of two successive stamens is regulated by pollinator visits. Anthesis lasted for 3–4 days. Stamens (102 ± 12.57) remained with closed anther inside petals early in the anthesis, after which they moved to the center of the flower and presented its pollen (male phase). After all stamens have reached the center of the flower, the female phase started. Bicolletes nordestina Urban, 2006 was the only floral visitor to A.
rupestris flowers, drinking nectar, collecting pollen, or sleeping on the flowers. Aosa
rupestris was autogamous, but fruit set was higher under natural conditions. The interval between movements of two successive stamens was not different among experiments. Therefore, stamen movements were spontaneous and did not respond to pollinator visits, in contrast to the pattern of stamen movements observed in other Loasaceae species. Although A. rupestris is autogamous, floral structure and behavior of the oligolectic bee pollinator ensured the highest level of fruit set in this species.
Paper highlights the new distributional record of Parnassia yui Z.P. Jien for India. Comments have been made on the possible threats and conservation status of a species.
