Floral morph composition and pollen limitation in the seed set of <Emphasis Type="Italic">Nymphoides indica</Emphasis> populations

We investigated the floral morph composition and seed set of the populations in a heterostylous aquatic plant, Nymphoides indica O. Kuntze (Menyanthaceae). The bias of floral morph ratio in the populations was negatively correlated with the seed set. In the populations with biased floral morph ratio, the pollen on the stigma of the common morphs were dominated by pollen of the same morph, resulting in reduced seed set. The addition of pollen of the opposite morph on the stigmas of the common morph resulted in an increase of fruit and seed set rates. The intermorph pollination rate and the fruit and seed set rates of Nymphoides indica were highest when two floral morphs were close in the populations. Various insect species including Lepidoptera, Diptera and Hymenoptera visited the flowers. However, geitonogamous pollination was common because of the short flying distance of the pollinators. These results indicate that the seed set of Nymphoides indica is limited by the shortage of compatible pollens and that the success of intermorph pollination is influenced by spatial distribution of the two floral morphs. As Nymphoides indica is endangered, conservation of the populations with high fecundity is proposed by us.     

Unravelling the stylar polymorphism in Melochia (Malvaceae): reciprocity and ancillary characters

Heterostyly is a genetic polymorphism in which plant populations possess two (distyly) or three (tristyly) morphs with flowers differing reciprocally in stigma and anther height. Sex organ deployment has been described as being highly variable among and within species of several distylous taxa belonging to different taxonomic groups. However, the number of studies considering within‐species disparities is still limited. For a better overview of the existing amount of variation that can occur within and between heterostylous species, we sampled 46 populations of six Melochia spp., a style‐polymorphic genus in Cuba. We characterized the floral morphology in all populations and described a set of ancillary characters per species. All of these Melochia spp. are distylous, except for the monomorphic M. nodiflora. The S‐morph produces fewer, larger pollen than L‐morphs, and has verrucose ornamentation. The L‐morph produces reticulate pollen and has larger stigmatic papillae than the S‐morph. The monomorphic M. nodiflora shows ancillary characteristics that are similar to the L‐morph individuals in the related species. As expected, there are differences in ancillary characters among species and also dissimilarities in reciprocity among and within species of Melochia. Our results highlight the importance of considering intraspecific variation in the morphometric characterization of heterostylous taxa. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 147–158.     

Three-dimensional reciprocity of floral morphs in wild flax (Linum suffruticosum): a new twist on heterostyly

Here, we studied the floral morphology and pollination of the distylous plant Linum suffruticosum (Linaceae) in southern Spain.We observed a previously unreported form of distyly that involved twisting and bending of styles and stamens during floral development to achieve three-dimensional reciprocity of anthers and stigmas in the long-styled (pin) and short-styled (thrum) morphs. This developmental pattern causes pin pollen to be placed on the underside of pollinating Usia flies (Bombyliidae), and thrum pollen to be placed on the top of the thorax and abdomen. The pin stigmas contact the flies on the dorsum, apparently picking up predominantly thrum pollen, and the thrum stigmas contact the flies on the ventral surface, apparently picking up predominantly pin pollen.This form of heterostyly would appear on morphological grounds to be far more efficient in dispersing pollen between compatible morphs than the typical pin-thrum system. If so, this plant fits Darwin's prediction of efficient pollen flow between heterostylous morphs more closely than anything Darwin himself reported.Molecular phylogenetic analyses indicate that this form of heterostyly evolved in a lineage that already had typical heterostyly. The analyses also indicate that there have been several independent origins of heterostyly in Linum and at least one reversal to stylar monomorphism.     

桂林唇柱苣苔和百寿唇柱苣苔的开花动态及花粉活力和柱头可授性的比较

对桂林唇柱苣苔的两个居群(YZ居群和DB居群)和百寿唇柱苣苔的开花动态、花粉活力和柱头可授性进行了比较研究。结果表明,桂林唇柱苣苔的两个居群花期、单花持续期存在明显差异,DB居群的花期较YZ居群晚,但花期长于后者。YZ居群的花期、单花持续期与百寿唇柱苣苔的花期、单花持续期相近。三者开花过程相似。花粉活性和柱头可授性达最大的时间、持续时间在桂林唇柱苣苔的两个居群以及百寿唇柱苣苔之间具有明显差异。     

Pollinator shifts and the loss of style polymorphism in Narcissus papyraceus (Amaryllidaceae)

Darwin proposed that the driving force for the evolution of style polymorphisms is the promotion of cross‐pollination between style morphs, through accurate placement of pollen on the pollinator’s body. This hypothesis has received much attention, but the effect of different pollinators in the fitness of morphs remains poorly understood. Narcissus papyraceus is a style dimorphic species (long ‐L‐ and short ‐S‐ styled) with isoplethic (1 : 1) and L‐monomorphic populations, mainly visited by long‐tongued (LT) nocturnal and short‐tongued (ST) diurnal pollinators, respectively. We studied natural female fertility of morphs, and assessed the role of diurnal and nocturnal pollinators. We also quantified female fertility of the morphs in experimental populations with different morph ratio, exposed to predominately long‐ or short‐tongued pollinators. We found that with LT pollinators, both morphs were successfully pollinated in all morph ratio conditions, suggesting that these insects could be involved in maintenance of the polymorphism, although other factors may also play a role. However, with ST pollinators, S‐plants displayed less fertility than L‐plants, and mating among L‐plants was favoured, implying that the polymorphism is lost. These results underscore the role of pollinators on variations in style polymorphism.     

Individual bee foragers are less-efficient transporters of pollen for plants from which they collect the most pollen in their scopae

Premise

Bees provision most of the pollen removed from anthers to their larvae and transport only a small proportion to stigmas, which can negatively affect plant fitness. Though most bee species collect pollen from multiple plant species, we know little about how the efficiency of bees' pollen transport varies among host plant species or how it relates to other aspects of generalist bee foraging behavior that benefit plant fitness, such as specialization on individual foraging bouts.

Methods

We compared the pollen collected and transported by three bee species for 46 co-occurring plant species. Specifically, we compared the relative abundance of pollen taxa in the individual bees' scopae, structures where bees store pollen to provision larvae, with the relative abundance of pollen taxa on the rest of bees' bodies, which is more likely to be transferred to stigmas.

Results

Bees carried five times more pollen grains in their scopae than elsewhere on their bodies. Within foraging bouts, bees were relatively specialized in their pollen collection, but transported proportionally less pollen for the host plants on which they specialized. Across foraging bouts, two bee species transported proportionally less pollen for some of their host plants than for others, though differences didn't consistently follow the same trend as at the foraging bout scale.

Conclusions

Our results suggest that foraging-bout specialization, which is known to reduce heterospecific pollen transfer, also results in less-efficient pollen transport. Thus, bee foragers that visit predominantly one plant species may have contrasting effects on that plant's fitness.

     

Heterostyly promotes compatible pollination in buckwheats: Comparisons of intraflower,intraplant, and interplant pollen flow in distylous and homostylous Fagopyrum

Premise of the Study

Heterostyly, the reciprocal positioning of stigmas and anthers in different floral morphs, has long been thought to promote intermorph pollination. However, extensive intramorph pollination occurs commonly in heterostylous species, leading to recurrent questions about the functional and evolutionary significance of heterostyly.

Methods

To identify the sources of stigmatic pollen (autogamous [intraflower], geitonogamous [intraplant], vs. interplant), we emasculated either one flower or entire plants in experimental populations of the two closely related buckwheat species, distylous Fagopyrum esculentum and homostylous F. tataricum. Differences in pollen size allowed unambiguous identification of pollen on stigmas.

Results

Only 2.4% of F. tataricum pollen and 1.5% of F. esculentum pollen arrived successfully on compatible stigmas of other plants. In the former (homostylous) species, 71.3% of the pollen load on stigmas was autogamous, 10.8% was geitonogamous, and 17.9% was interplant. In the latter (distylous) species, 37.45% of the pollen on stigmas was autogamous, 13.8% was geitonogamous, 17.0% was intramorph, and 31.75% was intermorph. The amount of incompatible pollen arriving on stigmas was greatly decreased by both one‐flower and whole‐plant emasculations, and thus, the proportion of compatible pollen deposited increased with one‐flower emasculation and increased even more with whole‐plant emasculation.

Conclusions

Our quantification of pollen‐donor sources in these two species indicated that heterostyly in Fagopyrum esculentum provided a nearly 2‐fold fitness advantage (in terms of compatible pollination) over expected (random) pollen transfers between morphs. Because of reduced herkogamy, the homostylous F. tataricum was highly autogamous.     

开花式样对传粉者行为及花粉散布的影响

理解植物花的特征可以从单花特征和群体特征两个层次入手。开花式样是植物的花在群体上的特征体现, 通过在开花数目、开花类型以及花的排列上的变化, 不同的开花式样对传粉者具有不同的吸引力, 影响昆虫在植株上的活动, 使花粉运动的方向发生相应变化, 从而影响着植物最终的交配结果。此外开花式样随环境改变也会发生一些变化。本文介绍了开花式样研究的进展, 对开花数目、开花类型以及花的排列等3个方面的已有研究进行了分别阐述, 并提出开花式样研究应更多地考虑影响传粉的各种因素。     

Seasonal changes in pollen limitation and femaleness along the snowmelt gradient in a distylous alpine herb,Primula modesta

Flowering phenology of alpine plants is strongly determined by the timing of snowmelt, and the conditions of pollination of widely distributed plants vary greatly during their flowering season. We examined the reproductive success of the distylous alpine herb, Primula modesta, along the snowmelt gradient under natural conditions, and compared it with the result of artificial pollination experiments. In addition, the compositions and visit frequencies of pollinators to the flower of P. modesta were examined during the flowering period. The pin and thrum plants of P. modesta growing at the same site have an equal ability to produce seeds if a sufficient amount of legitimate pollen grains are deposited on the stigma surface. However, under natural conditions, their seed‐set success was often (even if not always) restricted by pollen limitation, and the functional gender of the pin and thrum plants biased to the female and male, respectively, associated with their growing sites. These variations were not ascribed to resource limitation nor biased morph ratio but to the seasonal changes in pollination situations, a replacement of pollinator types from long‐ to short‐tongued pollinators resulted in unidirectional pollen transfer from long stamens (thrum plants) to long styles (pin plants). The functional gender specialization may enhance the evolution of dioecy from heterostyly, but the severe pollen limitation may cause the breakdown of heterostyly into homostyly. To consider the evolutionary pathway of heterostylous plants, an accumulation of the empirical data is required demonstrating how phenological synchrony between plants and pollinators is decided and to what degree this relationship is stable over years, along with estimates of selection and gene flow in individual plants.     

Relationship of stigma behaviors and breeding system in three Mazus (Phrymaceae) species with bilobed stigma

Sensitive stigma has been recognized to facilitate outcrossing. We hypothesized that species with different levels of sensitivity might have corresponding differences in components of their breeding system. In this study, three Mazus species with bilobed stigmas were used to test the hypothesis. We explored stigma behaviors of the species in reaction time, recovery time, permanent closing time, and the minimum pollen load causing permanent closure. We investigated floral traits, pollinator type and behavior, pollination intensity, and natural schedule of pollen deposition on stigma. Moreover, we evaluated the mating system of the species by checking seed set after controlled pollination treatments, namely, natural flowers with open pollination, enclosed flowers without pollination, and enclosed flowers with self and outcross hand pollination. Results indicated that stigma of M. pumilus (N. L. Burman) Steenis was not sensitive, whereas stigmas of M. miquelii Makino and M. stachydifolius (Turcz.) Maxim. closed and reopened quickly in response to pollination. Accordingly, hand pollination treatments revealed that seed set of self-spontaneous pollination in M. pumilus was similar to the other treatments. For M. miquelii, outcross pollen resulted in significantly higher seed set than self-pollen.Mazus stachydifolius was self-incompatible. Additionally, the corresponding characteristics in other components of the breeding system for each species were found. Our study indicated that the sensitivity of bilobed stigma might be linked with floral traits and the mating system in a given species. Sensitive stigma should be regarded as an evolutionary mechanism for enhancement of outcrossing.     

Crane flies and microlepidoptera also function as pollinators in Epidendrum (Orchidaceae: Laeliinae): the reproductive biology of E. avicula

Crane flies and microlepidoptera have been recorded as pollinators in unrelated orchid groups, but these insects have never been recorded in Epidendroideae, the most species‐rich orchid subfamily, which includes one of the most diverse genera among Orchidaceae, Epidendrum. Based on data on phenology, floral morpho‐anatomy, pollinators, pollination mechanisms and breeding system, the reproductive biology of E. avicula was studied in south‐eastern Brazil. Epidendrum avicula possess osmophores that produce a citric fragrance at night. The flowers attract Tipulidae flies and several families of microlepidoptera that drink the nectar produced in a tube formed by the adnation of the labellum and column. As is common in Epidendrum, after removing the pollinarium, both crane flies and micro‐moths get trapped by the proboscis, which frightens the insects and inhibits any possible intent to immediately visit another flower. The behavior of the pollinators on flowers, plus the retention of the anther cap by the pollinarium, results in a reduction in the occurrence of geitonogamy. Because E. avicula is self‐incompatible, the consequence of pollinator behavior and the floral mechanisms tend to reduce the pollen loss. As far as we know, this is the first study to report the reproductive biology of a species of Epidendroideae pollinated by crane flies and microlepidoptera. Based on more recent concepts of plant–pollinator interactions, although E. avicula is pollinated by several species belonging to two distinct orders, suggesting an unspecialized pollination system is involved, nectar‐seeking microlepidoptera and Tipulidae flies can be recognized as a single functional group.     

Pollination biology of Paeonia jishanensis T. Hong & W.Z. Zhao (Paeoniaceae), with special emphasis on pollen and stigma biology

The endangered wild tree peony. Paeania jishanensis T. Hong & W. Z. Zhao (formerly P. suffruticosa Andr. ssp. spontanea (Rehd.) S.G. Haw & L. A. Lauener) is one of the most important ancestral stocks of cultivated tree peony, P. suffruticosa Andr. Study of the natural population atjishan, Shanxi Province revealed that the seed set was very low (2.1 seeds per carpel). The low seed set should not be attributed to viable pollen limitation because the plant produces a great quantity of pollen and 36–75% of pollen is TTC-tested viable. Stigmas became receptive almost one day after the flower opened, and receptivity lasted for several days. All the stigmas were sufficiently pollinated, and pollen germinated readily on the wet crest of stigmas irrespective of whether cross pollen or self pollen was used. Hand-pollination showed that this plant was self-incompatible. No seed was harvested after self-pollination, while cross-pollination yielded 2.4 seeds per carpel. Many pollen tubes were recorded in the stigma but extremely few in the ovary chamber. This phenomenon indicated diat the self-incompatible system was activated when pollen tubes reached the ovary wall.     

Stylar polymorphism on the edge: unusual flower traits in Moroccan Narcissus broussonetii (Amaryllidaceae)

Heterostyly and related polymorphisms (e.g. stigma‐height dimorphism) have been used as model systems for studying the origin and maintenance of plant population variability. Stigma‐height dimorphism frequently occurs in Narcissus and is associated with a particular flower shape. In the present study, we describe a new, peculiar case of stigma‐height dimorphism in Narcissus broussonetii, a species on the margin of the geographical distribution of the genus. We determined the stylar condition of N. broussonetii and its variation across populations, analyzed perianth morphology and its relationship with stylar variation, and compared this species with other stylar dimorphic species of the genus. We also studied the incompatibility system and pollination ecology of the species. Narcissus broussonetii is a style‐dimorphic species, as suggested in early studies that were subsequently neglected, and displays unusual flower morphology, with a long floral tube and a virtual absence of a corona. The species shows a late‐ (ovarian) acting incompatibility system and crosses within and between morphs are fertile. We observed short‐tongued diurnal and long‐tongued nocturnal pollinators. Our findings confirm that the presence of the observed dimorphism across populations is most probably the result of the joint action of a nonheteromorphic incompatibility system, extremely long and narrow floral tubes, and a combined role of short‐ and long‐tongued pollinators. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177 , 644–656.     

Heteromorphic incompatibility and efficiency of pollination in two distylous Pentanisia species (Rubiaceae)

BACKGROUND AND AIMS: Distyly has been hypothesized to promote cross-pollination by reducing intrafloral and geitonogamous self-pollination, and enhancing intermorph pollination. Distylous plants typically display both reciprocal herkogamy and a heteromorphic incompatibility system, which allows mating only between morphs. Distyly and its pollination consequences were examined in two Pentanisia species with long-tubed flowers which are pollinated almost exclusively by butterflies. METHODS: Anther and stigma heights were measured to quantify reciprocal herkogamy. The type of incompatibility system was determined by observing pollen tubes and seed production following controlled hand pollination. Pollen loads on pollinators and stigmas were also examined to assess the efficiency of intermorph pollen flow. KEY RESULTS: Pentanisia prunelloides and P. angustifolia exhibit reciprocal herkogamy and a host of ancillary dimorphisms, including pollen colour, exine sculpturing, stigmatic papilla shape and floral-tube pubescence. Controlled hand-pollinations revealed the presence of a strong heteromorphic incompatibility system in both species. The site of incompatibility differed between the morphs; intramorph pollen tubes were blocked in the style of the short-styled morph and on the stigmatic surface of the long-styled morph. Butterflies carried pollen from the short- and long-styled morphs primarily on their head and proboscis, respectively. Natural pollination resulted in a higher proportion of pollen transfer from long- to short-styled plants than vice versa. Nevertheless, fruit set did not differ between morphs. CONCLUSIONS: Both Pentanisia species are fully distylous. Reciprocal herkogamy results in pollen from the two morphs being carried on different locations on pollinators' bodies, which in turn promotes intermorph pollination. Intramorph pollination does not result in fertilization, because of an effective heteromorphic incompatibility system.