WHY HERMAPHRODITIC PLANTS PRODUCE MANY MORE FLOWERS THAN FRUITS: EXPERIMENTAL TESTS WITH AGAVE MCKELVEYANA

Five hypotheses explaining the low fruit-to-flower ratios in self-incompatible hermaphroditic plants are tested for Agave mckelveyana. Results from pruning, bagging, and hand-pollination experiments indicate that “excess” flowers (i.e., flowers that fail to produce mature fruits) do not contribute to female fitness (i.e., fruit or seed production). These flowers are aborted regardless of their pollination history. Additional data on nectar production imply that these flowers act as pollen donors and contribute to male fitness.     

Sexual dimorphism in pollen grain size in cryptically dioecious Thalictrum macrostylum

While several plant species are initially described as androdioecious, upon more thorough investigation, many of these are found to be cryptically dioecious with functionally male flowers and perfect flowers that produce inaperturate pollen or are otherwise functionally female on separate plants. The change in function of pollen produced by perfect flowers opens up the possibility for the evolution of sexual dimorphism in pollen grain size. We found that Thalictrum macrostylum (Ranunculaceae) is cryptically dioecious, and produces apparently inaperturate pollen in perfect flowers. In four field sites throughout North Carolina, inaperturate grains are larger than grains from staminate flowers and also show a greater variance in size. We also found substantial variation in pollen grain size among plants. The sites with lower soil nutrient content also had smaller pollen grains of both types, although local adaptation or genetic drift may also be causing among-site variation.     

BUMBLE BEE POLLINATION AND FLORAL MORPHOLOGY: FACTORS INFLUENCING POLLEN DISPERSAL IN THE ALPINE SKY PILOT,POLEMONIUM VISCOSUM (POLEMONIACEAE)

Pollen dispersal success in entomophilous plants is influenced by the amount of pollen produced per flower, the fraction of pollen that is exported to other flowers during a pollinator visit, visitation frequency, and the complementarity between pollen donor and recipients. For bumble bee-pollinated Polemonium viscosum the first three determinants of male function are correlated with morphometric floral traits. Pollen production is positively related to corolla and style length, whereas pollen removal per visit by bumble bee pollinators is a positive function of corolla flare. Larger-flowered plants receive more bumble bee visits than small-flowered individuals. We found no evidence of tradeoffs between pollen export efficiency and per visit accumulation of outcross pollen; each was influenced by unique aspects of flower morphology. Individual queen bumble bees of the principal pollinator species, Bombus kirbyellus, were similar in male, female, and absolute measures of pollination effectiveness. An estimated 2.9% of the pollen that bumble bees removed from flowers during a foraging bout was, on average, deposited on stigmas of compatible recipients. Significant plant-to-plant differences in pollen production, pollen export per visit, and outcross pollen receipt were found for co-occurring individuals of P. viscosum indicating that variation in these fitness related traits can be seen by pollinator-mediated selection.     

Morning floral heat as a reward to the pollinators of the Oncocyclus irises

Relationships between flowering plants and their pollinators are usually affected by the amount of reward, mainly pollen or nectar, offered to pollinators by flowers, with these amounts usually positively correlated with floral display. The large Oncocyclus iris flowers, despite being the largest flowers in the East Mediterranean flora, are nectarless and have hidden pollen. No pollinators visit the flowers during daytime, and these flowers are pollinated only by night-sheltering solitary male bees. These iris flowers are partially or fully dark-colored, suggesting that they gather heat by absorbing solar radiation. Here we test the hypothesis that the dark-colored flowers of the Oncocyclus irises offer heat reward to their male solitary bee pollinators. Floral temperature was higher by 2.5°C than ambient air after sunrise. Solitary male bees emerged earlier after sheltering in Oncocyclus flowers than from other experimental shelter types. Pollination tunnels facing east towards the rising sun hosted more male bees than other aspects. We suggest that floral heat reward can explain the evolution of dark floral colors in Oncocyclus irises, mediated by the pollinators’ behavior.     

The dynamics of pollen removal and deposition,and its effects on sexual phases in a protandrous plant: Glechoma longituba (Lamiaceae)

The duration of sexual phases in dichogamous plants are affected by many factors. Using both experimental and observational studies, we investigated natural patterns of pollen removal and deposition, visiting frequency of pollinators, patterns of nectar secretion, and effects of pollen removal and stigmatic pollen deposition on the duration of sexual phases in a protandrous plant, Glechoma longituba. We found that visiting frequency of pollinators correlated with the nectar secretion pattern. The nectar volume during the male phase was higher than during the female phase. In the morning, the main pollinator, the bee Anthophora plumipes, mainly foraged for nectar and showed no preference for flowers in male or female phase, despite male phase flowers producing higher amounts of nectar. However, in the afternoon, they changed their behavior and foraged mainly for pollen, and then showed a preference for flowers in male phase. Furthermore, the rates of pollen removal and stigmatic pollen deposition can affect the starting time and the duration of the female phase. When pollen removal and pollination rates are low due to scarcity of pollinator services, the sexual phase can be prolonged, leading to an overlap, and thereby enhance the chance for sexual reproduction through pollinator‐facilitated self‐pollination. We consider the variation of sexual phases in Glechoma longituba an adaptive mechanism prepared for both cross‐pollination enhancement and reproductive assurance depending on the available pollination services.     

Morphological variation in the flowers of Jacaratia mexicana A. DC. (Caricaceae), a subdioecious tree

The Caricaceae is a small family of tropical trees and herbs in which most species are dioecious. In the present study, we extend our previous work on dioecy in the Caricaceae, characterising the morphological variation in sexual expression in flowers of the dioecious tree Jacaratia mexicana . We found that, in J. mexicana , female plants produce only pistillate flowers, while male plants are sexually variable and can bear three different types of flowers: staminate, pistillate and perfect. To characterise the distinct types of flowers, we measured 26 morphological variables. Our results indicate that: (i) pistillate flowers from male trees carry healthy-looking ovules and are morphologically similar, although smaller than, pistillate flowers on female plants; (ii) staminate flowers have a rudimentary, non-functional pistil and are the only flowers capable of producing nectar; and (iii) perfect flowers produce healthy-looking ovules and pollen, but have smaller ovaries than pistillate flowers and fewer anthers than staminate flowers, and do not produce nectar. The restriction of sexual variation to male trees is consistent with the evolutionary path of dioecy from hermaphrodite ancestors through the initial invasion of male-sterile plants and a subsequent gradual reduction in female fertility in cosexual individuals (gynodioecy pathway), but further work is needed to confirm this hypothesis.     

Inbreeding depression affects pollen performance in Cucurbita texana

Most studies of the effects of inbreeding focus on vegetative vigor and reproductive output through the female (fruit and seed) function. This study not only examines the effects of inbreeding on the female function but it also examines the effects of inbreeding on pollen performance both in vitro and in vivo. This study used Cucurbita texana, a wild gourd, and was performed under field conditions. In vivo performance was assessed by placing equal amounts of pollen from either the inbred or outcrossed plants onto a stigma together with pollen from a tester line. As with other studies, we found that outcrossed plants had greater reproductive output (male flowers and fruits) than plants produced from self pollinations. Unlike most studies of inbreeding depression, which mostly ignore the male function of plants, we also found that the pollen produced by outcrossed plants had faster pollen tube growth in vitro than the pollen produced on selfed plants. Moreover, pollen from selfed plants sired significantly fewer seeds than pollen from outcrossed plants under conditions of pollen competition (i.e. the number of pollen grains deposited onto the stigmas was larger than the number of available ovules). These findings indicate that inbreeding affects the performance of the resulting sporophytic generation and the microgametophytes they produce.     

Extremely high proportions of male flowers and geographic variation in floral ratios within male figs of Ficus tikoua despite pollinators displaying active pollen collection

Most plants are pollinated passively, but active pollination has evolved among insects that depend on ovule fertilization for larval development. Anther‐to‐ovule ratios (A/O ratios, a coarse indicator of pollen‐to‐ovule ratios) are strong indicators of pollination mode in fig trees and are consistent within most species. However, unusually high values and high variation of A/O ratios (0.096–10.0) were detected among male plants from 41 natural populations of Ficus tikoua in China. Higher proportions of male (staminate) flowers were associated with a change in their distribution within the figs, from circum‐ostiolar to scattered. Plants bearing figs with ostiolar or scattered male flowers were geographically separated, with scattered male flowers found mainly on the Yungui Plateau in the southwest of our sample area. The A/O ratios of most F. tikoua figs were indicative of passive pollination, but its Ceratosolen fig wasp pollinator actively loads pollen into its pollen pockets. Additional pollen was also carried on their body surface and pollinators emerging from scattered‐flower figs had more surface pollen. Large amounts of pollen grains on the insects' body surface are usually indicative of a passive pollinator. This is the first recorded case of an actively pollinated Ficus species producing large amounts of pollen. Overall high A/O ratios, particularly in some populations, in combination with actively pollinating pollinators, may reflect a response by the plant to insufficient quantities of pollen transported in the wasps’ pollen pockets, together with geographic variation in this pollen limitation. This suggests an unstable scenario that could lead to eventual loss of wasp active pollination behavior.     

SEX EXPRESSION,BREEDING SYSTEM,AND POLLEN BIOLOGY OF RICINOCARPOS PINIFOLIUS: A CASE OF ANDRODIOECY?

A population of 54 Ricinocarpos pinifolius (Euphorbiaceae) plants contained male plants, which produced only staminate flowers, and hermaphrodites, which produced staminate and pistillate flowers. The fraction of pistillate flowers ranged continuously from 0 to 0.68. Insect pollination was effective and fruit set virtually complete except for losses to herbivores. Self pollen, outcross pollen from male plants, and outcross pollen from hermaphrodites were all equivalent in viability, germination, tube growth, ovule penetration, and fruit setting ability. Inbreeding depression was manifested as late abortion of some selfed seeds. Geitonogamous selfing is largely prevented by temporal separation of male and female functions within plants. This temporal separation, combined with population-wide synchrony of flowering, may create unusual conditions allowing male plants at low frequency to match hermaphrodites in reproductive success.     

Gender specialization in <Emphasis Type="Italic">Palicourea demissa</Emphasis> (Rubiaceae), a distylous,hummingbird-pollinated treelet

Distyly has been interpreted as a mechanism that promotes cross-pollination among conspecific plants and as one of the routes leading to the evolution of dioecy. In one of the possible evolutionary pathways, pollinators may disrupt intermorph pollen flow, and, as a consequence, floral morphs may gradually specialize as either male or female (functional dioecy). Natural patterns of pollen deposition and fruit and seed production were estimated in Palicourea demissa (Rubiaceae) and used as parameters to assess functional gender differences between floral morphs. Pollen flow was asymmetrical in P. demissa. Long-styled flowers were more effective than short-styled flowers in pollen deposition towards compatible stigmas, whereas short-styled flowers were more effective in legitimate pollen receipt. Accordingly, short-styled plants produced more fruits and viable seeds than long-styled plants. The contributions of male and female function to the potential functional gender were equivalent in both morphs. However, the realized functional gender deviated significantly from the potential functional gender in both morphs, in which short-styled plants were more successful through their female function, but long-styled plants through their male function. If pollinators disrupt the complementarities of pollen transfer between the two morphs (asymmetric pollen flow), the expression of a more profitable gender is expected in each morph. Thus, our results support the hypothesis that dioecy may evolve in distylous populations through the gradual specialization of each morph as either male or female.     

Reproductive biology ofCistus ladanifer (Cistaceae)

The phenology, major floral characteristics, fruiting levels, and breeding system ofCistus ladanifer L. (Cistaceae), a common western Mediterranean shrub species, were studied in a southern Spanish population. The white, large (64 mm in diameter) flowers of this shrub appear during spring (March–May) and produce abundant pollen and nectar. In the year of study, flowers lasted up to three days, during which they were visited by a diverse array of insects including beetles, flies, and bees. Hand-pollinations revealed that flowers do not set any seed unless cross pollen is applied to the stigma. Microscopical observations indicate that self pollen tubes grow down the stigma but invariably fail to induce fruit maturation. At the plant level, all estimates of fecundity investigated (number of seeds per capsule, proportion of ovules developing into seed, and proportion of flowers setting fruit) were highly dependent on nearest neighbour distance, with isolated plants setting as little as 0% fruit. In contrast, plants within a clump often transformed into fruit as much as 90% of the flowers. At the population level, seed output was estimated to range between 3,000 and 270,000 seeds per plant during 1991.     

Adaptive function of duodichogamy: Why do chestnut trees have two pollen emission phases?

Premise

Intersexual mating facilitation in flowering plants has been largely underexplored. Duodichogamy is a rare flowering system in which individual plants flower in the sequence male-female-male. We studied the adaptive advantages of this flowering system using chestnuts (Castanea spp., Fagaceae) as models. These insect-pollinated trees produce many unisexual male catkins responsible for a first staminate phase and a few bisexual catkins responsible for a second staminate phase. We hypothesized that duodichogamy increases female mating success by facilitating pollen deposition on stigmas of the rewardless female flowers through their proximity with attractive male flowers responsible for the minor staminate phase.

Methods

We monitored insect visits to 11 chestnut trees during the entire flowering period and explored reproductive traits of all known duodichogamous species using published evidence.

Results

In chestnuts, insects visited trees more frequently during the first staminate phase but visited female flowers more frequently during the second staminate phase. All 21 animal-pollinated duodichogamous species identified are mass-flowering woody plants at high risk of self-pollination. In 20 of 21 cases, gynoecia (female flower parts) are located close to androecia (male flower parts), typically those responsible for the second minor staminate phase, whereas androecia are often distant from gynoecia.

Conclusions

Our results suggest that duodichogamy increases female mating success by facilitating pollen deposition on stigmas by means of the attractiveness of the associated male flowers while effectively limiting self-pollination.

     

The effects of the floral infection by a bacterial pathogen in a dioecious plant,Mallotus japonicus (Euphorbiaceae)

Among all the different organs of a plant, flowers might have one of the most dynamic microbial communities, since many microbes are transmitted during flowering by insects and pollen. However, little is known about how these microbes affect floral characteristics and plant reproduction. Among the microbes transmitted to flowers, pathogens may have highly negative effects on plants' fitness. In this study, we investigated whether a bacterial pathogen, Erwinia mallotivora, occurs on flowers of the host plant Mallotus japonicus, and whether the transmission of the pathogen to flowers can result in systemic infection and/or reduction of fruit production. The pathogen has been reported to infect through leaves, while its ecology on flowers is unknown. We first confirmed the presence of the pathogen on flowers, indicating possible transmission by visitors or pollen. Then, we showed that the bacteria can infect the plant through flowers by inoculating the pathogen to both male and female flowers. Interestingly, the symptoms on leaves appeared earlier on the female plants than on the males. Besides, the inoculation significantly decreased fruit set of the female plants. Our results suggest a higher cost of infection in a female than in a male once the pathogen infected flowers. Although the effects of pathogen infection to flowers have rarely investigated in wild plants, it would be an interesting topic for future study if such sexual differences in the infection cost can cause sexual conflict and intraspecific adaptation load.     

Effects of pollination intensity on the vigor of the sporophytic and gametophytic generation of Cucurbita texana

 We examined the effects of pollen competition (pollen load size) on sporophytic vigor and gametophytic performance in Cucurbita texana, a wild gourd, while controlling for alternative interpretations of the data. Under field conditions we compared the vigor of progeny produced from large and small pollen loads and examined the in vitro performance of the pollen produced by the progeny. We found that the progeny from large pollen loads germinated faster and had a greater reproductive output (male flowers and fruits) than progeny produced from small pollen loads. In addition, we found that the pollen produced on plants derived from large pollen loads grew faster in vitro than the pollen produced on plants derived from small pollen loads. These findings indicate that pollen competition affects the performance of the resulting sporophytic generation and the microgametophytes they produce. Received: 26 January 1997 / Revision accepted: 25 June 1997     

The Effects of Inflorescence Size and Flower Position on Biomass and Temporal Sex Allocation in <Emphasis Type="Italic">Lobelia sessiliflora</Emphasis>

To test the prediction of sex allocation theory that plants or flowers high in resource status emphasize the female function, we explored the variation in both biomass (the number of pollen grains and ovules) and temporal (male and female durations) sex allocation among and within plants of protandrous Lobelia sessilifolia in relation to plant size and flower position within plants. Among plants, the mean number of pollen grains and ovules per flower of a plant increased with plant size, whereas the mean P/O ratio (number of pollen grains/number of ovules ratio) decreased with plant size. The mean male duration, the mean female duration, and the mean ratio of male duration/flower longevity per flower of a plant were not correlated with plant size. Thus, large plants emphasized female function in terms of biomass sex allocation, which is consistent with the prediction of size-dependent sex allocation theory. The results for temporal sex allocation, however were inconsistent with the theory. Within plants, the mean number of pollen grains and ovules per flower at each position decreased from lower to upper flowers (early to late blooming flowers) and that of the P/O ratio increased from lower to upper flowers. The mean male duration and the mean female duration per flower decreased from lower to upper flowers, whereas the mean ratio of male duration/flower longevity increased from lower to upper flowers. The population sex ratio changed from male-biased to female-biased. Thus, later blooming flowers emphasized the male function in terms of both biomass and temporal sex allocation, consistent with the sex allocation theory, regarding the change in the population sex ratio.     

Isolated pollen culture in tobacco: plant reproductive development in a nutshell

Summary In the past, in vitro cultures of excised anthers and isolated pollen have been used to study normal male sexual development (gametophytic development) and, conversely, to produce and study haploid plant formation (sporophytic development). For years both branches have existed side by side, without much interaction. Today, a synthesis of the two branches is possible as well as necessary. Recent advances in the technique of isolated pollen culture in the tobacco plant model (Nicotiana tabacum L.) enable the researcher to strictly control pollen development in both the gametophytic and sporophytic direction. The nutritional status of the immature pollen grain at a particular stage of development provides the trigger for its development into one of the two phases found in the alternation of generations undergone by higher plants. In particular, a hunger signal is responsible for the derepression of cell division activity and the start of embryogenesis. Pollen starvation can occur in isolated pollen cultures in sucrose-free media, in excised anthers and flowers, and, under specific growth conditions, during pollen development in vivo.     

POLLINATION OF RAFFLESIA (RAFFLESIACEAE)

The genus Rqfflesia includes about 13 species of parasitic flowering plants, among which are the largest known flowers. The flower with subtending scales is the only part of the plant external to the host and is produced solitary on roots (rarely stems) of the genus Tetrastigma (Vitaceae). Field studies were made of the pollination process in R. pricei, a species endemic to the Crocker Range in the Malaysian state of Sabah (northern Borneo). Pollination is mediated by carrion (bluebottle) flies of the genera Lucilla and Chrysomya. Experimental data indicate that both visual and olfactory cues are important in attracting flies to flowers. Flies (mostly female L. papuensis) obtain loads of the viscous liquid pollen matrix by visiting male flowers and entering anther grooves on the central column of the flower, precisely guided by ridges armed with hairs that force the fly into a position in which the pollen is positioned on the dorsal part of the thorax. “Windows” on the inside of the perigone diaphragm apparently help orient their flight inside flowers. Pollen-loaded flies visiting female flowers may enter the infradiscoidal sulcus formed by a broad ring of stigmatic tissue above and the expanded base of the column below. On entering the sulcus the fly is wedged in so tightly that pollen is rubbed off the thorax onto the stigma. Only large flies could be effective in picking up pollen from male flowers and transferring it to female flowers. The pollination syndrome is sapromyophily, in which the flower closely parallels trap flowers of several other plant families, although it is not a trap. The flower provides no reward for pollinators but deceives them by an apparent offering of food and possibly brood place. Rafflesia plants are extremely rare, perhaps in part because of infrequency of pollination, which requires neighboring male and female flowers simultaneously in bloom.     

THE BREEDING SYSTEM OF OXALIS SUKSDORFII

The Pacific Coast species Oxalis suksdorfii (section Corniculatae) is morphologically tristylous. Flowers of the 3 kinds of plants present in natural populations differ in style length, stamen length, pollen size, stigma size and orientation, and stylar pubescence. Experimental studies and field observations indicate that plants with long-styled flowers are weakly self-compatible and show little differentiation in size or compatibility relationships of pollen from the 2 sets of stamens. Plants with mid-styled flowers have strongly differentiated pollen, but produce few capsules or seed after any artificial or natural pollinations. Plants with short-styled flowers are self-incompatible and show slight pollen differentiation. The data presented suggest that O. suksdorfii approaches functional dimorphism since the mid-styled form contributes little pollen and few seeds in sexual reproduction. The species may be in the process of losing the mid-styled form completely and provides a model of certain physiological and morphological changes which may have accompanied elimination of the mid-styled form in other Oxalis species. The abundance of plants with mid-styled flowers in natural populations suggests, however, that this form may be retained because it contributes to general population fitness, or because the genetic control of heterostyly in this species prevents its elimination.     

Interaction between floral color change and gender transition in the protandrous weed Saponaria officinalis

Natural selection has directed the evolution of floral traits so that pollinator visits are manipulated to maximize the fitness of individual plants by directing which other individual sires its seeds. In some plants, flowers change color over time and may have the ability to direct pollinators to rewarding flowers. In addition, by varying when pollen is available and when stigmas are receptive, protandrous plants can show variation in selfing rates. In this study, the association between color change and gender transition in flowers of Saponaria officinalis was examined. Anthocyanins were extracted from flowers of each gender stage to measure color using spectrophotometry. Female‐phase flowers were found to have significantly higher anthocyanin concentration than male‐phase flowers in both natural populations and experimental plots. This color change corresponded to a decrease in male sexual function, which was measured by the percentage of pollen grains stained as viable by lactophenol aniline blue and germinated on Brewbaker–Kwack media. Color change was phenotypically plastic. Plants grown in full sun had a more extensive color change than those grown in shaded experimental plots, and this effect was reversed the following year when the shading was removed. Pollinator observations documented both diurnal and nocturnal insect visitation. Fruit and seed set were equivalent on inflorescences bagged during daylight versus night, indicating that both diurnal and nocturnal insects are effective pollinators. If pollinators discriminate based on color, this could potentially reduce within‐plant floral visits and also geitonogamy. This study is the first to document flower color change and moth pollination in Saponaria officinalis.