Breeding system and pollen limitation in the masting tree Sorbus aucuparia L. (Rosaceae) in the NW Iberian Peninsula

Mast seeding or masting is the supra-annual periodic production of a large number of seeds by long-lived plants. It has been suggested that this may be a strategy to increase pollination efficiency. Sorbus aucuparia is a masting tree typically showing rather low fruit set, though with some variation among years and populations, together with marked among-year variation in flower and fruit production. Here we report a study of the reproductive biology and insect-visitor spectrum of S. aucuparia in the NW Iberian Peninsula. Results obtained over a 4-year period indicate marked self-incompatibility, so that fruit set is strongly dependent on pollinator service. Nevertheless, fruit and seed set were not limited by pollen supply in any of the years of study, since fruit and seed set after manual cross-pollination were no higher than after natural pollination. Inflorescences were visited by diverse insect species. There was no significant correlation between fruit set and insect visit frequency. Taken together, these findings indicate that the rather low fruit and seed sets observed in this species, and the spatiotemporal variation in these parameters, must be attributed to other factors, such as abiotic resource availability. We conclude that masting in S. aucuparia is probably not a strategy for increasing pollination efficiency.     

Rapid loss of self‐incompatibility in experimental populations of the perennial outcrossing plant Linaria cavanillesii

Transitions from self‐incompatibility to self‐compatibility in angiosperms may be frequently driven by selection for reproductive assurance when mates or pollinators are rare, and are often succeeded by loss of inbreeding depression by purging. Here, we use experimental evolution to investigate the spread of self‐compatibility from one such population of the perennial plant Linaria cavanillesii into self‐incompatible (SI) populations that still have high inbreeding depression. We introduced self‐compatible (SC) individuals at different frequencies into replicate experimental populations of L. cavanillesii that varied in access to pollinators. Our experiment revealed a rapid shift to self‐compatibility in all replicates, driven by both greater seed set and greater outcross siring success of SC individuals. We discuss our results in the light of computer simulations that confirm the tendency of self‐compatibility to spread into SI populations under the observed conditions. Our study illustrates the ease with which self‐compatibility can spread among populations, a requisite for species‐wide transitions from self‐incompatibility to self‐compatibility.     

AUTOGAMY AND INBREEDING DEPRESSION IN MOUNTAIN LAUREL,KALMIA LATIFOLIA (ERICACEAE)

We compared breeding systems, inbreeding depression, and pollination limitation between two populations of Kalmia latifolia in Virginia and Rhode Island. Plants were autogamous in Virginia but not Rhode Island. Although autogamy with selling is hypothesized to reduce levels of inbreeding depression, both populations showed similarly high inbreeding depression manifested as reduced fruit set. Autogamy may be uncorrelated with selling rate because autogamy is not obligate and because geitonogamy is likely. Autogamy in the Virginia population seems most likely to have evolved for reproductive assurance under competition for pollinator service. Fruit set was pollination limited in the Virginia population apparently because bumblebee pollinators were more attracted to a coflowering species, Vaccinium erythrocarpum.     

The role of a mixed mating system in the reproduction of a Mediterranean subshrub (Fumana hispidula, Cistaceae)

Knowledge about mixed mating systems can improve our understanding of the evolutionary dynamics of reproductive systems. Here we report a study of the pollination system (floral and reproductive biology, pollen limitation and stigmatic pollen load, floral visitors and inbreeding depression) of Fumana hispidula, a Mediterranean subshrub belonging to a species group with a strong selfing tendency. Autonomous self-pollination, hand self- and hand cross-pollination, open pollination and controls yielded fruits (0.28, 0.65, 0.68, 0.38, and 0.67, respectively); however, autonomous self-pollination resulted in the lowest fruit set. All individuals were fully self-compatible but we found great inter-individual variation in autonomous self-pollination ability, which was probably related to a variable expression of herkogamy degree. Inbreeding depression was low (0.040 for fruit set, 0.015 for seed set and ?0.026 for seed mass). The pollen supplementation experiment did not reveal pollen limitation and pollinators were seen visiting the flowers during the observation periods. These results support the idea that F. hispidula has a mixed mating strategy, which represents a successful reproduction mode in their patchy habitats.     

All in an afternoon: mixed breeding system in one-day lasting flowers of Hypericum elodes L. (Hypericaceae)

Knowledge about mixed mating systems can improve our understanding of the evolutionary dynamics of reproductive systems. Here we report a study of the floral and reproductive biology of Hypericum elodes, an Atlantic-European soft-water pools specialist which shows a floral architecture consistent with both self- and cross-pollination. Controlled pollination experiments were performed in a natural population during three consecutive years. Marked flowers were monitored until fruit production, and laboratory germination experiments were conducted with the seeds produced. Plants were self-compatible (SCI>0.75), however, compared with selfing, cross-pollination enhanced fruit-set, seed-set and seedling growth, but not seed germination. Inbreeding depression (δ) was mild in the pre-dispersal stages (δ = 0.22 for fruit set, 0.18 for seed set and 0.13 for seed mass), low for germination percentage (δ = 0.003) and mild for seedling growth (δ = 0.23). The breeding system of H. elodes promotes outcrossing and assures reproductive success by means of competitive autogamy. Our results suggest a mixed mating strategy for the studied population, characterized by mild inbreeding depression (cumulative δ = 0.57), highlighting the benefit of this reproductive mode in unpredictable habitat, as the typical shallow-water meadows where H. elodes grows.     

Different levels of inbreeding depression between outcrossing and selfing Serapias species

We quantified inbreeding depression for fruit production, embryo vitality and seed germination in three deceptive orchids, Serapias vomeracea, S. cordigera and S. parviflora, which do not provide any reward to their pollinators, and are predicted to experience high outcrossing. Of the three species examined only S. parviflora was autonomously selfing. Both S. vomeracea and S. cordigera showed highly significant differences in fitness between selfed and outcrossed progenies, resulting in high levels of inbreeding depression, which increased in magnitude from seed set to seed germination. Inbreeding depression may promote outcrossing in Serapias by acting as a post-pollination barrier to selfing. Cumulative inbreeding depression across three stages in S. parviflora was lower that in both outcrossing species. The large difference in germination between selfed and outcrossed seeds is an important issue in conservation biology.     

Wind pollination and insect pollination of two temperate willow species,Salix miyabeana and Salix sachalinensis

Pollination systems of Salix miyabeana and Salix sachalinensis were studied at a riverside in northern Japan in order to measure the balance of wind pollination and insect pollination. In 1996, 19 clones of each species were selected, and seed-set success by a net-bagging (to exclude insect visitation) and an artificial pollination (to remove pollen limitation) were compared to by natural pollination. For S. miyabeana, the same experiment was repeated in two populations in 1997. Proportion of seed set through wind pollination dominated in both species in this study. Pollen limitation was common under natural conditions, and S. sachalinensis relied more on insect pollination for seed production than S. miyabeana. Meteorological factors such as precipitation and hours of sunshine during the flowering season influenced the potential reproductive activity of the willow between years. In the wet and cloudy spring of 1996, clones which obtained high seed set depended more on insect pollination for both species, whereas in the dry and sunny spring of 1997, such clones depended more on wind pollination for S. miyabeana. Because the efficiency of wind pollination seemed to be more sensitive to fluctuating weather conditions than insect pollination, insect pollination was considered to play an assurance role for seed production in these willows.     

REPRODUCTIVE BIOLOGY OF THREE SPECIES OF EUPHORBIA SUBGENUS CHAMAESYCE (EUPHORBIACEAE)

The breeding system, pollen tube development, and floral biology of three species of Euphorbia subgenus Chamaesyce from southeastern Arizona have been examined in field and greenhouse studies. E. albomarginata is entirely dependent on insect vectors for pollination and seed production, E. capitellata requires insect visitors for maximum seed set but is capable of limited self-pollination, and E. hyssopifolia is self-pollinating and entirely independent of insect vectors. All three species are self-compatible. The differences in reliance on insect vectors, diversity of insects and probable amount of outcrossing are related to differences in cyathial size and arrangement. The reproductive biology of the three species is similar to that described for other weedy plant taxa.     

Fruit set in perennial vetch (Vicia unijuga): reproductive system and insect role in pollination

Perennial vetch (Vicia unijuga) is a wild plant found in parts of East Asia and potentially valuable as a forage species for more extreme environments. Information on its reproductive system and pollination biology is needed for progress in domestication of the species. We characterized the reproductive system of perennial vetch as facultative xenogamy (i.e. it is largely cross‐pollinated by insects but is also self‐compatible and can self‐pollinate). There was no significant difference (P > 0.05) in the fruit set ratio between insect cross‐pollination and artificial cross‐pollination at the seed maturation stage, but natural self‐pollination was inefficient. In our study conducted on the Tibetan plateau, eight insect species (especially certain bumble bees) are identified as potential pollinators, and four other insect species belonging to the Lepidoptera and Diptera visited flowers but are unlikely to be pollinators. The flower visitation rate of wild bumble bees was 1.6–3.3 times higher than domestic honeybees, with Bombus lepidus having the highest visitation rate of 15.7 florets/min. The diurnal floret opening rhythm of perennial vetch was synchronized with diurnal activity of potential pollinators. Optimal pollination of perennial vetch would likely be achieved using wild bees, as they have behaviour characteristics and flower tripping ability necessary, and are present in sufficient numbers to be efficient pollinators of this crop. However, even with sufficiency of pollination, there remains a fundamental problem with low fruit set which requires further investigation from a plant biology perspective.     

Autogamy in Boronia falcifolia: consequences for inbreeding and persistence in fragmented coastal heaths

Coastal heath is becoming increasingly fragmented, resulting in reduced pollinator abundance affecting species viability. The reproductive ecology and inbreeding of a common coastal heath species, Boronia falcifolia (Rutaceae), was investigated. Pollination observations and experiments were carried out at one site, and inbreeding was assessed using genetic markers at eight populations. Four pollination treatments were assessed: cross-pollination, self-pollination, autogamous pollination and open (insect) pollination. Boronia falcifolia was found to be highly self-compatible, frequently setting seeds from autogamous pollination. There were no significant differences between the autogamous, self and cross pollen treatments for any measures of reproductive success (pollen tube growth, fruit set, swollen locules and seed production). Insect activity resulted in fewer seeds per fruit than hand cross pollination, although pollinator visits were few. All populations studied were highly inbred. Autogamous self-pollination is widespread in B. falcifolia and this combined with its ability to vegetatively regenerate enhances its potential for survival when pollinators are few.     

Abnormalities in sexual development and pollinator limitation in Michelia coriacea (Magnoliaceae), a critically endangered endemic to Southeast Yunnan,China

Michelia coriacea (Magnoliacae) is a critically endangered tree, endemic to Southeast Yunnan province, China. Most of the individuals in the extant populations normally bear flowers, but fruit set and fertile seed production rates were only 6.7% and 0.2%, respectively. To identify possible causes of reproductive barriers, the following studies were carried out: examination of stamen and pistil development; experiments using controlled pollination; observations of behavior and frequency of floral visitors in both cultivated and natural populations. The results revealed that about 60% of pollen was abnormal and approx. 70% of ovules had delayed development. Hand pollination could effectively enhance the fruit set (F_4,25=35.139, P<0.0001) and seed set per fruit (F_4,25=85.022, P<0.0001). Both cultivated and wild M. coriacea had an extremely low frequency of floral visitors. Some beetles, a few species of Andrenidae and some Bombus sp. are likely to be the effective pollinators. The fruit set and seed set per fruit from controlled self-pollination and cross-pollination were significantly different (P<0.05), and thus it is inferred, that inbreeding depression may be a contributing factor in the very low seed production. It appears that low seed set in M. coriacea is due to a combination of factors: abnormalities in pollen and ovules, low number of effective pollinators, and inbreeding depression.     

Reproductive system and fitness of Vriesea friburgensis,a self‐sterile bromeliad species

Reproductive biology and plant fertility are directly related to many aspects of plant evolution and conservation biology. Vriesea friburgensis is an epiphytic and terrestrial bromeliad endemic to the Brazilian Atlantic rainforest. Hand‐pollination experiments were used to examine the reproductive system in a wild population of V. friburgensis. Plant fertility was assigned considering flower production, fruit and seed set, seed germination, and pollen viability. Self‐sterility observed from spontaneous selfing and manual self‐pollination treatments may be the consequence of late‐acting self‐incompatibility. Hand‐pollination results indicated no pollen limitation in the population studied. Floral biology features such as a few daily open flowers, nectar production, and sugar concentration corroborate hummingbirds as effective pollinators, although bees were also documented as pollinators. Components of fitness such as high flower, fruit, and seed production together with high seed and pollen viability indicate that this wild population is viable. From a conservation point of view, we highlight that this self‐sterile species depends on pollinator services to maintain its population fitness and viability through cross‐pollination. Currently, pollinators are not limited in this population of V. friburgensis. Conversely, the maintenance and continuous conservation of this community is essential for preserving this plant–pollinator mutualism.     

Mating systems and limits to seed production in two Dicerandra mints endemic to Florida scrub

We used hand-pollination experiments to test the mating systems of and evaluate limits to seed production in two federally listed endangered plants endemic to the Lake Wales Ridge in Florida, USA: Dicerandra frutescens Shinners ssp. frutescens Huck and D. christmanii Huck and Judd (Lamiaceae). Both are nonclonal, short-lived perennials found in gaps created by disturbance (e.g., fire, roads) in Florida scrub. We found that both species require pollen and insect visitation to produce seeds. We detected pollinator limitation of seed production in D. christmanii but not D. frutescens ssp. frutescens, which we suggest is a function of time-since-disturbance or gap size rather than intrinsic differences between the two species. Both species are self-compatible. Inbreeding depression reduced seed set by 60% in D. frutescens ssp. frutescens but did not occur in D. christmanii. We conclude that pollinator limitation (in fire-suppressed populations of both species) and inbreeding depression (in D. frutescens ssp. frutescens) have the potential to limit seed production in these seed-dependent, rare species. Appropriate fire management should mitigate both of these risks, by maintaining large populations and conditions attractive to pollinators. Although these two species are very similar in reproductive biology, comparisons with other Florida scrub endemics and with rare plants in general suggest that potential threats to conservation via reproductive biology are difficult to predict, depending on combinations of ecology, life-history, and phylogenetic history.     

The role of sexual and vegetative reproduction in the population maintenance of a monocarpic perennial herb,Cardiocrinum cordatum var. glehnii

Because monocarpic perennial plants have only one reproductive opportunity in their entire life, they need to ensure offspring production. Some plants reproduce both sexually and vegetatively, and vegetative reproduction could possibly compensate for seed production. Therefore, the role and significance of these reproductive modes is likely to differ between monocarps and polycarps, which can reproduce many times. Cardiocrinum cordatum var. glehnii is a monocarpic perennial that reproduces both sexually and vegetatively (bulblet formation). Here, we investigated the characteristics and contribution to population maintenance of sexual and vegetative reproduction to reveal the significance of these two reproductive modes in this species. First, we found that bulblet formation occurred in plants after the three‐leaved rosette stage. Second, resource allocation experiments revealed that although resources were mainly invested in fruit maturation after the flowering season, resource allocation was switched from sexual reproduction to vegetative reproduction if seed production was insufficient. Third, the outcrossing rate in this species varied greatly according to the environment surrounding the population. However, reproductive assurance by selfing kept seed production stable even if flowers did not receive sufficient pollen for full seed set via outcross pollination, and moreover, there was no intensive inbreeding depression. Finally, genotypic identification of ramets suggested that daughter ramets derived from vegetative reproduction received the space that the mother flowering ramet had occupied until the previous year.     

Reproductive biology of the andromonoecious Cucumis melo subsp. agrestis (Cucurbitaceae)

Background and Aims

Cucumis melo subsp. agrestis (Cucurbitaceae) is cultivated in many African regions for its edible kernels used as a soup thickener. The plant, an annual, andromonoecious, trailing-vine species, is of high social, cultural and economic value for local communities. In order to improve the yield of this crop, the first step and our aim were to elucidate its breeding system.

Methods

Eight experimental pollination treatments were performed during three growing seasons to assess spontaneous selfing, self-compatibility and effects of pollen source (hermaphroditic vs. male flowers). Pollination success was determined by pollen tube growth and reproductive success was assessed by fruit, seed and seedling numbers and characteristics. The pollinator guild was surveyed and the pollination distance determined both by direct observations and by indirect fluorescent dye dispersal.

Key Results

The species is probably pollinated by several Hymenoptera, principally by Hypotrigona para. Pollinator flight distances varied from 25 to 69 cm. No evidence for apomixis or spontaneous self-pollination in the absence of insect visitors was found. The self-fertility index (SFI = 0) indicated a total dependence on pollinators for reproductive success. The effects of hand pollination on fruit set, seed number and seedling fitness differed among years. Pollen tube growth and reproductive success did not differ between self- and cross-pollinations. Accordingly, a high self-compatibility index for the fruit set (SCI = 1·00) and the seed number (SCI = 0·98) and a low inbreeding depression at all developmental stages (cumulative δ = 0·126) suggest a high selfing ability. Finally, pollen origin had no effect on fruit and seed sets.

Conclusions

This andromonoecious species has the potential for a mixed mating system with high dependence on insect-mediated pollination. The selfing rate through geitonogamy should be important.     

Comparing the reproductive success and pollination biology of an invasive plant to its rare and common native congeners: a case study in the genus <Emphasis Type="Italic">Cirsium</Emphasis> (Asteraceae)

Previous studies have examined an association between reproductive success and pollination biology of rare versus widespread species through pair-wise comparisons of native and invasive congeners or rare and common congeners. To determine the importance of reproductive success and pollination biology for an invasive thistle, Cirsium vulgare, we compared it in its invaded range to five, co-occurring native Cirsium species that range from rare to common. Native study species include C. fontinale var. fontinale, C. andrewsii, C. brevistylum, C. occidentale, and C. quercetorum. We compared all species’ reproductive success, insect visitation rate and composition, autonomous self-pollination, and level of pollen limitation in multiple populations. Species differed in their reproductive success; the invasive C. vulgare produced more flower heads per plant than most native species. C. vulgare attracted more visitors than its congeners. In addition, reproductive success and insect visitation significantly varied between populations within species, mainly due to aphid infestation in one population of C. occidentale. Unlike the rare species (C. fontinale and andrewsii), C. vulgare did not require a pollinator for high-levels of seed production. The remaining native species set fewer seeds than C. vulgare without a pollinator. However, differences in insect visitation and autonomous self-pollination did not lead to differences in pollen limitation across species or between populations. This result suggests that factors other than pollination biology determine the difference in reproductive success of these species. However, high levels of autonomous self-pollination and generalist insect visitation may allow the invasive C. vulgare to easily establish new populations from low numbers of propagules. Our study provides one contrast that should build towards a larger comparative analysis to examine general patterns in the relationship between reproductive success, pollination biology, rare and invasive species, and our ability to predict biological invasions in introduced species.     

When is it worth being a self-compatible hermaphrodite? Context-dependent effects of self-pollination on female advantage in gynodioecious Silene nutans

In gynodioecious plant species with nuclear‐cytoplasmic sex determination, females and hermaphrodites plants can coexist whenever female have higher seed fitness than hermaphrodites. Although the effect of self fertilization on seed fitness in hermaphrodites has been considered theoretically, this effect is far from intuitive, because it can either increase the relative seed fitness of the females (if it leads hermaphrodites to produce inbred, low quality offspring) or decrease it (if it provides reproductive assurance to hermaphrodites). Hence, empirical investigation is needed to document whether relative seed fitness varies with whether pollen is or is not limiting to seed production. In the current study, we measured fruit set and seed production in both females and hermaphrodites and the selfing rate in hermaphrodites in two experimental patches that differed in sex ratios in the gynodioecious plant Silene nutans. We found an impact of plant gender, patch, and their interaction, with females suffering from stronger pollen limitation when locally frequent. In the most pollen‐limited situation, the selfing rate of hermaphrodites increased and provided hermaphrodites with a type of reproductive assurance that is not available to females. By integrating both the beneficial (reproductive assurance) and costly effects (through inbreeding depression) of self‐pollination, we showed that whether females did or did not exhibit higher seed fitness depended on the degree of pollen limitation on seed production.     

Reproductive biology in diploid Anthericum ramosum and tetraploid A. liliago (Anthericaceae)

Polyploidy is often thought to be associated with asexual reproduction, self-compatibility and self-pollination. Polyploids are also often regarded as being less sensitive than diploids to the negative effects of inbreeding. The reproductive biology of two lilioid species, the diploid Anthericum ramosum and the tetraploid A. liliago , was compared in a series of greenhouse and field experiments. Pollination experiments were carried out to study agamospermy (seed set without fertilization), self-compatibility and early inbreeding depression for both species. Tetraploid A. liliago showed no greater ability to self-pollinate than diploid A. ramosum and neither of the species showed agamospermy. Both species were self-compatible, but levels of fruit and seed set were lower after self-fertilization than after cross-fertilization in A. ramosum ( P <0.001). No reduction in fecundity after self-fertilization was observed in A. liliago . Fruit set in natural populations of A. ramosum increased significantly ( P <0.001) after emasculation (which excluded the possibility of autodeposition of pollen within flowers). In contrast, emasculation of flowers reduced the fruit set within natural populations of A. liliago ( P <0.05). The reproductive biology of diploid A. ramosum and tetraploid A. liliago is discussed in the context of polyploidization and the reduced fruit and seed set after self-fertilization in A. ramosum is discussed in terms of early inbreeding depression.     

Pollen limitation and Allee effect related to population size and sex ratio in the endangered Ottelia acuminata (Hydrocharitaceae): implications for conservation and reintroduction

Small populations may suffer more severe pollen limitation and result in Allee effects. Sex ratio may also affect pollination and reproduction success in dioecious species, which is always overlooked when performing conservation and reintroduction tasks. In this study, we investigated whether and how population size and sex ratio affected pollen limitation and reproduction in the endangered Ottelia acuminata, a dioecious submerged species. We established experimental plots with increasing population size and male sex ratio. We observed insect visitation, estimated pollen limitation by hand‐pollinations and counted fruit set and seed production per fruit. Fruit set and seed production decreased significantly in small populations due to pollinator scarcity and thus suffered more severe pollen limitation. Although frequently visited, female‐biased larger populations also suffered severe pollen limitation due to few effective visits and insufficient pollen availability. Rising male ratio enhanced pollination service and hence reproduction. Unexpectedly, pollinator preferences did not cause reduced reproduction in male‐biased populations because of high pollen availability. However, reproductive outputs showed more variability in severe male‐biased populations. Our results revealed two component Allee effects in fruit set and seed production, mediated by pollen limitation in O. acuminata. Moreover, reproduction decreased significantly in larger female‐biased populations, increasing the risk of an Allee effect.     

Insect and wind pollination of an alpine biennial Aconitum gymnandrum (Ranunculaceae)

Wind pollination can provide reproductive insurance for animal‐pollinated dioecious plants in the absence of available pollinators, but combinations of insect and wind pollination (ambophily) have rarely been studied in hermaphrodite herbs. We examined the stable occurrence of insect pollination and wind pollination over 4 years in a population of a biennial Aconitum species (A. gymnandrum) with actinomorphic and degenerate sepals. The total frequency of visits of two bumblebee species showed no distinct fluctuations in the studied population among the 4 years. However, seed production of netted flowers after emasculation indicated wind pollination had occurred. The seed number of bagged flowers with one visit by bumblebees was significantly less than that of netted flowers after one visit, or in control flowers. Both seed number and fruit set of netted flowers were significantly lower than in control flowers. These results suggest that wind pollination provides supplementary pollen to unvisited and/or once‐visited flowers, but accounts for only a small amount of seed production compared to bumblebee pollination in natural conditions. Such a combination of insect and wind pollination might play an important role in maintaining sexual reproduction of this biennial herb, allowing it to persist in arid habitats on the Qinghai‐Tibetan Plateau, especially during Quaternary glacial periods when pollinator populations oscillated extensively.