Pollinator-mediated Self-pollination Research Articles

Reduced pollination in bilateral flowers could reflect selfing avoidance

The multiple evolutionary transitions from radial to bilateral flower symmetry recorded across the angiosperms have been related to pollinator specialization and the promotion of outcross pollen transfer. In particular, the limited number of physical orientations associated with bilaterality results in a tighter morphological match between a flower and its specialized pollinators, which can enhance the transfer of incoming pollen while preventing autonomous, or even pollinator-mediated self-pollination when associated with dichogamy. In contrast, radial flowers have various planes of symmetry, which may allow pollination by a wider range of pollinators at the cost of more promiscuous pollen transfer. Here we used data from the literature and our own on pollen production, ovule production, and stigmatic pollen load compiled for 171 angiosperm species distributed worldwide to assess differences in pollen transfer in relation to flower symmetry within a phylogenetic comparative framework. We did not find evidence that bilateral and radial flowers differ in average pollen and ovule production. However, bilateral flowers tended to receive less pollen on their stigmas. This decrease in pollen receipt was most apparent among self-compatible species after accounting for the covarying effects of flower size and ovule production. Therefore, our findings indicate that the evolution of flower bilaterality, a trait we found is strongly associated with self-compatibility, comes at a quantitative pollination cost. However, they support the view that a bilateral flower morphology may provide the benefit of limiting self-pollen deposition, particularly in the absence of an alternative mechanism of selfing avoidance.

Pollinator-mediated self-pollination and reproductive assurance in an isolated tree of Magnolia grandiflora L.

BackgroundThe ability to produce seeds when pollinators or potential mates are scarce is one of the principal advantages of self-pollination in flowering plants. However, the role of pollinators mediating self-pollination to ensure seed set when pollen or potential mates are limited has received less attention. This study examined the reproductive consequences and involvement of pollinators in assuring seed set in an isolated tree of Magnolia grandiflora, a predominantly outcrossing species.MethodsWe tested various aspects of reproduction such as flower density, floral rewards, stigma receptivity, pollinator abundance and behaviour, fruit set and seed set, in two successive reproductive years (2015–2016).ResultsFlowers of M. grandiflora possess a suite of traits facilitating pollinator-mediated self-pollination (PMS), although the chances of autonomous self-pollination are reduced due to herkogamy, spatial separation of anther and stigma. The mean pollen production/flower was 5,152,289 ± 285,094 with a pollen-to-ovule ratio of 39430 ± 164. We found a significant positive correlation between number of visits and seed production for bees (r = 0.5099, p = 0.0007) and beetles (r = 0.7159, p = 0.00001), indicating these are effective at PMS. There was a significant negative correlation for thrips (r = – 0.3206, p = 0.044) and no correlation for flies or spiders. The percent fruit set was 100% and the seed set per ovule ranged between 19 and 20%.ConclusionsPMS will guarantee reproductive assurance and mitigate the effect of reduced mates or pollen limitation which is expected to increase the fecundity and establishment of individual trees in geographically isolated locations.

Effects of distance from models on the fitness of floral mimics.

Rewardless plants can attract pollinators by mimicking floral traits of rewarding heterospecific plants. This should result in the pollination success of floral mimics being dependent on the relative abundance of their models, as pollinator abundance and conditioning on model signals should be higher in the vicinity of the models. However, the attraction of pollinators to signals of the models may be partially innate, such that spatial isolation of mimics from model species may not strongly affect pollination success of mimics. We tested whether pollination rates and fruit set of the rewardless orchid Disa pulchra were influenced by proximity and abundance of its rewarding model species, Watsonia lepida. Pollination success of the orchid increased with proximity to the model species, while fruit set of the orchid increased with local abundance of the model species. Orchids that were experimentally translocated outside the model population experienced reduced pollinaria removal and increased pollinator-mediated self-pollination. These results confirm predictions that the pollination success of floral mimics should be dependent on the proximity and abundance of model taxa, and thus highlight the importance of ecological facilitation among species involved in mimicry systems.

Staminal hairs enhance fecundity in the pollen-rewarding self-incompatible lilyBulbine abyssinica

Flowering plants typically use floral rewards to attract animal pollinators. Unlike nectar, pollen rewards are usually visible and may thus function as a signal that influences landing decisions by pollen-seeking insects. Here we artificially manipulate the presence of both pollen and staminal hairs (a putative false signal of pollen reward availability) in the hermaphroditic lily Bulbine abyssinica (Xanthorrhoeaceae) to investigate their effects on bee visitation and fecundity, and also test for trade-offs between pollen production and seed production. Honeybees, the primary floral visitors, are probably not able to distinguish between colours of petals, staminal hairs and pollen of B. abyssinica, according to analysis of reflectance spectra in a bee vision model. Flowers with both pollen and hairs removed had the lowest levels of bee visitation, seed set and seed abortions. Flowers containing hairs had an ∼50% increase in visitation rate and seed set compared with emasculated flowers, while intact controls had the highest seed abortion rate. Ovule discounting in intact flowers is probably due to ovarian self-incompatibility (or strong early inbreeding depression) as ovules penetrated by tubes from self-pollen uniformly failed to develop into seeds. These results show that staminal hairs can enhance plant fecundity by increasing attraction of pollen-seeking insects to flowers without increasing the risk of ovule discounting through pollinator-mediated self-pollination.

Generalized food deception: colour signals and efficient pollen transfer in bee-pollinated species ofEulophia(Orchidaceae)

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

Emasculation increases seed set in the bird‐pollinated hermaphrodite Kniphofia linearifolia (Xanthorrhoeaceae): Evidence for sexual conflict?

Hermaphroditism in plants can lead to gender conflicts, such as pollen discounting-the loss of siring opportunities following self-pollination, and ovule discounting-the loss of seed production opportunities when self-pollen tubes disable ovules through early inbreeding depression or late-acting self-incompatibility. If ovules are discounted by self-pollination, it can be predicted that emasculation (removal of self-pollen) should increase seed production, as long as pollinators are not deterred by emasculation. • Using the hermaphroditic Kniphofia linearifolia, which belongs to a lineage known to possess late-acting self-incompatibility, we performed hand-pollinations with either self- or cross-pollen and recorded pollen tube growth and seed production. We paired experimentally emasculated plants with non-emasculated controls and quantified pollinator visitation rates, fruit, and seed set in both groups. • Ovules penetrated by tubes from self-pollen uniformly failed to develop into seeds, as expected from ovarian self-incompatibility (or strong early inbreeding depression). Experimental emasculation had no effect on the rate of visitation by birds, the primary pollinators of this species, but led to increased rejection by bees, which are secondary pollinators. Despite reducing visitation by some pollinators, emasculation led to increased seed production and reduced rates of seed abortion. • These results show that female performance in hermaphroditic flowers can be enhanced when flowers are emasculated, even if the overall number of pollinator visits is decreased. The most likely explanation for this effect of emasculation is that it reduces ovule discounting arising from pollinator-mediated self-pollination.

Carrion mimicry in a South African orchid: flowers attract a narrow subset of the fly assemblage on animal carcasses

Although pollination of plants that attract flies by resembling their carrion brood and food sites has been reported in several angiosperm families, there has been very little work done on the level of specificity in carrion mimicry systems and the importance of plant cues in mediating such specialization. Specificity may be expected, as carrion-frequenting flies often exploit different niches, which has been interpreted as avoidance of interspecific competition. Interactions between the orchid Satyrium pumilum and a local assemblage of carrion flies were investigated, and the functional significance of floral traits, especially scent, tested. Pollination success and the incidence of pollinator-mediated self-pollination were measured and these were compared with values for orchids with sexual- and food-deceptive pollination systems. Observations of insect visitation to animal carcasses and to flowers showed that the local assemblage of carrion flies was dominated by blow flies (Calliphoridae), house flies (Muscidae) and flesh flies (Sarcophagidae), but flowers of the orchid were pollinated exclusively by flesh flies, with a strong bias towards females that sometimes deposited live larvae on flowers. A trend towards similar partitioning of fly taxa was found in an experiment that tested the effect of large versus small carrion quantities on fly attraction. GC-MS analysis showed that floral scent is dominated by oligosulfides, 2-heptanone, p-cresol and indole, compounds that also dominate carrion scent. Flesh flies did not distinguish between floral and carrion scent in a choice experiment using olfactory cues only, which also showed that scent alone is responsible for fly attraction. Pollination success was relatively high (31·5 % of flowers), but tracking of stained pollinia also revealed that a relatively high percentage (46 %) of pollen deposited on stigmas originates from the same plant. Satyrium pumilum selectively attracts flesh flies, probably because its relatively weak scent resembles that of the small carrion on which these flies predominate. In this way, the plants exploit a specific subset of the insect assemblage associated with carrion. Pollination rates and levels of self-pollination were high compared with those in other deceptive orchids and it is therefore unlikely that this mimicry system evolved to promote outcrossing.

The invasive ‘mothcatcher’ (Araujia sericifera Brot.; Asclepiadoideae) co-opts native honeybees as its primary pollinator in South Africa

Successful invasive plants such as Araujia sericifera usually either are capable of automatic self-pollination or maintain pollinator services by having generalized pollination systems to make use of local pollinators in the invaded range. Alternatively, plants must co-opt new pollinators with similar morphology to native pollinators or reproduce asexually. We aimed to document the pollination biology of A. sericifera in South Africa. Given the success of this species as an invader, we predicted that sexual reproduction occurs either through self-pollination or because A. sericifera has successfully co-opted native insect pollinators. We examined the pollination biology of the South American A. sericifera in South Africa. We documented the effective pollinators including a comparison of the efficacy of nocturnal versus diurnal pollinators as well as the breeding system and long-term natural levels of the pollination success of this species. We found that native honeybees (Apis mellifera) were the main pollinators of A. sericifera in South Africa. Visiting moths are unimportant pollinators despite being attracted by the pale colour and nocturnal scent of the flowers. Plants from the Grahamstown population were incapable of autonomous self-pollination but pollinator-mediated self-pollination does occur. However, the highest fruit initiation resulted from out-crossed pollination treatments. The high pollen transfer efficiency of this species was comparable to other hymenopteran-pollinated exotic and native milkweeds, suggesting that A. sericifera maintains pollinator services at levels experienced by indigenous asclepiad species. Araujia sericifera reproduces successfully in South Africa due to a combined ability of this species to attract and exploit native honeybees as its pollinators and of individual plants to set fruit from pollinator-mediated self-pollination.

Relationships between population size and pollen fates in a moth-pollinated orchid

Management of small plant populations requires an understanding of their reproductive ecology, particularly in terms of sensitivity to Allee effects. To address this issue, we explored how components of pollen transfer and pollination success of individual plants varied among 36 populations of the self-compatible moth-pollinated orchid Satyrium longicauda in South Africa. Mean fruit set, seed production, proportion of flowers with pollen deposited or removed and proportion of removed pollen that reached stigmas (approx. 8% in this species) were not significantly related to population size (range: 1-450 flowering individuals), density or isolation. Plants in small populations did, however, have significantly higher levels of pollinator-mediated self-pollination (determined using colour-labelled pollen) than those in larger populations. Our results suggest that small populations of this orchid species are resilient to Allee effects in terms of overall pollination success, although the higher levels of pollinator-mediated self-pollination in small populations may lead to inbreeding depression and long-term erosion of genetic diversity.

Lack of floral nectar reduces self-pollination in a fly-pollinated orchid

One explanation for the widespread absence of floral nectar in many orchids is that it causes pollinators to visit fewer flowers on a plant, and thus reduces self-pollination. This, in turn, could increase fitness by reducing inbreeding depression in progeny and promoting pollen export. The few previous investigations of this hypothesis have all involved bee-pollinated orchids and some have given contradictory results. We studied the effects of adding artificial nectar (sucrose solution) to the spurs of a non-rewarding long-proboscid fly-pollinated orchid, Disa pulchra. Addition of nectar significantly increased the number of flowers probed by flies (2.6-fold), the time spent on a flower (5.4-fold), the number of pollinia removed per inflorescence (4.8-fold) and the proportion of removed pollen involved in self-pollination (3.5-fold). The level of self-pollination increased dramatically with the number of flowers probed by flies. Experimental self-pollination resulted in fruits with only half as many viable seeds as those arising from cross-pollination. Pollinators were more likely to fly long distances (>40 cm) when departing from non-rewarding inflorescences than when departing from rewarding ones. These findings provide support for the idea that floral deception serves to reduce pollinator-mediated self-pollination.

Self-compatibility and floral biology in subdioecious Wurmbea dioica (Colchicaceae)

Dioecy has long been interpreted as a mechanism to avoid self-fertilisation and the negative effects of inbreeding depression. We determined relative self-compatibility and temporal overlap of male and female functions for hermaphrodites in subdioecious Wurmbea dioica to assess the role of selfing in the maintenance of gender dimorphism. Plants were self-compatible but did not self-pollinate autonomously. Self- and open-pollinated hermaphrodites had high seed abortion and low seed set, whereas crossed hermaphrodites and crossed and open females had low seed abortion and high seed set. For selfed hermaphrodites, abortion occurred over a range of developmental stages and was negatively related to seed set. Inbreeding depression for seed set varied extensively among plants, averaging 0.56. Despite high inbreeding depression, substantial selfing occurred in open-pollinated hermaphrodites (S = 0.76), as estimated by a non-genetic method. Flowers were protogynous, although temporal separation of male and females functions was limited because anthers began to dehisce shortly after flowers opened. Anther dehiscence was staggered over 4 days and floral longevity, pollen longevity and stigma receptivity were prolonged, thus providing considerable opportunities for pollinator-mediated self-pollination. Our findings indicate that high levels of selfing and subsequent abortion of selfed embryos due to early acting inbreeding depression are important factors maintaining gender dimorphism in W. dioica.