Zygomorphic flowers are usually more complex than actinomorphic flowers and are more likely to be visited by specialized pollinators. Complex zygomorphic flowers tend to be oriented horizontally. It is hypothesized that a horizontal flower orientation ensures effective pollen transfer by facilitating pollinator recognition (the recognition-facilitation hypothesis) and/or pollinator landing (the landing-control hypothesis). To examine these two hypotheses, we altered the angle of Commelina communis flowers and examined the efficiency of pollen transfer, as well as the behavior of their visitors. We exposed unmanipulated (horizontal-), upward-, and downward-facing flowers to syrphid flies (mostly Episyrphus balteatus), which are natural visitors to C. communis. The frequency of pollinator approaches and landings, as well as the amount of pollen deposited by E. balteatus, decreased for the downward-facing flowers, supporting both hypotheses. The upward-facing flowers received the same numbers of approaches and landings as the unmanipulated flowers, but experienced more illegitimate landings. In addition, the visitors failed to touch the stigmas or anthers on the upward-facing flowers, leading to reduced pollen export and receipt, and supporting the landing-control hypothesis. Collectively, our data suggested that the horizontal orientation of zygomorphic flowers enhances pollen transfer by both facilitating pollinator recognition and controlling pollinator landing position. These findings suggest that zygomorphic flowers which deviate from a horizontal orientation may have lower fitness because of decreased pollen transfer.
Abstract. The invasive alien bumble bee Bombus terrestris may hinder the reproduction of native plants that have established specialized pollination systems with native bumble bees. To test this hypothesis, we examined the visitation frequency and behavior of native and alien bumble bee species and resultant seed production in Corydalis ambigua, a native plant in Hokkaido, Japan. This species is self-incompatible: the flower has a spur and requires visitation by bumble bees for effective seed production. We compared visitation frequency as well as fruit and seed set after cross-and open pollination at five sites of C. ambigua. Four of these sites occurred near a residential district and included naturalized populations of B. terrestris, and the fifth site was located in a forested habitat with no B. terrestris. The native species B. ardens and B. hypocrita and the alien B. terrestris frequently visited C. ambigua. Bombus ardens legitimately consumed nectar, whereas B. hypocrita and B. terrestris rob nectar by perforating spurs. The legitimate pollinator B. ardens produced fruits and seeds more efficiently than the nectar robbers. At three sites, the proportion of robbed flowers per inflorescence gradually increased through the flowering period, which may be caused by the intrusion of alien B. terrestris into the native plant-pollinator interactions. At these sites, C. ambigua suffered from pollen limitation, as seed production from open pollination was lower than from cross-pollination, despite the fact that the total abundance of three bumble bees was higher than in the other two sites. Legitimate B. ardens visited fewer flowers within inflorescences with more robbed flowers, suggesting that nectar robbing may reduce the frequency of visitations by B. ardens within inflorescences, and resulting in decreased fruit set. Furthermore, reduced seed set implies a reduction in the pollination quality by B. ardens, probably due to decreases in visiting time per flower. Thus, introduction of alien B. terrestris may alter the native plant-pollinator mutualism: C. ambigua could establish a novel pollination relationship with B. terrestris because of its nonzero pollination efficiency, similar to the native robber B. hypocrita.
To understand the relationships between floral morphologies and the reproductive strategies of plants, the contributions of multiple pollinators to plant reproductive success need to be examined. To outline recent advances on this topic, we review studies of five bumblebee-pollinated plants in Japan. These plant species are pollinated by one to three bumblebee species differing in proboscis length: Bombus consobrinus, Bombus diversus and Bombus honshuensis. These pollination systems allow us to compare the reproductive strategies of plants pollinated by single and multiple bumblebee species. First, we address the effects of morphological correspondence between flowers and pollinators on the reproductive success of plants. In plants with narrow tubular flowers, Isodon umbrosus and Clematis stans, pollination effectiveness depended on the morphological correspondence between floral tube length and pollinator mouthparts. These flowers are subject to varied directions and intensities of selection by multiple bumblebee species, resulting in the maintenance of large variation in floral morphology within and between populations, and even within individuals. In contrast, pollination effectiveness in plants having flowers with a wide entrance, Melampyrum roseum and Hosta sieboldiana, did not differ among bumblebee species because of good correspondence between floral morphology and bumblebee body size, resulting in small morphological variations among flowers. Thus, generalized pollination systems with multiple pollinator species favor floral traits that enable the use of various pollinators. Second, we address the quantity and quality of the pollination service in bumblebee-pollinated plants. Isodon umbrosus, with its generalized pollination system, suffered from pollen limitation because of low pollination quality. In contrast, Isodon effusus, which has a specialized pollination system, suffered from pollen limitation because of low pollination quantity. Isodon umbrosus produced large numbers of short tubular flowers to improve pollination quantity, whereas I. effusus produced small numbers of long tubular flowers to improve pollination quality, resulting in a clear trade-off between the size and number of flowers within plants. In M. roseum, which has a generalized pollination system, three bumblebee species achieved sufficient pollination, but seed production was limited by an increased rate of self-pollination. This is because this species invests more resources in crosspollinated seeds by selective abortion of selfed seeds. Our results demonstrate that the strategy of generalized plants is to improve pollination quantity, whereas the strategy of specialized plants is to improve pollination quality.
Although land-use changes such as urbanization have dramatically altered plant-pollinator interactions, little is known about their effects on pollen limitation and floral traits. In this study, we examined pollinator visit frequency, reproductive success, and floral trait measurements in 12 populations of the annual andromonoecious Commelina communis in an urban-rural area. Pollinator and mate availability decreased significantly with developed land area around the study site. Most urbanized populations suffered from significant pollinator-limited male and/or female reproductive success. High fruit set in urbanized populations may suggest the presence of high reproductive assurance by selfing. The stigma height and degree of herkogamy significantly decreased with increased pollinator limitation. Petal length, anther height, and/or the pollen:ovule ratio tended to be low in pollinator- and mate-limited urban populations. One urban population with high pollinator availability had flowers with higher herkogamy and stigma height compared to rural populations. These results suggest that urbanization may provide diverse selective forces that could affect the phenotypic variation in floral traits.
We examined the adaptive significance of a temporal decrease in the calyx tube length of Clematis stans, a dioecious species pollinated by Bombus diversus (long proboscis) and B. honshuensis (short proboscis). We compared visitation frequency, pollen removal, pollen deposition, and fruit set after a single visit among three flower stages, differentiated by calyx tube length. Bombus diversus frequently visited and removed significantly more pollen from long flowers. Bombus honshuensis visited and tended to remove more pollen from short flowers. Both pollinators deposited more pollen in short flowers, resulting in higher fruit set. These results indicate that size correspondence between the proboscis and the calyx tube enhances visitation frequency and pollen removal, but not pollen deposition. Because a single visit does not fertilize all ovules of a flower, multiple visits by two bumble bee species may increase seed production and genetic diversity of offspring. By temporally changing calyx tube length, C. stans can use two bumble bee pollinators and maintain specialized relationships with each. This strategy may be adaptive when the pollinator fauna fluctuates, and is economical because it eliminates costs required to produce different types of flowers. This constitutes a novel pattern of temporal specialization in flower-pollinator relationships.
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