Coping with third parties in a nursery pollination mutualism: Hadena bicruris avoids oviposition on pathogen-infected, less rewarding Silene latifolia

In nursery pollination systems, pollinator offspring usually feed on pollinated fruits or seeds. Costs and benefits of the interaction for plant and pollinator, and hence its local outcome (antagonism-mutualism), can be affected by the presence of 'third-party' species. Infection of Silene latifolia plants by the fungus Microbotryum violaceum halts the development of fruits that provide shelter and food for larvae of the pollinating moth Hadena bicruris. We investigated whether the moth secures its benefit by selective oviposition on uninfected flowers. Oviposition was recorded in eight natural populations as a function of plant infection status, local neighbourhood, plant and flower characteristics. Oviposition was six times lower on flowers from infected than on those from uninfected plants. Oviposition decreased with decreasing flower and ovary size. Moths could use the latter to discriminate against diseased flowers. Although moths show an adaptive oviposition response, they reduce the future potential of healthy hosts because they still visit infected plants for nectar, vectoring the disease, and they reduce any fitness advantage gained by disease-resistant plants through selective predation of those plants.     

开花时间与伴生种对鹤首马先蒿传粉和生殖成功的影响

开花物候是物种间相互作用的重要生活史特征和适合度因子,在全球气候变化的背景下而备受关注.为探讨开花时间如何存种内和种间水平上影响植物的传粉和生殖成功,我们连续3年(2003-2005)对不同花期和伴生种存在情况下的鹤首马先蒿(Pedicularis gruina)的传粉者访花忠实度、受粉率、坐果率、单果种子产量和果实被啃食频率进行了比较研究.结果表明鹤首马先蒿的坐果率主要受其传粉环境的影响:在没有伴生种时,不同时期鹤首马先蒿的坐果率没有显著差异,34-38％的花可以坐果;在有伴生种存在时既可以显著提高其坐果率,也可显著降低其坐果率,这取决于传粉者类型以及伴生种密穗马先蒿(P.densispica)花期的差异.密穗马先蒿具有花蜜和花粉双重报酬,在群落中可以作为主体物种吸引传粉者并间接促进与其伴生的鹤首马先蒿的传粉和生殖成功.同样无蜜的管花马先蒿(P.siphonantha)和鹤首马先蒿伴生,则是通过提高群落水平对传粉者的吸引力进而直接促进鹤首马先蒿的传粉和生殖成功.此外,研究结果也表明开花时间对坐果率没有显著影响,但是显著影响单果种子产量和果实被啃食的频率.在相同的传粉条件下早花期植株单果种子产量显著高于晚花期的种子产量,同时早花期的果实被啃食的频率显著增加.     

Large plant size counteracts early seed predation during the extended flowering season of a Silene uniflora (Caryophyllaceae) population

A population of the alvar race of the perennial herb, Silene uniflora (Caryophyllaceae), which grows on thin soils in open alvar habitats on the Baltic island of Oland SE Sweden, was found to have an extended and more or less bimodal flowering phenology Large individuals produced flowers during both periods, while small, and presumably young, individuals only produced flowers in either of the two periods, or in part of both In the early flowering period plants were heavily infested by the seed-predatory larvae of a noctuid moth, Hadena confusa , but in the late flowering period only a small proportion of the fruits was attacked by the seed predators The proportion of flowers developing into fruits was consistently high throughout the season Both the number of seeds per capsule and the mass of seeds decreased over the flowering season However, the germination success of early and late seeds did not differ Thus, although differing in number of seeds, both early and late flowers contributed to individual reproductive success Large individuals started to flower early in the season and despite their high loss of seeds in the early part of the summer they contributed a larger number of seeds to the seed pool than smaller and later-flowering individuals Although selection was acting to favour later flowering during a year with high early seed predation, consistency of date of flower initiation and of relative predation impact on individuals across years was low suggesting that recurrent selection by seed predators is weak Seed predation, although heavy, is therefore judged to be unlikely to cause a significant evolutionary response on flowering phenology in this plant     

Pollinator preference and pollen viability mediated by flower color synergistically determine seed set in an Alpine annual herb

Gentiana leucomelaena manifests dramatic flower color polymorphism, with both blue‐ and white‐flowered individuals (pollinated by flies and bees) both within a population and on an individual plant. Previous studies of this species have shown that pollinator preference and flower temperature change as a function of flower color throughout the flowering season. However, few if any studies have explored the effects of flower color on both pollen viability (mediated by anther temperature) and pollinator preference on reproductive success (seed set) in a population or on individual plants over the course of the entire flowering season. Based on prior observations, we hypothesized that flower color affects both pollen viability (as a function of anther temperature) and pollen deposition (as a function of pollinator preference) to synergistically determine reproductive success during the peak of the flowering season. This hypothesis was tested by field observations and hand pollination experiments in a Tibetan alpine meadow. Generalized linear model and path analyses showed that pollen viability was determined by flower color, flowering season, and anther temperature. Anther temperature correlated positively with pollen viability during the peak of the early flowering season, but negatively affected pollen viability during the peak of the mid‐ to late flowering season. Pollen deposition was determined by flower color, flowering season (early, or mid‐ to late season), and pollen viability. Pollen viability and pollen deposition were affected by flower color that in turn affected seed set across the peak of the flowering season (i.e., when the greatest number of flowers were being pollinated). Hand pollination experiments showed that pollen viability and pollen deposition directly influenced seed set. These data collectively indicate that the preference of pollinators for flower color and pollen viability changed during the flowering season in a manner that optimizes successful reproduction in G. leucomelaena. This study is one of a few that have simultaneously considered the effects of both pollen viability and pollen deposition on reproductive success in the same population and on individual plants.     

Spatial and temporal dispersion patterns of pollinators and their relationship to the flowering strategy of Yucca whipplei (Agavaceae)

Summary A field investigation of the mutualistic interaction between a monocarpic perennial plant, Yucca whipplei, and its host-specific pollinator and seed predator, Tegeticula maculata (Lepidoptera: Prodoxidae), was conducted to determine how the resource utilization pattern and population dynamics of the pollinator have influenced the evolution of the flowering and fruiting pattern of the plant. Although the temporal pattern of emergence of pollinators results in a relatively close tracking of flower abundance within a season, the ratio of pollinators to open flowers does vary significantly within a season, as well as between seasons. At any point in time during the flowering season, the population of adult yucca moths is distributed evenly among the available flowers, so that the number of pollinators on an inflorescence is directly proportional to the number of open flowers available. The relative isolation of individual flowering plants appears to have little effect on the distribution of pollinators among inflorescences. The number of fruits initiated on a plant is directly proportional to the number of flowers produced, and is also partially determined by the time of flowering. Yucca whipplei always produces many more flowers than fruits. Most flowers are not fertilized, and the plants also generally abort and abscise immature fruits after flowering. Fruit production of at least some plants, however, appeared limited by pollination. It is also expected that in some years the relative abundance of pollinators will be low enough that most plants will be pollinator-limited. It is suggested that the pattern of flowering and fruiting of this species has evolved in response to the unpredictability of pollinator availability, both within and between seasons. Resource uncertainty and selection acting on the male component of fitness may also be involved.     

Different effects of sphingid and noctuid moths on the fecundity ofPlatanthera metabifolia (Orchidaceae) in Hokkaido

The fecundity ofPlatanthera metabifolia was investigated in relation to different types of behavior and morphology in both noctuid and sphingid pollinator moths. Low capsule set in the native habitats resulted from low activity of pollinating moths. From different patterns of capsule formation on spikes, pollinated spikes could be classified into sphingid-pollinated and noctuid-pollinated types. The contributions of sphingids to capsule set were nearly constant at the three study sites. High percentage capsule set at one site was linked with high noctuid activity. Different preferences of sphingids and noctuids as to spike features were detected: sphingids selected spikes with large numbers of flowers in early stages of flowering. Flowers with different spur length were equally pollinated by sphingids. On the other hand, noctuids selected spikes with short and medium-sized spurs in the late stage of flowering. The size and density of spikes scarcely affected the pollination activity of noctuids. Selection pressure upon spike size and spur length in relation to sphingid pollination was suggested. The possibility of local differentiation in spur length due to activity of noctuids was discussed.     

Flowering phenology and female fitness: impact of a pre-dispersal seed predator on a sexually polymorphic species

In order to produce seeds, animal-pollinated plants must flower synchronously with and be attractive to their pollinators while avoiding antagonists. Here, we explore temporal and inter-individual patterns in pollination and pre-dispersal seed predation of Dianthus sylvestris by Hadena moths, within and among three sex morphs. We scored plants that started flowering at different periods in 2001 and 2003 and found that fruit set decreased and predation rates increased over one season, and most of the other season, granting a female reproductive advantage to early flowering plants, though, we found no morph-specific temporal patterns. Female plants set more fruits, and more of their fruits escaped predation in one year, but this did not grant them a reproductive advantage since they produce fewer flowers per plant than the other morphs. Instead, mixed plants showed a clear female reproductive advantage. We also examined predation types by Hadena and seed production in attacked and intact fruits of individually marked flowers. Though female Hadena moths laid eggs preferentially into perfect flowers, flower sexes suffered similar predation by itinerant caterpillars. Attacked fruits contained fewer and lighter seeds than un-attacked ones. We conclude that pre-dispersal seed predation by Hadena may select on flowering onset of this sexually polymorphic species.     

Extended flowering in a Mediterranean shrub: Seasonal variability in seed quality and quantity

Fluctuating conditions throughout the year and changes in floral display may promote shifts in pollinator activity and predator pressure, influencing female reproductive output, especially for extended flowering species under seasonal climates. In this regard, flowering and fruit production were tracked in 2 different years in 2 populations of Ononis tridentata in Central Spain. Total fruit production was estimated, and fruits were harvested to obtain primary fruit investment, pollination success, predation incidence, seed production, seed weight and germination rates. Ononis tridentata combined spring mass flowering with a steady long flowering period across the summer and fall. The fewer flowers that are produced in fall were successfully pollinated, and produced fruits that were subject to minimal predation pressure relative to spring fruits. Moreover, fall fruits contained a higher number of heavier seeds and showed higher germination rates than those of spring seeds. Fall reproductive output represent 10% of annual viable seeds and thus may act as an important complement to the main spring reproductive investment. Extended flowering could be interpreted as a “bet-hedging strategy” for enduring Mediterranean unpredictable and changing environmental conditions.     

Effects of season and population size on pollination and reproductive output in a Mediterranean shrub

• Pollinator guilds may change throughout extended flowering periods, affecting plant reproductive output, especially in seasonal climates. We hypothesised a seasonal shift in pollinator guild and an autumn reduction in pollinator abundance, especially in small and sparse populations.
• We recorded pollinator identity, abundance and behaviour in relation to flower density from plant to population throughout the extended flowering of Ononis tridentata. We evaluated female reproductive output by recording pollination success and pre‐dispersal seed predation in eight populations of contrasting size and density. Offspring quality was also characterised through seed weight and germination.
• A diverse guild of insects visited O. tridentata in spring, while only Apis mellifera was observed in autumn. Visitation frequency did not vary seasonally, but the number of flowers per foraging bout was lower, and seeds were heavier and had a higher germination rate in autumn. Plant and neighbourhood flowering display were not related to pollinator visitation frequency or behaviour. However, the rate of fertilised ovules, seed set and autumn flowering display size were positively related to population density.
• The maintenance of pollination in autumn enhances the reproductive performance of O. tridentata due to higher quality of autumn seed, and to a large reduction in seed predator pressure. We also suggest that observed changes in pollinator behaviour could be one of the processes behind seasonal variation in seed performance, since geitonogamous crosses were less likely to occur in autumn.

     

COMPARATIVE REPRODUCTIVE BIOLOGY OF HERMAPHRODITIC AND MALE-STERILE IRIS DOUGLASIANA HERB. (IRIDACEAE)

A comparative study of the reproductive biology of male-sterile and hermaphroditic plants in a gynodioecious population of Iris douglasiana Herb. (Iridaceae) was conducted at the University of California's Marine Laboratory at Bodega Bay, California, between 1976–1979. Each year of the study, there were 11.1% male-sterile plants in the population, some of which began blooming at the same time as the earliest blooming hermaphrodites. Male-sterile flowers made up between 7–21% of the flowers produced during the male-sterile flowering period. Male-sterile flowers had smaller sepals and petals than hermaphrodites, there were fewer of them per square meter, and they had fewer pollinated stigmas than did hermaphroditic flowers. In a test to determine pollinator preference, intact hermaphroditic flowers tended to have more pollinated stigmas than did hermaphrodites with their stamens removed or those flowers with shortened sepals made to resemble the smaller male-sterile flowers. Floral phenology and nectar-flow patterns were similar in both types of flowers as were the kinds of amino acids and sugar rewards in the nectar. Male-sterile flowers, however, produced much less nectar per flower. There were no significant differences in the number of ovules per flower or the number of seeds produced per capsule between the two flower types, but the loss of seeds through larval predation was much greater in capsules from hermaphroditic flowers. Early flowering and setting of seed by plants with male-sterile flowers could give them a reproductive advantage over plants with hermaphroditic flowers which experience higher levels of larval predation later in the growing season.     

The effects of stigma age on receptivity in Silene alba (Caryophyllaceae)

Silene alba, a perennial, dioecious plant, produces flowers that open in the evening and can remain open and receptive to pollination for up to 5 d, though in hot and dry conditions the flowers will wilt during the day only to reopen night after night. In the field, it is visited by two different kinds of pollinators with differential success: moths visit the flowers at night, and their movements result in broad pollen dispersal and large seed production, whereas bees, wasps, and flies visit the flowers in the mornings and have decreased pollination effectiveness. However, this differential success may be due to a decrease in stigmatic receptivity soon after the flowers open. We performed controlled pollinations to determine the effect of stigma age on pollen germination and seed set. We pollinated flowers at 12-h intervals up to 120 h and divided these into two sets: from one set, we removed stigmas 24 h after pollination to examine percentage of pollen germination. The second set of flowers was allowed to produce fruits, and the seeds were counted and weighed. Pollen germination declined significantly with stigma age, but there was no significant effect of stigma age at pollination on the number or mass of resulting seeds. Thus, the decreased pollination success of bees is not due to a decrease in stigmatic receptivity but is most likely a result of pollinator inefficiency.     

Community-level flowering phenology and fruit set: Comparative study of 25 woody species in a secondary forest in Japan

We investigated the flowering phenology, pollinator visitation, and fruit set of 25 animal-pollinated woody species in a warm temperate secondary forest in Japan. Various species flowered sequentially from February to October. The principal pollinators were bumblebees, honey-bees, flies and/or beetles and birds; bumblebees and flies/beetles pollinated most trees. The duration of flowering was shorter for species that bloomed in the middle of the season than it was for species that bloomed earlier or later in the season. The timing of flowering was more synchronous within species that had a shorter flowering duration; this was also detected when phylogenetically independent contrasts were calculated. This could be important for the effective pollination of species with a short flowering duration because such species bloom sequentially over a short period of less than 1month around May. Fruit set was related not to pollinator type, sex expression, flowering sequence (in order of the date of peak flowering) or flowering duration, but to the relative abundance of the species in the forest. This correlation was detected for fly- and beetle-pollinated species but not for bumblebee-pollinated species. Thus, relatively rare plant species with opportunistic pollinators might experience limited fruit set because of insufficient pollinator services. Bagging experiments conducted on eight hermaphrodite species revealed that the fruit set of bagged flowers was nearly zero, lower than that of control flowers. These results indicate the importance of pollinators for successful reproduction and thus for the coexistence of plants in this secondary forest.     

Pollinator activity and pollination success of Medicago sativa L. in a natural and a managed population

Medicago sativa L. is an important cash crop in the arid region of northwest China. Pollinator activity is an essential aspect of pollination success, but the relationships between pollinator visitation rate and seed set still need further study of M. sativa. We investigated the following characteristics of M. sativa in natural and managed populations: floral traits, pollinator activity, and breeding system. Our results indicated the management could affect the number of flowers produced; however, there was no detectable effect on the seed set per flower. We found the percentage of seeds among pollinated flowers in the managed population was significantly higher than that in the natural population. Moreover, the increase in the proportion of pollinated flowers could significantly increase seed set per flower, and pollinator visitation rate was the important limiting factor for seed set in both populations. Andrena lebedevi Popov was found to be the most frequent pollinator in both populations. Outcrossing was dominant in the breeding system and insect pollination played an important role in outcrossing. Our study suggested that proper management (artificial selection) could promote pollination success of M. sativa.     

Variable nursery pollinator importance and its effect on plant reproductive success

Nursery pollination, in which insects use as hosts the very plants they pollinate, ranges from obligate mutualism to parasitism. In the non-obligate interaction between Greya moths and the host Lithophragma sp., the relative density of nursery pollinators and copollinators, which do not use plant tissues for larval development, is a key determinant of the interaction’s outcome. Silene (Caryophyllaceae) nursery pollination by Hadena moths (Lepidoptera: Noctuidae), studied primarily in Europe, is considered antagonistic because copollinators comprise a substantial proportion of the pollinator community. However, there are few studies that ascertain the direction of the Silene–Hadena interaction by taking into account both pollinator service and seed predation. Here, we report a novel comprehensive evaluation of the direction of the interaction between North American Hadena ectypa on Silene stellata, by comparing the relative contributions of nursery and copollinators to S. stellata pollination and relate this to variation in fruit predation and reproductive success of S. stellata across multiple sites and years. Hadena ectypa pollinator importance (pollen deposited/visit/h) varied between years, resulting from variable visitation rate. Copollinator importance was higher than H. ectypa in 1 year and equivalent in another. In two of three sites, lowered H. ectypa activity was not correlated with a significant decrease in plant reproductive success, indicating a negative interaction. Although pollinator service by H. ectypa is substantial in this system, copollinators’ service is at least as great, and when the cost of fruit predation is factored in, the net effect of the interaction is parasitism of host plants.     

Significance of intra-inflorescence variation on flowering time of a spring ephemeral, <Emphasis Type="Italic">Gagea lutea</Emphasis> (Liliaceae), under seasonal fluctuations of pollinator and light availabilities

I studied the relationship between seed-set patterns within inflorescences and temporal variations in light and pollinator availabilities for 2 years in the spring ephemeral species Gagea lutea in a deciduous forest. Timing of canopy closure and seasonal trend of pollinator frequency did not synchronize with the annual fluctuation in flowering phenology. In the early snowmelt year, seed-set success reflected the seasonal pollinator abundance from early to middle flowering periods. In the late snowmelt year, however, seed-set rates were independent of pollinator activity and decreased with canopy closing even after hand pollination. The restricted seed production by defoliation and the increase in seed-set rates at the forest edge suggested that seed production was supported by current photosynthetic carbon gain. Thus, annual fluctuations of reproductive success can explain the variation in flowering phenology within a population although seasonal light deterioration would serve as a selective force for flowering in the early season.     

Characterizing the interaction between the bogus yucca moth and yuccas: do bogus yucca moths impact yucca reproductive success?

Yucca moths are most well known for their obligate pollination mutualism with yuccas, where pollinator moths provide yuccas with pollen and, in exchange, the moth larvae feed on a subset of the developing yucca seeds. The pollinators, however, comprise only two of the three genera of yucca moths. Members of the third genus, Prodoxus, are the bogus yucca moths and are sister to the pollinator moths. Adult Prodoxus lack the specialized mouthparts used for pollination and the larvae feed on plant tissues other than seeds. Prodoxus larvae feed within the same plants as pollinator larvae and have the potential to influence yucca reproductive success directly by drawing resources away from flowers and fruit, or indirectly by modifying the costs of the mutualism with pollinators. We examined the interaction between the scape-feeding bogus yucca moth, Prodoxus decipiens, and one of its yucca hosts, Yucca filamentosa, by comparing female reproductive success of plants with and without moth larvae. We determined reproductive success by measuring a set of common reproductive traits such as flowering characteristics, seed set, and seed germination. In addition, we also quantified the percent total nitrogen in the seeds to determine whether the presence of larvae could potentially reduce seed quality. Flowering characteristics, seed set, and seed germination were not significantly different between plants with and without bogus yucca moth larvae. In contrast, the percent total nitrogen content of seeds was significantly lower in plants with P. decipiens larvae, and nitrogen content was negatively correlated with the number of larvae feeding within the inflorescence scape. Surveys of percent total nitrogen at three time periods during the flowering and fruiting of Y. filamentosa also showed that larval feeding decreased the amount of nitrogen in fruit tissue. Taken together, the results suggest that although P. decipiens influences nitrogen distribution in Y. filamentosa, this physiological effect does not appear to impact the female components of reproductive success.     

Multi-cycle synchronous protandry in raceme-like inflorescences of a bumblebee-pollinated herb Aconitum grossedentatum

Multi-cycle synchronous dichogamy is expected to be a mechanism for reducing self-pollination and sexual interference. It is often found in plants with umbellate inflorescences where pollinator movement is unpredictable, but not in plants with raceme inflorescences that are pollinated by bumblebees. Plants with raceme inflorescences often acropetally open flowers, resulting in an arrangement of females at lower level and males at upper level. This is good enough to preclude geitonogamy because bees tend to move upwardly within the inflorescences. Furthermore, although the degree of segregation of sexes varies among species, their intraspecific variations within a population have rarely been examined. Here, we present a synchronous protandry in bee-pollinated Aconitum grossedentatum, which has a raceme-like inflorescence and opens flowers basipetally. To evaluate the functional significance of synchronous dichogamy in mating, we firstly observed the distribution of sex phases of open flowers. Then, we assessed the effect of each phase flower on foraging behavior by pollinators and seed-set success. The inflorescences tended to exhibit either male- or female-phase flowers at any moment early in the flowering season, but the degree of segregation of sexes declined over time within a population. The degree of the segregation did not affect bumblebee visits to flowers, but it decreased seed-set success of female-phase flowers at that time. Our results demonstrated that synchronous protandry was beneficial for pollination success in A. grossedentatum by avoiding geitonogamy. Nevertheless, we also found asynchronous protandry late in the season, suggesting that the benefits by synchronous protandry decreased over the season.

     

Pollen dispersal in Yucca filamentosa (Agavaceae): the paradox of self-pollination behavior by Tegeticula yuccasella (Prodoxidae)

We investigated pollen dispersal in an obligate pollination mutualism between Yucca filamentosa and Tegeticula yuccasella. Yucca moths are the only documented pollinator of yuccas, and moth larvae feed solely on developing yucca seeds. The quality of pollination by a female moth affects larval survival because flowers receiving small amounts of pollen or self-pollen have a high abscission probability, and larvae die in abscised flowers. We tested the prediction that yucca moths primarily perform outcross pollinations by using fluorescent dye to track pollen dispersal in five populations of Y. filamentosa. Dye transfers within plants were common in all populations (mean ± 1 SE, 55 ± 3.0%), indicating that moths frequently deposit self-pollen. Distance of dye transfers ranged from 0 to 50 m, and the mean number of flowering plants between the pollen donor and recipient was 5 (median = 0), suggesting that most pollen was transferred among near neighbors. A multilocus genetic estimate of outcrossing based on seedlings matured from open-pollinated fruits at one site was 94 ± 6% (mean ± 1 SD). We discuss why moths frequently deposit self-pollen to the detriment of their offspring and compare the yucca-yucca moth interaction with other obligate pollinator mutualisms in which neither pollinator nor plant benefit from self-pollination.     

Reproduction of beetle‐pollinated Anaxagorea dolichocarpa (Annonaceae) is resilient to habitat disturbance in rainforest fragments

Strong evidence exists that fragmentation negatively affects pollination and plant reproduction, but little research has been conducted with regards to tropical trees. Specifically, effects of forest fragmentation on reproduction of plants with beetle‐pollinated flowers are poorly understood, and there are no data on the impact of fragmentation on reproduction in the structurally important tropical family Annonaceae. We examined the relationship between fragment size, pollinator abundance and seed set of beetle‐pollinated Anaxagorea dolichocarpa (Annonaceae) in a disturbed Brazilian Atlantic rainforest. Flower and fruit production and abundance of pollinators were quantified over ten months in three large (306–388 ha) and three small (6–14 ha) forest fragments. We recorded per flower pollinator abundance, resulting fruit set (fruits per flower) and seed set (monocarps per fruit) for a total of 209 individually marked flowers, and compared pollinator abundance in 186 flowers across all fragments. Flower and fruit production differed among fragments, but were similar for the combined large and small fragments. Between 64.8% (large fragments) and 66.3% (small fragments) of flowers received at least one pollinator. We found no significant difference in pollinator numbers between large and small fragments, and no correlation between pollinator abundance and fruit and seed set. A single visitor had a high probability of pollinating a flower. We conclude that 1) fragment size had no influence on pollinator number and plant reproductive success, and 2) generalist behavior of the pollinating beetles mitigate the risk of pollination failure for the reproductively specialized plant. However, further research may yet reveal genetic impoverishment of populations in small fragments due to restricted pollinator movements.