Reproductive success of individuals with different fruit production patterns. What does it mean for the predator satiation hypothesis?

The predator satiation hypothesis states that synchronous periodic production of seeds is an adaptive strategy evolved to reduce the pressure of seed predators. The seed production pattern is crucial to the predator satiation hypothesis, but there are few studies documenting the success of individuals that are in synchrony and out of synchrony with the whole population. This study is based on long-term data on seed production of Sorbus aucuparia and specialised pre-dispersal seed predation by Argyresthia conjugella, in a subalpine spruce forest in the Western Carpathians (Poland). At the population level, we tested whether functional and numerical responses of predators to the variation of fruit production operate. At the individual level, we tested whether individuals with higher interannual variability in their own seed crops and higher synchrony with the population have higher percentages of uninfested fruits. The intensity of pre-dispersal seed predation was high (average 70 %; range 19–100 %). There were both functional and numerical responses of predators to the variation of fruit production at the population level. We found that individuals that were expected to be preferred under seed predator pressure had higher reproductive success. With increasing synchrony of fruit production between individual trees and the population, the percentage of infested fruits decreased. There was also a negative relationship between the interannual variation in individual fruit production and the percentage of infested fruits. These results confirm selection for individuals with a masting strategy. However, the population does not seem well adapted to strong seed predation pressure and we suggest that this may be a result of prolonged diapause of A. conjugella.     

Temporal variations in seed dispersal patterns of a bird-dispersed tree, <Emphasis Type="Italic">Swida controversa</Emphasis> (Cornaceae), in a temperate forest

The seed dispersal patterns of bird-dispersed trees often show substantial seasonal and annual variation due to temporal changes in frugivorous bird and bird-dispersed fruit distributions. Elucidating such variation and how it affects plant regeneration is important for understanding the evolution and seed dispersal maintenance strategies of these plants. In this study, we investigated the seed dispersal quantity and distance of a bird-dispersed plant, Swida controversa, for 2 years and detected large seasonal variations in dispersal pattern. Early in the fruiting season, short seed dispersal distance and large amounts of fruit consumption by birds (seed dispersal quantity) were observed. In contrast, late in the fruiting season, a long seed dispersal distance and small seed dispersal quantity were observed. This relationship between seed dispersal distance and quantity may help to maintain constant seed dispersal effectiveness during the long S. controversa fruiting season. Annual variation was also detected for both seed dispersal quantity and distance. More effective seed dispersal was achieved in the masting year, because both seed dispersal quantity and distance were greater than that in the non-masting year. These seed dispersal dynamics may contribute to the evolution and maintenance of S. controversa masting behavior. Thus, we identified substantial temporal variation on both seasonal and annual scales in the seed dispersal pattern of a bird-dispersed plant. The temporal variation in seed dispersal pattern revealed in this study probably plays a substantial role in the life history and population dynamics of S. controversa.     

Population and individual level of masting in a fleshy-fruited tree

Masting is usually considered as a population phenomenon but it results from individuals?? reproductive patterns. Studies of individual patterns of seed production and their synchrony are essential to an understanding of the mechanisms of masting. The aim of this study was to find the relationship between population and individual levels of masting. We examined individuals?? contribution to masting, considering their endogenous cycles, interannual variability and associated weather cues, as well as inter-individual synchrony of fruit production. We studied masting of Sorbus aucuparia L., which in Europe is one of the most common trees bearing fleshy fruits and is strongly affected by a specialized seed predator. The data are 11-year measurements of fruit production of 250 individuals distributed on a 27-ha area of subalpine forest in the Western Carpathians (Poland). Population- and individual-level interannual variability of fruit production was moderate. Synchrony among individuals was relatively high for all years, but the trees were much less synchronized in heavy crop years than in years of low fruit production. Weak synchrony among trees for heavy production years suggests that the predator satiation hypothesis does not explain the observed masting behavior. Fruit production, both at individual and at population level, was highly correlated with weather conditions. However, the presence of masting cannot be fully explained by the resource-matching hypothesis either. We suggest that adverse weather conditions effectively limit fruit production, causing high inter-individual synchrony in low crop years, whereas the unsynchronized heavy crop years seem to have been affected by individually available resources.     

Nocturnal and diurnal pollination of Clerodendrum molle (Verbenaceae) in the Gal��pagos Islands

The primary hypothesis of this study was that in the Galápagos Islands, fruit and seed set via nocturnal pollination would exceed that of diurnal pollination because of the greater insect activity at night typical of hot, arid regions. Clerodendrum molle, a widespread member of the Galápagos flora was submitted to pollination experiments, visitor observations, nectar sampling, pollen transfer studies, pollen?Covule ratio studies, and pollen measurements. Flowers set fruit and seed via open pollination, autonomous autogamy, facilitated autogamy, facilitated cross-pollination, diurnal pollination, and nocturnal pollination. Results indicate no significant difference in fruit set. Cross-pollinated flowers showed a significant increase in seed set over all treatments except facilitated autogamy. Nocturnal and diurnal fruit and seed set did not differ significantly. Nocturnal visitors included ants, spiders, hawk moths, and roaches whereas diurnal visitors included carpenter bees and ants. Galápagos members of C. molle exhibit incomplete protandry and set fruit via autonomous autogamy as a result of natural selection in an environment with few faithful pollinators. Overall low fruit and seed set are likely because of a combination of pollen and resource limitation, the latter exacerbated by nectar robbing. Studies of island angiosperms are crucial for complete understanding of the population dynamics of indigenous plants, which can assist conservation officials in protecting these species.     

Pollination of the heterostylous Galápagos native, <Emphasis Type="Italic">Cordia lutea</Emphasis> (Boraginaceae)

The hypothesis of this study was that in the Galápagos Islands, fruit and seed set via nocturnal pollination would exceed that of diurnal pollination due to greater insect activity at night typical of hot, arid regions. Cordia lutea, a heterostylous member of the Galápagos flora, was submitted to pollination experiments, visitor observations, nectar sampling, pollen transfer studies, pollen-ovule ratio studies, and pollen measurements. Flowers set fruit and seed via open pollination, autonomous autogamy, facilitated autogamy, facilitated cross-pollination, diurnal pollination, and nocturnal pollination. There was a significant difference in fruit set between flowers experiencing legitimate cross-pollinations (pin × thrum) and those experiencing all other pollination treatments except facilitated autogamy. There was no significant difference in seed set among any of the treatments, but there was a trend toward greater seed set for flowers experiencing open-pollination, legitimate cross-pollination, and nocturnal pollination. There was no significant difference in fruit set or seed set between flowers experiencing diurnal pollination and nocturnal pollination, although there was a trend toward greater seed set resulting from nocturnal pollination. Carpenter bees were the most effective diurnal pollinators, whereas moths were the most effective nocturnal pollinators. Of the two, moths are more efficient at transporting pollen from plant to plant. Results indicate that an overall low productivity of this species is due to pollen limitation exacerbated by nectar robbing. Cordia lutea exhibits a mixed mating system, producing a relatively low level of fruits through a combination of self- and cross-pollination, facilitated by the relatively few insects that are available.     

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.     

Impact of habitat structure and fruit abundance on avian seed dispersal and fruit predation

So far, it is poorly understood how differential responses of avian seed dispersers and fruit predators to changes in habitat structure and fruit abundance along land-use gradients may translate into consequences for the seed dispersal of associated plants. We selected a gradient of habitat modification (forest, semi-natural, and rural habitat) characterized by decreasing tree cover and a high variation in local fruit availability. Along this gradient we quantified fruit removal by avian seed dispersers and fruit predators from 18 Sorbus aucuparia trees. We analyzed the relative importance of tree cover and fruit abundance in explaining species richness, abundance and fruit removal rates of both guilds from S. aucuparia trees. Species richness and abundance of seed dispersers decreased with decreasing tree cover, whereas fruit removal by seed dispersers decreased with decreasing fruit abundance independent of tree cover. Both variables had no effect on species richness, abundance and fruit removal by fruit predators. Consequently, seed dispersers dominated relative fruit removal in fruit-rich sites but the dispersal/predation ratio shifted in favor of predation in fruit-poor habitat patches. Our study demonstrates that variation in local habitat structure and fruit abundance can cause guild-specific responses. Such responses may result in a shift in fruit removal regimes and might affect the dispersal ability of dependent fruiting plants. Future studies should aim at possible consequences for plant recruitment and guild-specific responses of frugivores to disturbance gradients on the level of entire plant–frugivore associations.     

The birds and the seeds: opportunistic avian nectarivores enhance reproduction in an endemic montane aloe

Opportunistic bird pollination has become more evident in studies that confirm distinct differences in floral adaptations that attract opportunistic, rather than specialist, bird pollinators. Pollination syndrome studies investigating the effectiveness of different pollinator guilds on reproduction seldom do so by measuring seed viability. We studied pollination in Aloe peglerae, a high altitude endemic succulent of the Magaliesberg mountain range, previously thought to be largely sunbird (specialist) pollinated. Using field observation and pollinator exclusion treatments, i.e. (i) open to all visitors, (ii) bird excluded, and (iii) all visitors excluded, we established that birds contributed significantly more to fruit (2.3–5.6 times) and seed (1.3–1.4 times) set than insect or self-pollination, respectively. Overall, pollination by opportunistic avian nectarivores amplified seed production per aloe ~7 and 10 times compared to insects and self-pollination, respectively. One of three opportunistic nectarivores, the Cape Rock-Thrush (Monticola rupestris), played a significant role in pollination, contributing ~60 % of all probes at inflorescences. The difference in reproductive output between insect visited and visitor excluded flowers was not significant and suggests possible self-pollination in A. peglerae which is particularly unusual in Aloe species. Breeding system experiments would help clarify this. In assessing the effectiveness of pollinator guild on seed viability, we found no differences in percentage seed viability, seed germination or seedling emergence between exclusion treatments. Seed viability and germination were low and variable; however, ~19 % seedling emergence was observed across the treatments. Practically, the net effect of bird pollination may result in 8–12 times more potential seedlings compared to insect and self-pollination respectively. These findings highlight the importance of pollination by opportunistic avian nectarivores in Aloe.     

INTERPOPULATIONAL VARIATION IN FRUIT PRODUCTION: THE ROLE OF POLLINATION-LIMITATION IN THE OLYMPIC MOUNTAINS

Fruit set varied from a mean of 44% to 93% among six populations of Veronica cusickii L. (Scrophulariaceae) spanning a distance of 13 km in the Olympic Mountains, WA. Hand pollinations in three populations showed that this variation resulted primarily from differences in the level of limitation by insect pollination. In every pollination, hand-pollinated flowers averaged at least 82% fruit set. In 1981 and 1982, addition of excess pollen significantly increased mean fruit set per plant in the Blue Mountain population, but not in two other populations with higher natural fruit sets. At Blue Mountain, hand pollination more than doubled the mean seed set of V. cusickii and also significantly increased seed set in two of three other species visited primarily by flies or solitary bees. Pollination-limitation appears to be common at this site where the weather is frequently cold and damp.     

Floral morph composition and pollen limitation in the seed set of <Emphasis Type="Italic">Nymphoides indica</Emphasis> populations

We investigated the floral morph composition and seed set of the populations in a heterostylous aquatic plant, Nymphoides indica O. Kuntze (Menyanthaceae). The bias of floral morph ratio in the populations was negatively correlated with the seed set. In the populations with biased floral morph ratio, the pollen on the stigma of the common morphs were dominated by pollen of the same morph, resulting in reduced seed set. The addition of pollen of the opposite morph on the stigmas of the common morph resulted in an increase of fruit and seed set rates. The intermorph pollination rate and the fruit and seed set rates of Nymphoides indica were highest when two floral morphs were close in the populations. Various insect species including Lepidoptera, Diptera and Hymenoptera visited the flowers. However, geitonogamous pollination was common because of the short flying distance of the pollinators. These results indicate that the seed set of Nymphoides indica is limited by the shortage of compatible pollens and that the success of intermorph pollination is influenced by spatial distribution of the two floral morphs. As Nymphoides indica is endangered, conservation of the populations with high fecundity is proposed by us.     

Masting of rowan <Emphasis Type="Italic">Sorbus aucuparia</Emphasis> L. and consequences for the apple fruit moth <Emphasis Type="Italic">Argyresthia conjugella</Emphasis> Zeller

 Masting of rowan Sorbus aucuparia L. has been studied in 45 sites in southern Norway for 22 years. We present data on the year-to-year variation in fruit setting of rowan, and show that masting is spatially synchronous in Norway and probably all over Fennoscandia. The apple fruit moth Argyresthia conjugella Zeller is an important seed predator on rowan. We present data on the abundance of apple fruit moth in rowanberries during these years and discuss the consequences of masting and intermasting of rowan for apple fruit moth as a pest of apple. We conclude that growth and climate have little impact on flowering intensity and suggest that masting of rowan is an adaptive defense against seed predation and a new example of predator satiation: intermast years inhibit predators and prepare the rowan for the subsequent mast. Received: September 3, 2001 / Accepted: February 24, 2003     

Pollinator supplementation mitigates pollination deficits in smallholder avocado (Persea americana Mill.) production systems in Kenya

Avocado (Persea americana Mill.) is a major horticultural crop that relies on insect mediated pollination. In avocado production, a knowledge gap exists as to the importance of insect pollination, especially in East African smallholder farms. In this study, conducted in a leading smallholder avocado production region in Kenya, we assessed the dependence of avocado fruit set on insect pollination and whether current smallholder production systems suffer from a deficit in pollination services. Furthermore, we assessed if supplementation with colonies of the Western honey bee (Apis mellifera L.) to farms mitigated potential pollination deficits. Our results revealed a very high reliance of avocado on insect pollinators, with a significantly lower fruit set observed for self- and wind-pollinated (17.4%) or self-pollinated flowers (6.4%) in comparison with insect-pollinated flowers (89.5%). We found a significant pollination deficit across farms, with hand-pollinated flowers on average producing 20.7% more fruits than non-treated open flowers prior to fruit abortion. This pollination deficit could be compensated by the supplementation of farms with A. mellifera colonies. Our findings suggest that pollination is limiting fruit set in avocado and that A. Mellifera supplementation on farms is a potential option to increase fruit yield.     

Pollination biology and breeding system in five nocturnal species of <Emphasis Type="Italic">Oenothera</Emphasis> (Onagraceae): reproductive assurance and opportunities for outcrossing

The capacity to produce seed, both by selfing and outcrossing, or mixed mating strategies, is considered a mechanism for overcoming unpredictable pollinator availability. In the present study, we investigate breeding system, insect visitations and the role of insect visitors in the pollination of five species of Oenothera subsect. Oenothera. Field experiments showed that autonomous selfing occurs at bud stage, prior to the opening of the flower. Control flowers showed similar seed set to hand-pollinated flowers, whereas emasculated flowers and those subject to open pollination set fewer seed. These results are consistent with the hypothesis that the investigated Oenothera exhibit a great capacity for autonomous selfing and that selfing is selected in order to provide reproductive assurance. Although flowers were visited mostly by nocturnal lepidopterans, these insects did not precipitate pollination and are thus considered nectar thieves. Conversely, analysis of pollen loads and behavior during foraging by diurnal insect visitors revealed that honeybees and bumblebees are the probable pollinators. We conclude that production of flowers capable of autonomous selfing at bud stage, followed by anthesis and opportunities for outcrossing, probably improves the invasive potential of these Oenothera in Europe, together with a rapid increase in their populations, even when pollinators are scarce.     

Relative contributions to seed production by floral visitors of slickspot peppergrass, Lepidium papilliferum (Brassicaceae)

Assessing the relative contributions to seed production made by different types of floral visitors is fundamental to understanding the evolution of floral morphology and the influence that particular pollinator taxa have on plant fitness and reproduction. This 3-year study examined the pollinator activity and the seed production in three populations of Lepidium papilliferum, a threatened mustard endemic to sagebrush-steppe habitat in southwest Idaho. Relative amounts of time visitor taxa spent foraging on flowers, visitation rates (number of flowers visited per unit time during a foraging bout), and pollination effectiveness (fruit set per single visit to a virgin flower) were recorded for each of 12 insect taxa that visited L. papilliferum flowers. Relative contributions to seed production were calculated as the product of relative interaction frequencies (the relative number of flowers visited by each taxon—the “quantity” component of pollination) and pollination effectiveness (fruit set per single visit to a virgin flower—the “quality” component of pollination). Despite the superiority of some insect taxa in terms of pollination effectiveness, estimates of relative pollinator contributions to seed production were influenced primarily by an insect taxon’s interaction frequency with flowers. Pollinator assemblages varied widely both spatially and temporally, which suggest that L. papilliferum is not under strong selective pressure to shift from its generalist pollination strategy toward greater specialization. For this threatened plant, reliance on a diverse assemblage of insect pollinators may serve as an important buffer against disruption in reproductive success caused by fluctuations in population sizes of individual pollinator taxa.     

Pollination biology in an endangered rocky mountain toadflax (Linaria cavanillesii)

Knowledge about the reproductive system of species inhabiting rocky habitats is scarce. The reproductive biology (floral biology, experimental pollination, insect visits, inbreeding depression, and seed predation) of the rupicolous Linaria cavanillesii was analyzed under field and experimental conditions. Self-compatibility was revealed by the high fruit set, seed set, and seed mass in the pollination experiment. Furthermore, results disclose that this species does not need insect visitors for seed production since fruit set after autonomous self-pollination was similar to that by hand cross-pollination. Self-offsprings were not affected by a strong degree of inbreeding depression in early life-cycle stages. Seed predation by Cucurlionidae is the main limiting factor of fruit and seed production in this species. Contrary to other perennial species of Linaria previously studied, L. cavanillesii represents the first clear report of self-fertility.     

Effects of natural and artificial pollination on fruit and offspring quality

Worldwide, many crops rely on insect pollination. Insufficient pollination can reduce fruit and seed set by directly reducing pollen deposition, and can also affect offspring quality, such as growth rate and resistance to herbivores, by limiting outcrossing opportunities. Both effects are important in fruit agroecosystems where fruit size and the quality of seeds for re-planting are dependent on sufficient pollination. We experimentally manipulated pollination of the cape gooseberry, Physalis peruviana L. (Solanaceae), to test the effects of honey and bumble bee pollination compared to manual outcrossing and autonomous self-pollination on fruit and offspring characteristics. Compared to manual and self-pollination, bee pollination increased fruit size, seed set and germination rates, supporting the hypothesis that sufficient pollination increases plant fitness. Interestingly, plant growth rate and herbivore resistance were significantly and marginally greater in manually outcrossed plants compared to self-pollinated offspring, suggesting that inbreeding reduces offspring quality. Herbivore resistance and plant growth did not differ between one honeybee visit and self-pollination suggesting that multiple pollinator visits are needed to prevent inbreeding events. Our data suggest that the quantity and quality of pollen deposited by bee visitation can significantly alter ecologically and economically relevant traits in this agroecosystem.     

Status of pollinators and their efficiency in coffee fruit set in a fragmented landscape mosaic in South India

The region of Kodagu, South India, comprises a fragmented landscape with a high density of remnant forest patches dispersed within a mosaic dominated by shaded coffee agro-forests. We evaluated the role of self, wind and insect pollination to Coffea canephora production in this landscape. The giant Asian honeybee, Apis dorsata, which nests in remnant forests, was the main pollinator of coffee (accounting for 58% of the floral visitors). The proportion of flowers that developed into fruits was highest when hand cross-pollinated (44%), followed by open- (insect and wind combined; 33%) and wind- (22.1%) pollination treatments. Pollination by bees therefore increases fruit production by 50% over that achieved by wind. Self-pollination (1.7%) and no pollination (1%) treatments produced very low fruit set, emphasizing the importance of cross-pollination in C. canephora. Unlike measures of pollination success, initial fruit set (five weeks after flowering) proved an unreliable proxy for final fruit set. Size of adjoining forest fragments (mostly 0.3–20 ha, with a few exceeding 200 ha) positively influenced pollinator visitation to coffee flowers, but distance to such fragments had no influence on pollination. This study demonstrates the importance of cross-pollination for crop production in C. canephora, the important contribution that pollinating insects make to coffee production, and the benefits of relatively large forest fragments within the landscape mosaic to support insect pollinators of coffee. A comparison of pollinator composition to that of 100 years ago indicated that coffee pollination services remained intact despite changes in pollinator community composition.     

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.     

Plants,position and pollination: Planting arrangement and pollination limitation in a revegetated eucalypt woodland

The spatial arrangement of plants is a key determinant of pollination services in natural ecosystems. Despite this, plant arrangements are rarely considered an important characteristic of revegetated communities and this may be limiting successful pollination dynamics in these re‐created systems. We assessed if aggregated South Australian Blue Gum (Eucalyptus leucoxylon, F. Muell) had greater pollination success than more dispersed trees by measuring fruit set, seed production and germination in a revegetated eucalypt woodland. The proportion of buds that developed into fruit (fruit set) was similar between aggregated (five flowering Blue Gum within 30 m) and dispersed (no flowering Blue Gum within 30 m) trees (<14%). Aggregated and dispersed trees produced a similar number of seeds per fruit in 2015, when fewer trees flowered and those that flowered produced fewer flowers (ca 8 seeds/fruit). In 2016, when flowering was more abundant, aggregated trees produced more seeds per fruit than dispersed trees (12 seeds/fruit compared to 4 seeds/fruit). Despite differences in seed number, there was no difference in the quality of seed produced, indicating outcrossed pollen was received by both aggregated and dispersed trees. Although outcrossing was likely, this did not prevent pollination limitation, with the addition of outcrossed pollen increasing fruit and seed set for trees in both arrangements. Consequently, we propose that planting individuals of the same species (conspecifics) in clumps, rather than intermixing species, can increase seed set in revegetated eucalypts, particularly in good flowering years. However, aggregated plantings will be most effective if the needs and foraging behaviour of pollinators are also considered, to attract and sustain pollinators in revegetated systems, thereby minimizing the risk of pollination limitation.     

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.