High invasive pollen transfer, yet low deposition on native stigmas in a Carpobrotus-invaded community

Background and Aims

Invasive plants are potential agents of disruption in plant–pollinator interactions. They may affect pollinator visitation rates to native plants and modify the plant–pollinator interaction network. However, there is little information about the extent to which invasive pollen is incorporated into the pollination network and about the rates of invasive pollen deposition on the stigmas of native plants.

Methods

The degree of pollinator sharing between the invasive plant Carpobrotus affine acinaciformis and the main co-flowering native plants was tested in a Mediterranean coastal shrubland. Pollen loads were identified from the bodies of the ten most common pollinator species and stigmatic pollen deposition in the five most common native plant species.

Key Results

It was found that pollinators visited Carpobrotus extensively. Seventy-three per cent of pollinator specimens collected on native plants carried Carpobrotus pollen. On average 23 % of the pollen on the bodies of pollinators visiting native plants was Carpobrotus. However, most of the pollen found on the body of pollinators belonged to the species on which they were collected. Similarly, most pollen on native plant stigmas was conspecific. Invasive pollen was present on native plant stigmas, but in low quantity.

Conclusions

Carpobrotus is highly integrated in the pollen transport network. However, the plant-pollination network in the invaded community seems to be sufficiently robust to withstand the impacts of the presence of alien pollen on native plant pollination, as shown by the low levels of heterospecific pollen deposition on native stigmas. Several mechanisms are discussed for the low invasive pollen deposition on native stigmas.Key words: Alien plant, Carpobrotus aff. acinaciformis, competition for pollinators, invasion, Mediterranean shrubland, plant-pollinator network, pollen loads, pollinator visits, stigma     

Intraspecific variation in morphology of spiny pollen grains along an altitudinal gradient in an insect-pollinated shrub

• Intraspecific variations in pollen morphological traits are poorly studied. Interspecific variations are often associated with pollination systems and pollinator types. Altitudinal environmental changes, which can influence local pollinator assemblages, provide opportunities to explore differentiation in pollen traits of a single species over short distances. The aim of this study is to examine intraspecific variations in pollen traits of an insect-pollinated shrub, Weigela hortensis (Caprifoliaceae), along an altitudinal gradient.
• Pollen spine phenotypes (length, number and density), pollen diameter, lipid mass (pollenkitt) around pollen grains, pollen production per flower and pollinator assemblages were compared at four sites at different altitudes.
• Spine length and the spine length/diameter ratio of pollen grains were greater at higher altitudes but not correlated with flower or plant size. Spine number and density increased as flower size increased, and pollen lipid mass decreased as plant size increased. Bees were the predominant pollinators at low-altitude sites whereas flies, specifically Oligoneura spp. (Acroceridae), increased in relative abundance with increasing altitude.
• The results of this study suggest that the increase in spine length with altitude was the result of selection favouring longer spines at higher-altitude sites and/or shorter spines at lower-altitude sites. The altitudinal variation in selection pressure on spine length could reflect changes in local pollinator assemblages with altitude.

     

Forest fragments influence pollination and yield of soybean crops in Chaco landscapes

Habitat remnants act as a source of pollinators potentially relevant for crop pollination and yield. This work analyzes how habitat loss influences pollinators, effective pollination and yield of soybean crops. The study area comprises ten sites adjacent to forest patches surrounded by a soybean matrix in central Argentina (eight sites in the season 2014–2015 and two sites in the season 2015–2016). Pollination was estimated by pollen deposition and frequency of flower visitors. Pollen deposition on stigmas and seed set were measured comparing open plants and plants with pollinator exclusion. These response variables were compared considering increasing distance to the forest edge and an increasing gradient of forest patch size. Bees were the most frequent visitors of soybean flowers, especially honeybees, but also at least three native bee species were recorded. Open plants showed higher rates of stigmatic pollen deposition than plants with pollinator exclusion, but seed set was similar. Total insect visitation rates, especially of native insects, decreased with distance to the forest edge and so did pollen deposition. Pollen deposition and seed set increased with increasing forest patch size for plants located near and far from the forest edge, respectively. Overall, our results suggest that the contribution of native pollinators from local forest patches is important for effective pollination across the landscape. Small patches of forest (approximately 1 ha.) guarantee pollinators to ensure plant yields similar to the yields of plants growing close to large patches, but only at short distances; while larger forest patches provide better pollination services for the crop at larger distances from the forest edge. However, we encourage further studies because results suggest that other factors may also influence soybean pollination and production.     

Pollinator dependence but no pollen limitation for eight plants occurring north of the Arctic Circle

Effective interactions between plants and pollinators are essential for the reproduction of plant species. Pollinator exclusion experiments and pollen supplementation experiments quantify the degree to which plants depend on animal pollinators and the degree to which plant reproduction is pollen limited. Pollen supplementation experiments have been conducted across the globe, but are rare in high latitude regions. To fill this knowledge gap, we experimentally investigated the dependence on animal pollinators and magnitude of pollen limitation in eight plant species north of the Arctic Circle in Lapland, Finland. Our findings show that all plant species were pollinator dependent, but not pollen limited. We discuss several mechanisms that might buffer our focal plants from pollen limitation, including plant and pollinator generalization, and attractive plant traits. Our results demonstrate that many plant species north of the Arctic Circle are currently receiving adequate pollinator service and provide a baseline for future comparisons of pollinator dependence and pollen limitation in the Arctic across space and time.     

Facial area and hairiness of pollinators visiting semi-natural grassland wild plants predict their facial pollen load

1. Consequences of a decline in pollination function in semi-natural ecosystems are largely unknown due to variability in pollinator effectiveness, that is, their contribution to pollen deposition alone. While pollination effectiveness has been shown to be related to body size and hairiness of pollinators for some crops, studies encompassing a wide diversity of pollinators interacting with wild plant communities are lacking. 2. Thus, the relationships between pollen load, which is a measurement of pollen transport ability and a proxy of pollinator effectiveness, and morphological traits of pollinators sampled in 16 grasslands in Moselle, France, were investigated. The area, hairiness, and pollen load of each pollinator's face were measured for 658 individuals from 127 bee and fly species interacting with 36 wild plant species. Pollinator dry mass was also measured on 543 individuals from 109 species. 3. Dry body mass and facial area of pollinators were positively linked. This study highlights that bees transported significantly more pollen grains on their face than flies. Furthermore, bees' faces were larger and hairier. We also found that pollinators' facial pollen load increased with facial area and hairiness when we considered all pollinators. However, hairiness is not significant within pollinator group (bees or flies), mirroring a potential phylogenetic signal. 4. Hence, this study shows a wide diversity of pollinator and plant species in which larger and hairier pollinators may transport more pollen grains, at least on their face. However, future studies involving other pollinator body parts are needed to generalise these relationships.     

Do pollinators influence seed-set in Banksia paludosa Sm. and Banksia spinulosa R. Br.?

The consequences of observed variations in pollinator activity for plant reproduction depend on the breeding system of the plant and also on whether pollination is a resource in short supply. These factors are frequently assumed rather than tested. In bagging experiments with Banksia paludosa in heath and B. spinulosa var. spinulosa in woodland, the present study demonstrated that seed-set does not occur by autogamy and that pollinators are indeed necessary. Experimental addition of outcrossed pollen to inflorescences failed to produce any increase in the mean number of seeds per inflorescence, measured for non-barren inflorescences, for either species. However, in B. paludosa, the addition of pollen increased the numbers of inflorescences that set seed from 20% (controls) to 45% (pollen-added treatment). This suggests either unusual patterns of pollen movement among and within plants or control of the pattern of seed-set within a plant. Pollen additions failed to alter seed-set in B. spinulosa. It is possible that a greater abundance of pollinators in the woodland ensures adequate pollination for these plants     

Change of floral orientation affects pollinator diversity and their relative importance in an alpine plant with generalized pollination system,Geranium refractum (Geraniaceae)

Floral orientation may affect pollinator attraction and pollination effectiveness, and its influences may differ among pollinator species. We, therefore, hypothesized that, for plant species with a generalized pollination system, changes in floral orientation would affect the composition of pollinators and their relative contribution to pollination. Geranium refractum, an alpine plant with downward floral orientation was used in this study. We created upward-facing flowers by altering the flower angle. We compared the pollinator diversity, pollination effectiveness, and pollinator importance, as well as female reproductive success between flowers with downward- and upward-facing orientation. Results indicated that the upward-facing flowers were visited by a wider spectrum of pollinators (classified into functional groups), with higher pollinator diversity than natural flowers. Moreover, due to influences on visitation number and pollen removal, the pollinator importance exhibited by the main pollinator groups differed between flower types. Compared with natural flowers, the pollination contribution of principal pollinators (i.e., bumblebees) decreased in upward-facing flowers and other infrequent pollinators, such as solitary bees and muscoid flies, removed more pollen. Consequently, stigmatic pollen loads were lower in upward- than in downward-facing flowers. These findings reveal that floral orientation may affect the level of generalization of a pollination system and the relative importance of diverse pollinators. In this species, the natural downward-facing floral orientation may increase pollen transfer by effective pollinators and reduce interference by inferior pollinators.     

Floral reward presentation favored the expression of male function in the pollen‐only flower Melastoma malabathricum

Abstract Animal‐pollinated plant species modulate the presentation of pollinator rewards to maximize reproductive success. In plants providing pollen as the only reward for pollinators, it is usually difficult to unravel the dual roles of reward presentation and the realization of male and female functions (pollen removal and deposition). Exploiting the two types of anther in the androecia of Melastoma malabathricum L., we examined whether the removal of pollen for reward is regulated primarily to favor male function or female function. Pollen removal by carpenter bees from the feeding and pollination anthers, as well as pollen deposition on the stigmas, were quantified during anthesis of M. malabathricum. There was no significant difference in pollen removal rates from the feeding and pollination anthers of M. malabathricum between the onset of anthesis and flower wilting. The stigmatic pollen loads exceeded the ovule number after three sonication bouts, and female function was satisfied earlier than male function. The results support the hypothesis that the presentation of pollination reward in this species is regulated primarily to favor the expression of male function, rather than female function, in agreement with the pollen‐donation hypothesis. A cooperative relationship between the feeding and pollination anthers was demonstrated in heterantherous flowers, which optimizes the balance in investments between pollinator rewards and “functional pollen” for gene transfer.     

Experimental reduction of pollinator visitation modifies plant–plant interactions for pollination

The strength of interactions between plants for pollination depends on the abundance of plants and pollinators in the community. The abundance of pollinators may influence plant associations and densities at which individual fitness is maximized. Reduced pollinator visitation may therefore affect the way plant species interact for pollination. We experimentally reduced pollinator visitation to six pollinator‐dependent species (three from an alpine and three from a lowland community in Norway) to study how interactions for pollination were modified by reduced pollinator availability. We related flower visitation, pollen limitation and seed set to density of conspecifics and pollinator‐sharing heterospecifics inside 30 dome‐shaped cages partially covered with fishnet (experimental plots) and in 30 control plots. We expected to find stronger interactions between plants in experimental compared to controls plots. The experiment modified plant–plant interactions for pollination in all the six species; although for two of them neighbourhood interactions did not affect seed set. The pollen limitation and seed set data showed that reduction of pollinator visits most frequently resulted in novel and/or stronger interactions between plants in the experimental plots that did not occur in the controls. Although the responses were species‐specific, there was a tendency for increasing facilitative interactions with conspecific neighbours in experimental plots where pollinator availability was reduced. Heterospecifics only influenced pollination and fecundity in species from the alpine community and in the experimental plots, where they competed with the focal species for pollination. The patterns observed for visitation rates differed from those for fecundity, with more significant interactions between plants in the controls in both communities. This study warns against the exclusive use of visitation data to interpret plant–plant interactions for pollination, and helps to understand how plant aggregations may buffer or intensify the effects of a pollinator loss on plant fitness.     

马先蒿属花冠形态的多样性与传粉式样的关系

马先蒿属(Pediculais)是有花植物中花冠形态多样化最为集中的属。该属主要的传粉者是熊蜂属(Bormbus)昆虫;在北美,熊蜂和蜂鸟是马先蒿植物一些种类有效的传粉者;也发现壁蜂(Osmia)为其传粉。不同的传粉机制要求某一特定的取食式样储藏和释放花粉。本文讨论了花冠类型的进化趋势与传粉式样和花粉形态的关系。传粉者的选择压力是决定花冠多样化的重要因素之一;花冠类型与传粉者和传粉行为紧密相关。马先蒿植物和传粉者的相互依赖与其花冠类型、功能和物候互相适应,但花冠类型与花粉形态两者之间似乎没有明显的一一对应关系。通过北美、日本和喜马拉雅不同地理分布马先蒿种类的比较研究表明,具有相同花冠类型的种类有着相同的传粉方式,花冠形态与传粉式样存在紧密的协同进化关系。     

Phylogenetic Community Context Influences Pollen Delivery to <Emphasis Type="Italic">Allium cernuum</Emphasis>

Few studies have examined how the number and identity of species in the neighbouring community influences the reproductive success of particular focal species. Pollen delivery, an important component of fitness of sexual plants, is a function of not just the floral traits of any particular individual, but of features of the population and community as it depends on pollinator abundance and preferences. Many pollinators in flowering communities will prefer patches with high floral abundance or diversity yet may exhibit lower floral constancy when more flowering species are present. Thus, pollination efficiency could increase or decrease with increased species richness and this will alter the selection pressures placed upon the floral traits (such as floral colour or reward) of any member of a particular community. Moreover, recent studies have indicated that plant-pollinator networks are phylogenetically structured (pollinators visit related plant species more than expected by chance) and this may be an important factor structuring flowering plant communities. Thus, the sheer number of species within a patch may be less important than the number of closely-related species. We investigate whether species richness or phylogenetic proximity of coflowering species influences the amount and proportion of conspecific pollen delivered to nodding onion, Allium cernuum, in fragment patches of Garry Oak meadows in South Western British Columbia, Canada. We find that pollen delivery depended upon the presence of close relatives far more than on species richness or population density, indicating a central role of the community structure on pollination in flowering plant communities. Insofar as pollen delivery relates to the relative number of seeds produced by members of the community, pollination may in turn determine the community structure of the next generation.     

Molecular assays of pollen use consistently reflect pollinator visitation patterns in a system of flowering plants

Determining how pollinators visit plants vs. how they carry and transfer pollen is an ongoing project in pollination ecology. The current tools for identifying the pollens that bees carry have different strengths and weaknesses when used for ecological inference. In this study we use three methods to better understand a system of congeneric, coflowering plants in the genus Clarkia and their bee pollinators: observations of plant–pollinator contact in the field, and two different molecular methods to estimate the relative abundance of each Clarkia pollen in samples collected from pollinators. We use these methods to investigate if observations of plant–pollinator contact in the field correspond to the pollen bees carry; if individual bees carry Clarkia pollens in predictable ways, based on previous knowledge of their foraging behaviors; and how the three approaches differ for understanding plant–pollinator interactions. We find that observations of plant–pollinator contact are generally predictive of the pollens that bees carry while foraging, and network topologies using the three different methods are statistically indistinguishable from each other. Results from molecular pollen analysis also show that while bees can carry multiple species of Clarkia at the same time, they often carry one species of pollen. Our work contributes to the growing body of literature aimed at resolving how pollinators use floral resources. We suggest our novel relative amplicon quantification method as another tool in the developing molecular ecology and pollination biology toolbox.     

雄全异株植物瘿椒树（省沽油科）的传粉生物学

从开花动态、传粉昆虫、花的形态结构、繁育系统、花粉活力和柱头可授性等方面研究了我国特有珍稀植物瘿椒树（Tapiscia sinensis Oliv.）的传粉生物学特性。瘿椒树是典型的雄全异株植物,两性花中含有功能性花粉,且自交亲和,但雄花花粉活力和萌发力是两性花的10倍以上。雄株和两性植株具有相同开花物候期,花期均为5月下旬至6月上旬,单花期为4-5天,雄花和两性花的5枚花药开裂的不同步性明显延长了散粉时间。两性花雌蕊先熟,柱头可授性较长。具有适应风媒和虫媒传粉的花部特征。传粉昆虫主要为蜜蜂科（Apidae）和食蚜蝇科（Syrphidae）昆虫,访花高峰期为8：30-10：30。维持瘿椒树雄全异株的可能机制是：雄株总体上增加了异交花粉的数量和质量;两性花的雄蕊为该物种提供了繁殖保障,同时为传粉者提供了报酬。     

雄全异株植物瘿椒树(省沽油科)的传粉生物学

从开花动态、传粉昆虫、花的形态结构、繁育系统、花粉活力和柱头可授性等方面研究了我国特有珍稀植物瘿椒树(Tapiscia sinensis Oliv.)的传粉生物学特性。瘿椒树是典型的雄全异株植物,两性花中含有功能性花粉,且自交亲和,但雄花花粉活力和萌发力是两性花的10倍以上。雄株和两性植株具有相同开花物候期,花期均为5月下旬至6月上旬,单花期为4-5天,雄花和两性花的5枚花药开裂的不同步性明显延长了散粉时间。两性花雌蕊先熟,柱头可授性较长。具有适应风媒和虫媒传粉的花部特征。传粉昆虫主要为蜜蜂科(Apidae)和食蚜蝇科(Syrphidae)昆虫,访花高峰期为8:30-10:30。维持瘿椒树雄全异株的可能机制是:雄株总体上增加了异交花粉的数量和质量;两性花的雄蕊为该物种提供了繁殖保障,同时为传粉者提供了报酬。     

Effects of multiple competitors for pollination on bumblebee foraging patterns and Mimulus ringens reproductive success

When co‐occurring plant species overlap in flowering phenology they may compete for the service of shared pollinators. Competition for pollination may lower plant reproductive success by reducing the number of pollinator probes or by decreasing the quality of pollen transport to or from a focal species. Pair‐wise interactions between plants sharing pollinators have been well documented. However, relatively few studies have examined interactions for pollination among three or more plant species, and little is known about how the outcomes and mechanisms of competition for pollination may vary with competitor species composition. To better understand how the dynamics of competition for pollination may be influenced by changes in the number of competitors, we manipulated the presence of two competitors, Lythrum salicaria and Lobelia siphilitica, and quantified reproductive success for a third species, Mimulus ringens. Patterns of pollinator preference and interspecific transitions in mixed‐species arrays were significantly influenced by the species composition of competitor plants present. Both pair‐wise and three‐species competition treatments led to a similar ～ 40% reduction in Mimulus ringens seed set. However, the patterns of pollinator foraging we observed suggest that the relative importance of different mechanisms of competition for pollination may vary with the identity and number of competitors present. This variation in mechanisms of competition for pollination may be especially important in diverse plant communities where many species interact through shared pollinators.     

Are there magnet plants in Australian ecosystems: Pollinator visits to neighbouring plants are not affected by proximity to mass flowering plants

Aggregations of resource-rich plants can act as “magnets” drawing pollinators from other plants. Magnets can have positive and negative impacts on co-flowering neighbours: enhanced pollination via a ‘spillover-effect’ or a reduction in pollination via competition. Support for the importance of magnets largely comes from studies conducted in the northern hemisphere. We used a comparative approach to test two hypotheses for three pairs of Australian native plants: (1) putative magnets attract a greater number and more diverse suites of pollinators than co-flowering species; and (2) the quantity, diversity and specificity of pollinators varies with distance from putative magnets. We surveyed pollinator activity on co-flowering plants before and after bagging to experimentally exclude pollinators from putative magnets, dominant flowering species with populations ranging in size from 700 to 4000 m². Selected focal species were found to be pollinator magnets, but did not appear to influence the pollination of neighbours. Prior to bagging, putative magnets received more visits but visitors were predominantly (90–100%) exotic honeybees (Apis mellifera). The number and diversity of pollinators on co-flowering species did not consistently increase when magnets were bagged. Moreover, pollinator visitation, diversity and constancy did not vary with distance from putative magnets before or after bagging. All sampled (n = 388) honeybees had pollen of only one plant species on their bodies and no honeybee sampled on a co-flowering species carried pollen of magnet species (n = 212). We found that interactions between pollinators and co-flowering Australian plants differ substantially from those reported for the northern hemisphere; this is most likely due to the impact of abundant, introduced honeybees.     

Predicting patterns of mating and potential hybridization from pollinator behavior

Hybridization in flowering plants is determined in part by the rate at which animal pollinators move between species and by the effectiveness of such movements in transferring pollen. Pollinator behavior can also influence hybrid fitness by determining receipt and export of pollen. We incorporated information on pollinator effectiveness and visitation behavior into a simulation model that predicts pollen transfer between Ipomopsis aggregata, Ipomopsis tenuituba, and hybrids. These predictions were compared with estimates of pollen transfer derived from movement of fluorescent dyes in experimental plant arrays. Interspecific pollen transfer was relatively uncommon in these arrays, whereas transfer between hybrids and the parental species was at least as common as conspecific transfer. Backcrossing was asymmetrical; I. aggregata flowers frequently received mixed loads of hybrid and conspecific pollen. The simulation suggests that these patterns of pollen transfer are largely explained by the visitation sequences of hummingbird and insect pollinators, with little contribution from mechanical isolation. Pollen receipt by hybrids exceeded that of both parental species in a year when pollinators preferred to visit F(1) and F(2) hybrids and was intermediate in another year when they preferred to visit I. aggregata. This suggests that natural variation in pollination may produce spatiotemporal variation in hybridization and hybrid fitness.     

Effect of invader removal: pollinators stay but some native plants miss their new friend

Removal of invasive species often benefits biological diversity allowing ecosystems’ recovery. However, it is important to assess the functional roles that invaders may have established in their new areas to avoid unexpected results from species elimination. Invasive animal-pollinated plants may affect the plant–pollination interactions by changing pollinator availability and/or behaviour in the community. Thus, removal of an invasive plant may have important effects on pollinator community that may then be reflected positive or negatively on the reproductive success of native plants. The objective of this study was to assess the effect of removing Oxalis pes-caprae, an invasive weed widely spread in the Mediterranean basin, on plant–pollinator interactions and on the reproductive success of co-flowering native plants. For this, a disturbed area in central Portugal, where this species is highly abundant, was selected. Visitation rates, natural pollen loads, pollen tube growth and natural fruit set of native plants were compared in the presence of O. pes-caprae and after manual removal of their flowers. Our results showed a highly resilient pollination network but also revealed some facilitative effects of O. pes-caprae on the reproductive success of co-flowering native plants. Reproductive success of the native plants seems to depend not only on the number and diversity of floral visitors, but also on their efficiency as pollinators. The information provided on the effects of invasive species on the sexual reproductive success of natives is essential for adequate management of invaded areas.     

Construction,validation, and application of nocturnal pollen transport networks in an agro‐ecosystem: a comparison using light microscopy and DNA metabarcoding

1. Moths are globally relevant as pollinators but nocturnal pollination remains poorly understood. Plant–pollinator interaction networks are traditionally constructed using either flower‐visitor observations or pollen‐transport detection using microscopy. Recent studies have shown the potential of DNA metabarcoding for detecting and identifying pollen‐transport interactions. However, no study has directly compared the realised observations of pollen‐transport networks between DNA metabarcoding and conventional light microscopy. 2. Using matched samples of nocturnal moths, we constructed pollen‐transport networks using two methods: light microscopy and DNA metabarcoding. Focussing on the feeding mouthparts of moths, we developed and provide reproducible methods for merging DNA metabarcoding and ecological network analysis to better understand species interactions. 3. DNA metabarcoding detected pollen on more individual moths, and detected multiple pollen types on more individuals than microscopy, although the average number of pollen types per individual was unchanged. However, after aggregating individuals of each species, metabarcoding detected more interactions per moth species. Pollen‐transport network metrics differed between methods because of variation in the ability of each to detect multiple pollen types per moth and to separate morphologically similar or related pollen. We detected unexpected but plausible moth–plant interactions with metabarcoding, revealing new detail about nocturnal pollination systems. 4. The nocturnal pollination networks observed using metabarcoding and microscopy were similar yet distinct, with implications for network ecologists. Comparisons between networks constructed using metabarcoding and traditional methods should therefore be treated with caution. Nevertheless, the potential applications of metabarcoding for studying plant–pollinator interaction networks are encouraging, especially when investigating understudied pollinators such as moths.     

Intrinsic and extrinsic factors acting on the reproductive process in alpine‐snowbed plants: roles of phenology,biological interaction,and breeding system

Pollinator activity and competition for pollinators lead to quantitative and qualitative pollen limitations on seed production and affect the reproductive success of plant species, depending on their breeding system (e.g., self‐compatibility and heterospecific compatibility) and genetic load (e.g., inbreeding depression and hybrid inviability). In alpine ecosystems, snowmelt regimes determine the distribution and phenology of plant communities. Plant species growing widely along a snowmelt gradient often grow with different species among local populations. Their pollinators also vary in their abundance, activity, and behavior during the season. These variations may modify plant–pollinator and plant–plant interactions. We integrated a series of our studies on the alpine dwarf shrub, Phyllodoce aleutica (Ericaceae), to elucidate the full set of intrinsic (species‐specific breeding system) and extrinsic factors (snow condition, pollinator activity, and interspecific competition) acting on their reproductive process. Seasonality of pollinator activity led to quantitative pollen limitation in the early‐blooming populations, whereas in the late‐blooming populations, high pollinator activity ensured pollination service, but interspecific competition for pollinators led to qualitative and quantitative pollen limitation in less competitive species. However, negative effects of illegitimate pollen receipt on seed‐set success might be reduced when cryptic incompatibility systems (i.e., outcross pollen grains took priority over self‐ and heterospecific pollen grains) could effectively prevent ovule and seed discounting. Our studies highlight the importance of species‐specific responses of plant reproduction to changing pollinator availability along environmental gradients to understand the general features of pollination networks in alpine ecosystems.