Threats and benefits of invasive alien plant species on pollinators

Invasive alien plant species are usually disliked due to their high pressure on native communities. However, their ecological effects on pollinators are complex: some species provide abundant floral resources, boosting the number of pollinators, while they often disrupt plant-pollinator interactions by outcompeting native plants. Our direct knowledge is mainly based on single-species studies, while understanding the mechanism of these complex ecological interactions needs multi-species field-based approaches. It is also imperative to clarify the pros and cons of invasive plants and drivers of invasion from the perspective of pollinators. We conducted a standard protocol-driven regional study in Central and Eastern Europe, comparing 6-7 invaded and non-invaded sites of 12 herbaceous invasive plant species. We sampled floral resources, bees, and hoverflies before and during the flowering of the invasive plants. We analysed the effects of plant invasion at the invasive plant species level and in combined analyses, and tested whether the life span (perennial vs. annual) and flowering time (early-, middle-, and late-flowering) of invasive plants affect the abundance, species richness, diversity and species composition of native plants and pollinators. The combined analyses showed lower abundance and species richness of flowering plants and pollinators before, and higher abundance of both during the flowering of invasive plants in invaded sites. However, invasive plants had significant species-specific effects. Perennial invasive plants had a stronger negative impact on floral resources and pollinators already before their flowering compared to annuals. Flowering time of invasive plants affected the pollinator guilds differently. We suggest that in certain critical time periods of the year, invasive plants might provide the dominant foraging resources for pollinators in an invaded ecosystem. But, they also often cause significant losses in native floral resources over the year. Instead of simple eradication, careful preparation and consideration might be needed during removal of invasive plants.     

POLLINATION ECOLOGY OF LABIATAE IN A PHRYGANIC (EAST MEDITERRANEAN) ECOSYSTEM

This study was conducted in a phryganic (East Mediterranean) ecosystem at Daphni, near Athens, Greece. The Labiatae, represented by ten species belonging to nine genera, dominate in this ecosystem type. They flower from February to July. Both flowering time and nectar quantity are related to the species ability to tolerate intense water stress. Labiatae are visited by 201 insect species. Of these, 43 are exclusively supported by the family and 37 are monotropous. Solitary bees (mainly Anthophoridae, Megachilidae, Halictidae) constitute 47.3% of pollinators. The family is important in hosting specialized bees (15 species) in phrygana, particularly late in the flowering season. Labiatae species form two equally represented groups in this system; namely, the late winter-early spring (early) flowering, visited by relatively few pollinator species, and the late spring-summer (late) flowering species, visited by numerous pollinators. This temporal distinction is accompanied by different pollination profiles that include duration of anthesis, reward to pollinators, floral attractiveness, and flower character differentiation. All of these attributes are maximized in the early flowering period. This strategy suggests a mechanism for resource partitioning at a time when the pollinator resource is limited and competition for the services of pollinators is expected to be intense. Contrary to the current theory concerning cornucopian species, the copiously rewarding flowers of Labiatae in phrygana are not those abundantly serviced by pollinators.     

Mechanisms that limit pollinator range in Ericaceae

Studies were conducted in 2001-2003 at Valdai National Park (Novgorod region) and at the Zvenigorod biological station of Moscow State University. The morphology of flowers, flowering dynamics and composition of insect visiting flowers of Ericaceae species: Andromeda polifolia, Chamaedaphne calyculata, Ledum palustre, Oxycoccus palustris, Vaccinium myrtillus, V. uliginosum, and V. vitis-idaea L. were studied. Some species of insects visiting flowers were excluded from the list of pollinators on the basis of observation on their behavior. L. palustre was visited mainly by flies where as other investigated species were visited mainly by bumblebees. In some cases bumblebees were the only visitors of the investigated plants. Mechanisms that protect flowers from flies and short-tongued solitary bees visits and ensure a best pollination by bumblebees are various among different species of Ericaceae. Efficiency of nectary protection also differs among different plant species and is defined by particularities of their habitats and flowering phenology. As far as all species of this family during the flowering are dominants in typical habitats, a competition for the pollination with species of other families in most cases is megligible. Flowering periods of V. vitis-idaea and V. myrtillus in forest ecosystems overlapped weakly. Moreover, V. myrtillus is pollinated mainly by bumblebee queens where as pollinators of V. vitis-idaea are bumblebee workers, solitary bees and horse flies. The other investigated plant species inhabit only oligotrophic peat bogs. Thery are pollinated by bumblebees but periods of flowering are not overlapped and consequently follow one after another. L. palustre and V. uliginosum flower simultaneosly but they are pollinated by different pollinators.     

The ecological pollination syndromes of insect-pollinated plants in an alpine meadow

The insect pollination of an alpine plant community consisting of herbs and shrubs, was observed on Mt. Kisokoma-ga-take, central Honshu, Japan. There were two main groups of pollinators, syrphid flies and bumble bees. Although some shrubs were visited by both types of insects, other shrubs and the herbs were visited by either syrphid flies or bumble bees. Two types of herbs categorized by the difference of flower-visiting insects, the Syrphid-type and the Bombus-type, exhibited some clearly contrasting ecological characteristics such as the flowering behavior of individual plants, spatial distribution of the plant populations and segregation of flowering phenology at the community level. The Syrphid-type herbs were densely distributed throughout wide areas in the tall herb stand, and all the flowers borne by an individual plant bloomed simultaneously. Each species did not markedly segregate its flowering time from that of other species of the same type. The Bombus-type herbs were distributed locally and/or at low density, and the individual flowers borne by an individual plant showed staggered flowering times. Each species had a more strictly segregated flowering time. These ecological characteristics of these two flower types seemed to be related to the behavioral characteristics of their pollinators.     

Interrelation between the flower structure and composition of the pollinator groups for Dipsacaceae and Asteraceae with externally similar anthodia

The competitive relations between members of phylogenetically distant plant families Asteraceae (Centaurea and Cirsium) and Dipsacaceae (Knautia and Succisa) with purple anthodia, sharing a common wide range of pollen vectors and competing for them, were studied. The composition of pollen vectors is somewhat different in different plant species. Only bumble-bees, the most effective pollinators, were observed visiting every studied plants species. Syrphidae flies, Lepidoptera, Coleoptera, and some other insects were also observed in different proportions. The principal importance for pollination of the corolla tube size, correlating with the size of insect mouthparts, and the additional importance of particular traits of the inflorescence are confirmed. Convergent similarity of the aspect of anthodia in two species of different families is shown to be based on different structural and functional features. Insect pollinators are the factor of anthodia convergence. The plant species studied are divided into the following three groups, according to the proportion of bumble-bees among pollen vectors and to the range of species-specific pollinators; species coadapted to one pollinator taxon; species coadapted to two or three pollinator taxa; and species coadapted to many pollinator taxa. Asteraceae species in general (with the exception for Cirsium arvense) are characterized by constant contacts with a narrower range of pollinators than Dipsacaceae species (and Cirsium arvense), characterized by wider range of pollinators. Among flowering plants with similar anthodia, the tighter structural coadaptations of Asteraceae with their effective pollinators provide their greater competitive ability as compared to Dipsacaceae.     

珍稀濒危植物单性木兰传粉生态学研究

野外定位观测了单性木兰的花期物候、访花昆虫种类、访花频率、访花行为和同花期植物种类,并对其花粉散播距离和繁育系统进行了检测,旨在探讨制约单性木兰传粉过程的某些因素,为单性木兰的保护生物学提供科学依据。结果表明,单性木兰雄株和雌株在花期物候上存在差异,雌株在结实上存在明显的大小年现象。单性木兰以虫媒传粉为主,雄株访花昆虫30种,雌株访花昆虫仅14种,雌株和雄株共有的访花昆虫仅6种。单性木兰同花期植物共17种,其访花昆虫种类大部分与单性木兰的访花昆虫种类相同。蜂类和蝶类均非单性木兰的传粉者,其结实率低的原因不仅与访花昆虫种类少和访花频率少有关,更与其缺乏有效的传粉昆虫有关。     

Pollination systems in a warm temperate evergreen broad-leaved forest on Yaku Island

Animal pollination in a warm temperate evergreen broad-leaved forest was observed on Yaku-shima Island, south of Kyushu, Japan. Three groups of plants were categorized: canopy-flowering tree species, understory-flowering tree species, and climber and epiphyte species. Each of these formed different pollination systems. The canopy-flowering tree species had shallow, dish-shaped flowers and utilized various types of opportunistic pollinators. Most of the climber and epiphyte species had deep, tube-shaped flowers and specialized pollinators, although some climber species which bloomed in the canopy especially in winter, had opportunistic pollinators. The understory-flowering tree species had large dish- or funnel-shaped flowers and endothermic pollinators able to tolerate the dark and cold conditions under the canopy. The individual trees of canopy-flowering tree species produced large numbers of flowers simultaneously (mass-flowering) and had a well synchronized flowering period. Each canopy-flowering tree species segregated its flowering time from those of the anothers. Climber and epiphyte species and most of the understory-flowering tree species produced small numbers of flowers sequentially (extended flowering) and showed a long flowering period.     

Pollinator coupling can induce synchronized flowering in different plant species

Synchronous and intermittent plant reproduction has been identified widely in diverse biomes. While synchronous flowering is normally observed within the same species, different species also flower in synchrony. A well-known example of interspecific synchrony is “general flowering" in tropical rain forests of Southeast Asia. Environmental factors, such as low temperature and drought, have been considered as major trigger of general flowering. However, environmental cues are not enough to explain general flowering because some trees do not flower even when they encounter favorable environmental cues. We propose alternative explanation of general flowering; “pollinator coupling”. When species flower synchronously, the elevated pollen and nectar resource may attract increased numbers of generalist pollinators, with a concomitant enhancement of pollination success (facilitation). However, under these circumstances, plants of different species may compete with one another for limited pollinator services, resulting in declines in pollination success for individual species (competition). Here, we present a model describing resource dynamics of individual trees serviced by generalist pollinators. We analyze combinations of conditions under which plants reproduce intermittently with synchronization within species, and/or (sometimes) between different species. We show that plants synchronize flowering when the number of pollinators attracted to an area increases at an accelerating rate with increasing numbers of flowers. In this case, facilitation of flowering by different species exceeds the negative influence of interspecific plant competition. We demonstrate mathematically that co-flowering of different species occurs under a much narrower range of circumstances than intraspecific co-flowering.     

Phenotypic selection on flowering phenology and pollination efficiency traits between Primula populations with different pollinator assemblages

Floral traits have largely been attributed to phenotypic selection in plant–pollinator interactions. However, the strength of this link has rarely been ascertained with real pollinators. We conducted pollinator observations and estimated selection through female fitness on flowering phenology and floral traits between two Primula secundiflora populations. We quantified pollinator‐mediated selection by subtracting estimates of selection gradients of plants receiving supplemental hand pollination from those of plants receiving open pollination. There was net directional selection for an earlier flowering start date at populations where the dominant pollinators were syrphid flies, and flowering phenology was also subjected to stabilized quadratic selection. However, a later flowering start date was significantly selected at populations where the dominant pollinators were legitimate (normal pollination through the corolla tube entrance) and illegitimate bumblebees (abnormal pollination through nectar robbing hole which located at the corolla tube), and flowering phenology was subjected to disruptive quadratic selection. Wider corolla tube entrance diameter was selected at both populations. Furthermore, the strength of net directional selection on flowering start date and corolla tube entrance diameter was stronger at the population where the dominant pollinators were syrphid flies. Pollinator‐mediated selection explained most of the between‐population variations in the net directional selection on flowering phenology and corolla tube entrance diameter. Our results suggested the important influence of pollinator‐mediated selection on floral evolution. Variations in pollinator assemblages not only resulted in variation in the direction of selection but also the strength of selection on floral traits.     

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.     

Fly pollination of Linum lewish (Linaceae)

This study examines the reproductive biology of Linum lewisii Pursh. (Linaceae), a polyphilic species visited by small bees and generalist flies in montane Colorado. L. lewisii plants growing at different sites experience large temporal and spatial variations in pollinator visits. Their ability to attract both dipteran and hymenopteran pollinators allows pollination under varying conditions as pollinator pool composition changes. Although L. lewisii is self-compatible, hand-pollination studies indicate that insects are required for seed production. The relative effectiveness of fly and bee pollinators is assessed in terms of per-visit pollen deposition. Insect visitation patterns are combined with per-visit effectiveness data to evaluate the relative importance of different pollinator groups. Overall, bees tend to be more effective than flies in depositing pollen. However, in many instances flies appear to be responsible for more pollen deposition due to their higher visitation rates.     

Vulnerability of phenological synchrony between plants and pollinators in an alpine ecosystem

The relationship between flowering phenology and abundance of bumble bees (Bombus spp.) was investigated using 2 years of phenological data collected in an alpine region of northern Japan. Abundance of Bombus species was observed along a fixed transect throughout the flowering season. The number of flowering species was closely related to the floral resources for pollinators at the community scale. In the year with typical weather, the first flowering peak corresponded to the emergence time of queen bees from hibernation, while the second flowering peak corresponded to the active period of worker bees. In the year with an unusually warm spring, however, phenological synchrony between plants and bees was disrupted. Estimated emergence of queen bees was 10 days earlier than the first flowering date owing to earlier soil thawing and warming. However, subsequent worker emergence was delayed, indicating slower colony development. The flowering season finished 2 weeks earlier in the warm-spring year in response to earlier snowmelt. A common resident species in the alpine environment, B. hypocrita sapporoensis, flexibly responded to the yearly fluctuation of flowering. In contrast, population dynamics of other Bombus species were out of synchrony with the flowering: their frequencies were highest at the end of the flowering season in the warm-spring year. Therefore, phenological mismatch between flowers and pollinators is evident during warm years, which may become more prevalent in a warmer climate. To understand the mechanism of phenological mismatch in the pollination system of the alpine ecosystem, ground temperature, snowmelt regime, and life cycle of pollinators are key factors.     

A new species of Aspidistra (Ruscaceae s.l., Asparagales) from southern Vietnam, field observations on its flowering and possible pollination by flies (Phoridae)

The genus Aspidistra with almost 100 species is the most diverse in southern China and northern Vietnam. We describe a new species Aspidistra phanluongii N.Vislobokov from southern Vietnam. Species of Aspidistra are herbs characteristic of Southeast Asian forests. Flowering of these plants can be considered cryptic. There are no recorded field observations on phenology, biology of flowering or pollination of Aspidistra. Previously proposed pollinators of Aspidistra include collembolans, amphipods, fungus gnats (Diptera: Mycetophilidae, Sciaridae) and even slugs. We present observation data on the flowering of A. phanluongii in the wild. Flowers were visited by flies of Megaselia (Phoridae) and ants. Megaselia flies, well-known pollinators of numerous tropical plant species, are shown to be likely pollinators of Aspidistra phanluongii. The present study does not provide evidence of pollination by fungus gnats.     

POLLINATION AND POLLEN ENERGETICS IN MEDITERRANEAN ECOSYSTEMS

Most plants in Mediterranean ecosystems are insect pollinated, with pollen being the main reward to pollinators. The great majority of pollinators (70%) are bees and flies. We measured the energy content of pollen from 40 plant species in these ecosystems that represent abiotic and biotic pollination modes as well as the number of species of their pollinators. Pollen energy content correlates with pollinator diversity. Pollen of wind-pollinated plants contained less energy than that of insect-pollinated plants; there was no difference between insect-pollinated dicots and insect-pollinated monocots. The median date of flowering (from 1 January) estimated for each of the plant species did not vary significantly either with the number of pollinator species or with the energy content of pollen. The reasons for the differing values of pollen energy content are discussed; in particular, its relation to the type of pollen reserves, length of the flower style, and pollination enhancement.     

Mass flowering of dipterocarp forests in the aseasonal tropics

At irregular intervals of 2 to 10 years the aseasonal tropical rain forests in west Malesia come into heavy mass flowering, followed by mast fruiting. During a heavy flowering almost half the mature individuals and over 80% of the canopy and emergent tree Species in a forest may flower. This involves over 200 tree species in a forest flowering over a short period of 3–4 months. The pollination needs during a mass flowering appears to be overcome in several ways. A rapid increase in the number of pollinators seems to occur in the forest. This is partly caused by the migration of pollinators from the fringes of the forest to forage on the superabundance of flowers. At the same time, some groups of plants which share common pollinators appear to reduce pollinator competition by flowering in interspecific sequence. Many members of the family Dipterocarpaceae have evolved sequential flowering too. They also share unique pollinators, common flower thrips which appear to build up rapidly in numbers by feeding and breeding on the millions of dipterocarp flower buds which are present several weeks before the flowering. The environmental cue for this irregular, but widespread mass flowering can be traced to a small dip of about 2° C below mean night-time temperature for 4 or 5 nights. The conditions for such temperature drops occur during El Nino events.     

Pollination of Euphorbia dendroides by lizards and insects: Spatio-temporal variation in patterns of flower visitation

The patterns of flower visitation by lizards (Podarcis lilfordi, Lacertidae) and insects (mainly flies, bees and wasps) on the shrub Euphorbia dendroides, were studied in the island of Cabrera (Balearic Islands) during the flowering seasons of 1995 and 1996. Lizards act as true pollinators of the plant, moving large quantities of pollen within and among shrubs. To our knowledge, this is the first time that pollination by lizards has been empirically demonstrated. Variation in the quantitative component of pollination (frequency of visits × flower visitation rate) by the two groups of pollinators (lizards and insects) is documented at both spatial (within a plant population) and temporal scales (throughout the flowering season and between seasons). Variation in lizard density on a small spatial scale (within c. 200 m), presumably due to differences in vegetation cover, strongly affected their frequency of flower visitation. Insects were rather scarce, mainly because the plant flowers at a time (mid-March) when temperatures are still low. At the site where lizards were abundant, their frequency of flower visits was more than 3 times that of insects, they stayed on the shrubs about 3 times longer and visited about 8 times more cyathia per minute than did insects. Fruit and seed set were greater at this site, and this is attributed to the different frequency of flower visits by lizards, as shrubs are similar in size and produce similar amounts of cyathia in the two sites compared. Both, lizards and insects went more frequently to plants with large flower crops. However, flower crop was not associated with seed viability. We found no evidence for pollinator-mediated selection on plant traits related to fitness. Received: 28 August 1996 / Accepted: 26 February 1997     

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.     

How many flowering plants are pollinated by animals?

It is clear that the majority of flowering plants are pollinated by insects and other animals, with a minority utilising abiotic pollen vectors, mainly wind. However there is no accurate published calculation of the proportion of the ca 352 000 species of angiosperms that interact with pollinators. Widely cited figures range from 67% to 96% but these have not been based on firm data. We estimated the number and proportion of flowering plants that are pollinated by animals using published and unpublished community‐level surveys of plant pollination systems that recorded whether each species present was pollinated by animals or wind. The proportion of animal‐pollinated species rises from a mean of 78% in temperate‐zone communities to 94% in tropical communities. By correcting for the latitudinal diversity trend in flowering plants, we estimate the global number and proportion of animal pollinated angiosperms as 308 006, which is 87.5% of the estimated species‐level diversity of flowering plants. Given current concerns about the decline in pollinators and the possible resulting impacts on both natural communities and agricultural crops, such estimates are vital to both ecologists and policy makers. Further research is required to assess in detail the absolute dependency of these plants on their pollinators, and how this varies with latitude and community type, but there is no doubt that plant–pollinator interactions play a significant role in maintaining the functional integrity of most terrestrial ecosystems.     

Pollination biology in the Snowy Mountains of Australia: Comparisons with montane Colorado,USA

Various aspects of the pollination biology of the alpine flora of Kosciusko National Park, NSW, were examined from late December 1983 until the end of March 1984, including flowering phenology, corolla tube lengths, flower colour, ultraviolet reflectance patterns, visitation rates to the flowers and proboscis lengths of the flower-visiting insects. An average of 5.3 species flowered in each of 13, 2 m×2 m montane plots and 5.6 species in the 13 alpine plots. The maximum number in flower simultaneously averaged 4.1 species in the montane and 3.3 in the alpine plots; flowering peaked in mid-January, Corolla tube lengths of the flora averaged 1.73 mm. The most common floral colour was white or predominantly white (40 species), followed by yellow (14 species). Only six of the 38 species (16%) examined had some type of reflectance pattern; the remaining species all absobed ultraviolet. Flies appeared to be the major pollinators. The insects collected in the study area comprised 60 species of Diptera, 33 species of Hymenoptera, and several species each of Lepidoptera and Coleoptera. On average, 14.4% of flowers watched during 379 observation periods (10 min each) were visited. On average, each plant species was visited by 6.4 species of flies, 2.4 species of bees, wasps or sawflies, one species of butterfly or moth and 0.3 species of beetles. Visitation rates increased over the growing season, and were significantly affected by ambient temperature (positively), light levels (positively) and wind speed (negatively). The maximum proboscis length for the 25 most common species of bees was 2.76 mm, but 18 of 51 species of flies had proboscis lengths longer than this. The mean proboscis length for all 25 species of bees was 1.68 mm, and for 51 species of flies was 2.31 mm. Proboscis lengths for flies were positively correlated with the average corolla length for the plant species they visited. For bees, however, the range in proboscis lengths was relatively small and did not show this pattern. There appear to be significant differences between the plant-pollinator community of alpine Australia and other alpine areas where bumblebees are common pollinators. These differences include shorter proboscis and corolla tube lengths, and perhaps an increased diversity and significance of flies as pollinators.     

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。