Floral divergence, pollinator partitioning and the spatiotemporal pattern of plant–pollinator interactions in three sympatric Adenophora species

Floral divergence among congeners may relate to differential utilization of pollinators and contribute to reducing overlap in pollination niches. To investigate whether and how floral differences are associated with differential utilization of pollinators in three sympatric Adenophora species, we analyzed floral traits and evaluated the contribution of different visitors to pollination. We compared visitation rates of different pollinator categories in different years and sites. A suite of floral traits differed among the three Adenophora species, suggesting adaptation to diurnal versus nocturnal pollination and an intermediate condition. However, many visitor species were shared among the three plant species, suggesting that floral traits did not rigorously filter visitors. Effective pollinators were large bees and moths. The importance of large bees as pollinators decreased whereas that of moths increased along the gradient from typically bee-pollinated to moth-pollinated flowers. The intermediate species (A. khasiana) differed substantially from the other two species in pollinator species but not in pollinator categories. The principal pollinator category of each species was constant across years and sites except in the intermediate species where it differed between two sites. Overall, the three sympatric species of Adenophora partition pollinators by floral divergence and the principal pollinators coincide with the predictions based on floral syndromes.     

Mecardonia tenella (Plantaginaceae) Attracts Oil-, Perfume-, and Pollen-Gathering Bees in Southern Brazil

Floral characteristics often indicate the pollinators' functional group visiting the plant and the pollination syndromes associated with them. This idea has been challenged in the past decades due to increasing evidence that most plants, including those exhibiting floral syndromes, are visited by large arrays of species that differ in their effectiveness as pollinators. Our study focuses on Mecardonia tenella (Plantaginaceae) from the Araucaria forest of southern Brazil, which exhibits characteristics of the oil flower pollination syndrome. However, it is visited by three types of functional groups of bees: male orchid bees, oil-collecting bees, and pollen-seeking bees. The relative contribution of each functional group to the plant's reproductive success was estimated based on their pollen load, visitation frequency, and morphology. We assessed resources, phenology, and breeding system of M. tenella . Our results indicate that flowers lack nectar, but volatiles, lipids, and pollen are resources that can be gathered by visitors. This combination of floral traits and visitors' assemblage makes M. tenella a challenge to the concept of pollination syndromes. Our findings indicate that the current interactions may not reflect the circumstances under which some floral traits of this plant were selected.     

Pollination by hummingbirds and bees in eight syntopic species and a putative hybrid of Ericaceae in Southeastern Brazil

We report on flowering phenology, floral morphology, pollinators, and nectar for eight species and a putative natural hybrid belonging to Agarista, Gaultheria and Gaylussacia that occur syntopically in a montane area. The campanulate to tubular flowers of eight out of nine Ericaceae taxa are primarily pollinated by either hummingbirds or bees. Flowering overlaps in all species but slight differences of floral shape, colour, and nectar characterize pollination by each pollinator group. Differences in floral traits are not large enough to exclude secondary pollinators. Thus, either the main pollinators of a species belonging to its syndrome, or secondary pollinators of a species belonging to different syndromes, may allow for inter-specific crosses.     

Reproductive biology of Echinopsis terscheckii (Cactaceae): the role of nocturnal and diurnal pollinators

The aim of this study was to analyse the reproductive biology of Echinopsis terscheckii, a species endemic to northwest Argentina that has nocturnal flowers. We expected that this species had a generalised pollination system, with moths and diurnal visitors as the primary pollinators. To test this, we studied the floral biology, breeding system and floral visitors of this species and the effectiveness of nocturnal and diurnal visitors. Floral biology was defined based on floral morphology, floral cycle and nectar production of the flowers. The breeding system and relative contributions of diurnal and nocturnal visitors to fruit and seed set were analysed through field experiments. E.?terscheckii flowers opened at sunset and closed the following day. The peak of nectar production occurred at midnight. Flowers were determined to be self-incompatible. Moths, bees and birds were identified as floral visitors. Moths were the most frequent visitors at night, whereas bees were the most frequent visitors during the day. Fruit production by diurnal pollinators was less than that by nocturnal pollinators; among all floral visitors, moths were the most effective pollinators. We have demonstrated for the first time that moths are the primary pollinators of columnar cacti of the genus Echinopsis. Our results suggest that moths might be important pollinators of columnar cactus species with nocturnal flowers in the extra-tropical deserts of South America.     

Reproductive biology of two Himalayan alpine gingers (Roscoea spp., Zingiberaceae) in China: pollination syndrome and compensatory floral mechanisms

According to the concept of pollination syndromes, floral traits reflect specialisation to a particular pollinator or set of pollinators. However, the reproductive biology of endemic, and often specialised, plants may require increased attention as climate change accelerates worldwide. Species of Roscoea endemic to the Himalayan region have striking orchid-like flowers with long corolla tubes, suggesting pollination by long-tongued insects. Until now, the reproductive biology of species of Roscoea has been poorly documented. We investigated the floral biology, breeding system and pollination ecology of R. cautleoides and R. humeana, from Hengduan Mountains, a global biodiversity hotspot in southwest China. We also tested whether floral longevity increases pollination success. Pollination experiments showed that the two species were self-compatible and depended on insects for fruit production. Over several flowering seasons we did not observe any potential pollinators with long tongues that matched the corolla tube visiting flowers in centres of distribution. The principal pollinators observed were pollen-collecting generalist bees, with low visitation frequencies. In general, members of the ginger family are characterised by short-lived (usually 1 day) flowers, but flowers of R. cautleoides and R. humeana last 8 and 6 days, respectively. Removing stigmas decreased fruit set in both study populations. Our results suggest that the original pollinators may have been long-tongued insects that are now absent from the Chinese Himalayas because habitats have responded to climate change. However, long-lived and self-compatible flowers, coupled with the presence of generalist pollinators, are traits that have allowed these gingers to reproduce and continue to persist in the alpine habitats.     

Three pollination guilds and variation in floral characteristics of Bornean gingers (Zingiberaceae and Costaceae)

The pollinators of 29 ginger species representing 11 genera in relation to certain floral morphological characteristics in a mixed-dipterocarp forest in Borneo were investigated. Among the 29 species studied, eight were pollinated by spiderhunters (Nectariniidae), 11 by medium-sized Amegilla bees (Anthophoridae), and ten by small halictid bees. These pollination guilds found in gingers in Sarawak are comparable to the pollination guilds of neotropical Zingiberales, i.e., hummingbird-, and euglossine-bee-pollinated guilds. Canonical discriminant analysis revealed that there were significant correlations between floral morphology and pollination guilds and suggests the importance of plant–pollinator interactions in the evolution of floral morphology. Most species in the three guilds were separated on the plot by the first and second canonical variables. Spiderhunter-pollinated flowers had longer floral tubes, while Amegilla-pollinated flowers had wider lips than the others, which function as a platform for the pollinators. Pistils and stamens of halictid-pollinated flowers were smaller than the others. The fact that gingers with diverse morphologies in a forest with high species diversity were grouped into only three pollination guilds and that the pollinators themselves showed low species diversity suggests that many species of rare understory plants have evolved without segregating pollinators in each pollination guild.     

The pollination of the gynomonoecious Bdallophytum oxylepis (Cytinaceae,Malvales)

Bdallophytum oxylepis is a rare and endemic species belonging to the Cytinaceae family, a root holoparasitic plant in which most resources are allocated to attracting pollinators. This species is gynomonoecious with intraindividual variation in flower size and sex. Moreover, the flowers exhibit sapromyophilous traits, as do other species of Bdallophytum. Firstly, this study aimed to determine whether all floral morphs can form seeds and be pollen donors (in the case of bisexual flowers). Secondly, as this species has floral traits hypothesized to adapt to particular types of pollen vectors (carrion flies), we also studied the pollination of B. oxylepis to confirm whether the syndromes correspond to what occurs in nature. Through pollination treatments, we determined that all floral morphs are functional. By monitoring the inflorescences, we found that pollination is specialized in the studied population. Stingless bees performed pollination, as they have a high visitation rate, frequency, and constancy, and they are unique visitors that deposit pollen on the stigmas. Thus, they appear to be effective pollinators rather than carrion flies, as predicted by the syndrome. As shown here, animal–plant interaction studies can help establish a basis for conserving rare species such as holoparasites. Moreover, knowledge about the reproductive aspects of B. oxylepis reveals essential clues about its life cycle and role in maintaining native pollinators with economic and cultural value, such as stingless bees.     

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.     

Chrysophyllum marginatum (Sapotaceae): Generalist pollination and cryptic gynomonoecious

Chrysophyllum (Chrysophylloideae, Chrysophylleae) is the second largest genus in the Sapotaceae. Studies of pollination ecology in this genus are non-existent, although there are records of entomophily for this family. Considering the lack of detailed studies on pollination ecology and sexual systems in Chrysophyllum species, we investigate the floral morphology and biology and floral visitors of Chrysophyllum marginatum to verify which sexual system is present in the studied population and whether flowers of this species are visited and pollinated by different insect groups. The population of C. marginatum has weak and cryptic gynomonoecy because the plants produce a low percentage of functionally pistillate flowers (4.2%) and these flowers appear to be perfect flowers (hermaphrode). Flowers of C. marginatum are phenotypically, ecologically and functionally generalist because: (a) they are actinomorphic, open and not restrictive in terms of access to floral resources; (b) they are visited by 26 species of insects that are potential pollinators; and (c) among these species several groups can be effective pollinators, mainly bees and flies, according to the most effective pollinator principle. We consider bees and flies to be the main pollinator group of C. marginatum, due to their high visitation rate, richness and intrafloral visiting behavior, and because they especially forage among plant individuals and are able to promote xenogamy. Nectaries were found in the ovary base and osmophores in the petal margins, as floral attractants. For Chrysophyllum, this is the first record of gynomonoecy and for the family this is considered the second record. Chrysophyllum marginatum has generalist and entomophilous pollination, as recorded in other Sapotaceae Neotropical species.     

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。     

The Potential Influence of Bumble Bee Visitation on Foraging Behaviors and Assemblages of Honey Bees on Squash Flowers in Highland Agricultural Ecosystems

Bee species interactions can benefit plant pollination through synergistic effects and complementary effects, or can be of detriment to plant pollination through competition effects by reducing visitation by effective pollinators. Since specific bee interactions influence the foraging performance of bees on flowers, they also act as drivers to regulate the assemblage of flower visitors. We selected squash (Cucurbita pepo L.) and its pollinators as a model system to study the foraging response of honey bees to the occurrence of bumble bees at two types of sites surrounded by a high amount of natural habitats (≥ 58% of land cover) and a low amount of natural habitats (≤ 12% of land cover) in a highland agricultural ecosystem in China. At the individual level, we measured the elapsed time from the departure of prior pollinator(s) to the arrival of another pollinator, the selection of honey bees for flowers occupied by bumble bees, and the length of time used by honey bees to explore floral resources at the two types of sites. At the community level, we explored the effect of bumble bee visitation on the distribution patterns of honey bees on squash flowers. Conclusively, bumble bee visitation caused an increase in elapsed time before flowers were visited again by a honey bee, a behavioral avoidance by a newly-arriving honey bee to select flowers occupied by bumble bees, and a shortened length of time the honey bee takes to examine and collect floral resources. The number of overall bumble bees on squash flowers was the most important factor explaining the difference in the distribution patterns of honey bees at the community level. Furthermore, decline in the number of overall bumble bees on the squash flowers resulted in an increase in the number of overall honey bees. Therefore, our study suggests that bee interactions provide an opportunity to enhance the resilience of ecosystem pollination services against the decline in pollinator diversity.     

Diurnal and nocturnal pollination of Silene alba (Caryophyllaceae)

Flowers that are open for >12 h may be visited by both diurnal and nocturnal pollinators. I compared the effectiveness (measured as seed production and pollen movement distance) of diurnal and nocturnal pollinators of Silene alba, a species whose flowers open in evening but close by midmorning the following day. By bagging flowers either during evening hours or during daylight hours or both day and night, I compared seed production caused by diurnal and nocturnal pollinators. Flowers exposed only to nocturnal visitors (mostly sphingid and noctuid moths) produced significantly more seeds than flowers exposed only to diurnal visitors (bees, flies, and wasps). Fluorescent dye applied to anthers moved significantly further and to more stigmas at night than during the day. In both measures of pollination effectiveness, nocturnal-visiting moths are better pollinators of S. alba than are the diurnal-visiting bees, flies, and wasps. These data support the hypothesis that floral phenology is an adaptation to expose flowers to the most effective pollinators.     

同域分布的紫堇属三种植物的繁育系统和传粉差异

为研究近缘物种之间繁育系统分化对传粉环境的适应性意义,本文针对湖北地区的3种紫堇属植物（紫堇Corydalis edulis Maxim.、尖距紫堇C.shearer S.Moore.和小花黄堇C.racemosa（Thunb.） Pers.）进行了传粉生态学研究,对比分析了它们在花部特征、分布模式、花期、交配系统、传粉系统等方面的差异。3种紫堇属植物常见伴生现象,花期有一定重叠;花色、距长、花蜜量等方面均有显著差异;尖距紫堇交配系统为自交不亲和、依靠传粉者异花授粉;而紫堇和小花黄堇交配系统为自交亲和,兼有自交和异交的混合交配系统。3个物种均由蜂类传粉,且花部性器官与传粉者的接触部位一致,但访花频率差异较大。在混合群落中,传粉者访花具有较高的忠实性,花部特征差异可能是传粉者选择性访花的原因。对于紫堇属3个物种,花部特征和交配系统的分化有助于其避免传粉过程的相互干扰,交配系统与传粉环境具有一定相关性,混合交配系统可能有利于提高植物对不同生境和气候的适应性。     

Visual cues and foraging choices: bee visits to floral colour phases in Alkanna orientalis (Boraginaceae)

When a pollination vector is required, any mechanism that contributes to floral visitation will potentially benefit the reproductive fitness of a plant. We studied the effect of floral colour change in the desert perennial Alkanna orientalis on the foraging behaviour of the solitary bee Anthophora pauperata . Flowers changed colour over time from bright yellow (with moderate nectar reward) to pale yellow/white (with significantly lower nectar reward). Bee visitation was non-random with respect to colour phase availability within the flower population and was biased towards the more rewarding flowers. At plants where the availability of colour phases had been manipulated experimentally to produce 'bright' or 'pale' plants, bees visited significantly more flowers (and for longer periods) on the bright plants. The change of flower colour was not simply age-related; we observed variation in the temporal course of colour change and our data suggest that visitation, leading to deposition of cross-pollen, can accelerate the process. In subpopulations with limited pollinators, Alkanna can influence bees by using their colour-related foraging preferences to alter visitation patterns.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 427–435.     

Are pollination syndromes useful predictors of floral visitors in Tasmania?

Abstract Diurnal visitors to the flowers of many native plant species were identified in a wide range of Tasmanian sclerophyllous vegetation between September 1996 and April 1997. These foraging profiles were analysed to determine whether they were characteristic of various floral morphologies in predictable ways. It was found that although visitor profiles were sometimes consistent with classic pollination syndromes, these syndromes were unreliable predictors of floral visitors. Very few flowers were exclusively bird‐pollinated, and none were strictly fly‐, beetle‐, wasp‐, or butterfly‐pollinated. The majority of flowering plants were unspecialized in their morphology, and consequently hosted a diverse array of visitors. In addition, visitor profiles to congeners with similar floral morphologies, and even to conspecifics, differed between habitats. Altitude was a major factor in determining visitors, with flies being the most abundant visitors above 700 m. However, congeners in several genera of Epacridaceae, as well as the genus Correa, which differed in floral morphology also differed in visitor profiles. Tubular flowers were associated with birds, while flowers with more accessible nectar were visited by insects. The only taxa exhibiting a bee‐pollination syndrome that were largely visited by bees were the Fabaceae and Goodenia ovata Sm. Several species with purple or pink flowers were also predominantly visited by bees, but did not strictly conform to the melittophilous syndrome. In contrast, other flowers exhibiting an ostensibly mellitophilous syndrome hosted very few bees. Of these, species that occurred at high altitude were mainly visited by flies, while others received very few potential pollen vectors.     

IS FLORAL SPECIALIZATION AN EVOLUTIONARY DEAD‐END? POLLINATION SYSTEM TRANSITIONS IN RUELLIA (ACANTHACEAE)

Pollination systems frequently reflect adaptations to particular groups of pollinators. Such systems are indicative of evolutionary specialization and have been important in angiosperm diversification. We studied the evolution of pollination systems in the large genus Ruellia. Phylogenetic analyses, morphological ordinations, ancestral state reconstructions, and a character mapping simulation were conducted to reveal key patterns in the direction and lability of floral characters associated with pollination. We found significant floral morphological differences among species that were generally associated with different groups of floral visitors. Floral evolution has been highly labile and also directional. Some specialized systems such as hawkmoth or bat pollination are likely evolutionary dead-ends. In contrast, specialized pollination by hummingbirds is clearly not a dead-end. We found evidence for multiple reverse transitions from presumed ancestral hummingbird pollination to more derived bee or insect pollination. These repeated origins of insect pollination from hummingbird-pollinated ancestors have not evolved without historical baggage. Flowers of insect-pollinated species derived from hummingbird-pollinated ancestors are morphologically more similar to hummingbird flowers than they are to other more distantly related insect-pollinated flowers. Finally, some pollinator switches were concomitant with changes in floral morphology that are associated with those pollinators. These observations are consistent with the hypothesis that some transitions have been adaptive in the evolution of Ruellia.     

Orchard pollination in Capitol Reef National Park,Utah, USA. Honey bees or native bees?

Capitol Reef National Park in central Utah, USA surrounds 22 managed fruit orchards started over a century ago by Mormon pioneers. Honey bees are imported for pollination, although the area in which the Park is embedded has over 700 species of native bees, many of which are potential orchard pollinators. We studied the visitation of native bees to apple, pear, apricot, and sweet cherry over 2 years. Thirty species of bees visited the flowers but, except for pear flowers, most were uncommon compared to honey bees. Evidence that honey bees prevented native bees from foraging on orchard crop flowers was equivocal: generally, honey bee and native bee visitation rates to the flowers were not negatively correlated, nor were native bee visitation rates positively correlated with distance of orchards from honey bee hives. Conversely, competition was tentatively suggested by much larger numbers of honey bees than natives on the flowers of apples, apricots and cherry; and by the large increase of native bees on pears, where honey bee numbers were low. At least one-third of the native bee species visiting the flowers are potential pollinators, including cavity-nesting species such as Osmia lignaria propinqua, currently managed for small orchard pollination in the US, plus several fossorial species, including one rosaceous flower specialist (Andrena milwaukiensis). We suggest that gradual withdrawal of honey bees from the Park would help conserve native bee populations without decreasing orchard crop productivity, and would serve as a demonstration of the commercial value of native pollinators.     

Contribution of diurnal and nocturnal insects to the pollination of Jatropha curcas (Euphorbiaceae) in southwestern China

Jatropha curcas L. (Euphorbiaceae) is being increasingly planted worldwide, but questions remain regarding its pollination biology. This study examined the contribution of diurnal and nocturnal insects to the pollination of monoecious J. curcas, through its floral biology, pollination ecology, and foraging behavior of potential pollinators. Nectar production of both male and female flowers peaked in the morning, declined in the afternoon, and rapidly bottomed during the night in all of their anthesis days. The diurnal visitors to the flowers of J. curcas are bees and flies, and the nocturnal visitors are moths. Flowers received significantly more visits by diurnal insects than by nocturnal insects. Through bagging flowers during night or day or both or exclusion, we compared fruit and seed production caused by diurnal and nocturnal pollinators. Both nocturnal and diurnal visitors were successful pollinators. However, flowers exposed only to nocturnal visitors produced less fruits than those exposed only to diurnal visitors. Thus, diurnal pollinators contribute more to seed production by J. curcas at the study site.     

The function of ant repellence by flowers: testing the “nectar protection” and “pollinator protection” hypotheses

According to the “nectar protection” and “pollinator protection” hypotheses, ant repellents in flowers have evolved to prevent ants from exploiting floral nectar and chasing away pollinators, respectively. We used weaver ants, Oecophylla smaragdina, to determine the strength of ant repellence in 32 bee-pollinated plant species and used the comparative method to test whether nectar production, size of pollinating bees and plant growth form were related to floral repellence. Flowers were more likely to repel ants if they offered nectar as a reward and were pollinated by small bees than if they were nectarless and pollinated by large bees. Furthermore, tree flowers were more likely than shrub or vine flowers to repel ants. Our results validate the pollinator protection hypothesis and the nectar protection hypothesis. Depending on the ecological context, therefore, ant repellents can function as direct or indirect exploitation barriers: they can prevent ants from removing nectar without effecting pollination (direct barriers) and, when flowers are pollinated by large bees, the absence of ant repellents—or even the presence of ant attractants—can result in ants chasing small ineffective pollinators away (indirect barriers).     

The pollination biology of Burmeistera (Campanulaceae): specialization and syndromes

The floral traits of plants with specialized pollination systems both facilitate the primary pollinator and restrict other potential pollinators. To explore interactions between pollinators and floral traits of the genus Burmeistera, I filmed floral visitors and measured pollen deposition for 10 species in six cloud forest sites throughout northern Ecuador. Nine species were primarily bat-pollinated (84-100% of pollen transfer); another (B. rubrosepala) was exclusively hummingbird-pollinated. According to a principal components analysis of 11 floral measurements, flowers of B. rubrosepala were morphologically distinct. Floral traits of all species closely matched traditional ornithophilous and chiropterophilous pollination syndromes; flowers of B. rubrosepala were bright red, lacked odor, opened in the afternoon, and had narrow corolla apertures and flexible pedicels, which positioned them below the foliage. Flowers of the bat-pollinated species were dull-colored, emitted odor, opened in the evening, and had wide apertures and rigid pedicels, which positioned them beyond the foliage. Aperture width appeared most critical to restricting pollination; hummingbirds visited wide flowers without contacting the reproductive parts, and bats did not visit the narrow flowers of B. rubrosepala. Aperture width may impose an adaptive trade-off that favors the high degree of specialization in the genus. Other floral measurements were highly variable amongst bat-pollinated species, including stigma exsertion, calyx lobe morphology, and pedicel length. Because multiple species of Burmeistera often coexist, such morphological diversity may reduce pollen competition by encouraging pollinator fidelity and/or spatially partitioning pollinator's bodies.