Effectiveness of bats as pollinators of Stenocereus stellatus (Cactaceae) in wild, managed in situ, and cultivated populations in La Mixteca Baja, central Mexico

Stenocereus stellatus is an endemic, self-incompatible, columnar cactus found in central Mexico where many of its wild populations have been fragmented. As an economically important species of fruit-producing cactus, S. stellatus occurs in wild, managed in situ, and cultivated populations. The objectives of this study were to determine the effective pollinators of S. stellatus, to compare pollinator visits and reproductive parameters among the three types of populations, and to determine if nectar feeding-bats are moving among populations. Effective pollinators were the nectarivorous bats Choeronycteris mexicana, Leptonycteris curasoae, and L. nivalis. Fewer total visits per flower per night and fewer visits by Choeronycteris were observed in cultivated populations, while the opposite pattern was observed for Leptonycteris. One aggressive interaction was filmed in which Choeronycteris was physically displaced by Leptonycteris, and Choeronycteris visits were significantly affected by Leptonycteris visits. Cultivated populations received more pollen grains and had more fruit set. Variation in pollinator visits between different populations and the consequent effects on reproductive success were likely a result of competition between bat species, and differences in foraging and in sensitivity of bat species to human populations. Three marked L. curasoae traveled 15 km from their roosting site to their foraging area, and one visited cultivated and managed populations, suggesting that this species may be particularly important in moving pollen among populations.     

Reproductive ecology of five sympatric Agave Littaea (Agavaceae) species in central Mexico

We studied a community of Agave species that coexist in the Metztitlán Canyon in Central Mexico. During 2001, 2002, and 2003, we analyzed floral traits and rosette allometry in five species belonging to the subgenus Littaea: A. celsii albicans, A. xylonacantha, A. difformis, A. striata, and Agave sp.; and observed floral visitors for each species. We report the first evidence of bat visitation in the subgenus Littaea and find that bats (Leptonycteris curasoae, Choeronycteris mexicana, and Glossophaga sp.) are the primary pollinators in four species. Honeybees, hummingbirds, bumblebees and hawkmoths were also common visitors. We propose that the presence of diurnal pollinators may increase the reproductive success of the plant when offering pollinator services additional to the coadapted pollinator. We also found evidence of selection pressures toward semelparity because pollinators are selecting for taller inflorescences in three of the five species. There is phenological complementarity in this community because the flowering periods of the five species span the entire year, although there are some periods when pairs of species overlap. Additionally, we found evidence for character displacement in rosette sizes and separation of spatial and temporal resource use in pollinator composition among species.     

Pollination ecology of Stenocereus queretaroensis (Cactaceae), a chiropterophilous columnar cactus, in a tropical dry forest of Mexico

Flowers of columnar cacti are animal-pollinated, often displaying a chiropterophylic syndrome. This study examined if the columnar cactus Stenocereus queretaroensis, a tropical species endemic to western Mexico, is bat-pollinated, by studying its pollination biology and the foraging behavior of potential pollinators. Flowers were produced in winter through spring, peaking in April. Anthesis was nocturnal, and stigma and anther turgidity began around 2200 hours. Production of nectar secretion and highest sugar concentration and energy supply were nocturnal, peaking between 2200 and 2400 hours. Manual auto-pollination and exclusion experiments showed that self-pollination yielded no fruits, while nocturnal pollinators resulted in high fruit set and seed set compared to diurnal pollination treatments. The nectar-feeding bat Leptonycteris curasoae (Phyllostomidae) was the main nocturnal pollinator with the highest effective pollination. Peak bat visitation coincided with peaks in nectar production. The high abundance of L. curasoae throughout the 4-yr study, suggests that it is a seasonally reliable pollinator for this columnar cactus. While pollination syndromes have been increasingly called into question in recent years, this study suggests that at least for this system, there is a fairly close fit between pollinator and pollination syndrome.     

The pollination biology of two paniculate agaves (Agavaceae) from northwestern Mexico: contrasting roles of bats as pollinators

Paniculate agaves from tropical deserts depend on nectar-feeding bats for their reproduction, while species from extratropical areas near the northern limit of Leptonycteris curasoae are pollinated by diurnal and nocturnal insects and birds. Agave angustifolia is a paniculate agave with a broad distribution in Mexico whose range coincides with the distribution of L. curasoae, while A. subsimplex has a narrow distribution in Sonora within the range of nectar-feeding bats. We studied the pollination biology of A. angustifolia and A. subsimplex in northwestern Mexico to evaluate the relative importance of bat pollination in a region where L. curasoae is seasonal. Flower visitors included a wide variety of animals, with bats having greater visitation rates in A. angustifolia. A pollinator-exclusion experiment revealed that bats were responsible for most of the control fruit set in A. angustifolia, whereas for A. subsimplex, diurnal and nocturnal visitors were equally effective. Overall, our data indicate that in central Sonora, A. angustifolia depends on nectar-feeding bats for its sexual reproductive success, while A. subsimplex relies on both diurnal and nocturnal pollinators. Given the contrasting distribution ranges of paniculate agaves, our results seem to support the trend from specialization to generalization along the continuum of tropical to extratropical deserts.     

Pollination biology of two columnar cacti (Neobuxbaumia mezcalaensis and Neobuxbaumia macrocephala) in the Tehuacan Valley,central Mexico

We document the pollination biology and mating systems of Neobuxbaumia mezcalaensis and Neobuxbaumia macrocephala, two Mexican giant columnar cacti. These two species form mixed forests in the western Tehuacan Valley, Mexico. The flowers of both N. mezcalaensis and N. macrocephala exhibit nocturnal anthesis, are self-incompatible, and are pollinated primarily by three species of nectar-feeding bats (Choeronycteris mexicana, Leptonycteris curasoae, and Leptonycteris nivalis). Neobuxbaumia mezcalaensis is androdioecious, a breeding system that appears to be uncommon among Cactaceae. Neobuxbaumia macrocephala is hermaphroditic. We hypothesize that columnar cacti show a geographical dichotomy in floral biology specialization that probably can be related to predictability in pollinator abundance.     

Reproductive biology and the process of domestication of the columnar cactus Stenocereus Stellatus in Central Mexico

Pollination biology, breeding system, and floral phenology of the columnar cactus Stenocereus stellatus were studied in wild, wild managed in situ and cultivated populations of central Mexico, in order to examine whether these aspects have been modified under domestication and whether they determine reproductive barriers between wild and manipulated individuals. Individuals of both wild and manipulated populations are self-incompatible, indicating that artificial selection has not modified the breeding system. Their pollination biology is also similar. Anthesis is mainly nocturnal, with a peak of nectar production between 0200 and 0400 when the stigma presents maximum turgidity. Nocturnal visitors are the effective pollinators. Nearly 75% of flowers exposed for nocturnal pollination set fruit, while none of the flowers exposed for diurnal pollination produced fruits. The bats Leptonycteris curasoae, L. nivalis, and Choeronycteris mexicana (Glossophaginae) are the most likely pollinators, and their time of foraging is synchronized with the time of nectar production and stigma receptivity in S. stellatus. Bats potentially move pollen over a considerable distance, so there is apparently no spatial isolation to prevent pollen exchange between wild and cultivated populations. Phenological studies showed that there are also no apparent temporal barriers. However, manual cross pollination failed between some domesticated and wild phenotypes, suggesting that gene flow between wild and cultivated populations might be limited by pollen incompatibility.     

Reproductive biology of Pachira aquatica Aubl. (Malvaceae: Bombacoideae): a tropical tree pollinated by bats,sphingid moths and honey bees

We investigated the reproductive biology, including the floral biology, pollination biology, breeding system and reproductive success, of Pachira aquatica, a native and dominant tropical tree of fresh water wetlands, throughout the coastal plain of the Gulf of Mexico. The flowers present nocturnal anthesis, copious nectar production and sugar concentration (range 18–23%) suitable for nocturnal visitors such as bats and sphingid moths. The main nocturnal visitors were bats and sphingid moths while bees were the main diurnal visitors. There were no differences in legitimate visitation rates among bats, moths and honey bees. Bats and honey bees fed mainly on pollen while moths fed on nectar, suggesting resource partitioning. Eight species of bats carried pollen but Leptonycteris yerbabuenae is probably the most effective pollinator due to its higher pollen loads. The sphingid moths Manduca rustica, Cocytius duponchel and Eumorpha satellitia were recorded visiting flowers. Hand pollination experiments indicated a predominant outcrossing breeding system. Open pollination experiments resulted in a null fruit set, indicating pollen limitation; however, mean reproductive success, according to a seasonal census, was 17 ± 3%; these contrasting results could be explained by the seasonal availability of pollinators. We conclude that P. aquatica is an outcrossing species with a pollination system originally specialized for bats and sphingid moths, which could be driven to a multimodal pollination system due to the introduction of honey bees to tropical America.     

Effects of habitat disruption on the activity of nectarivorous bats (Chiroptera: Phyllostomidae) in a dry tropical forest: implications for the reproductive success of the neotropical tree Ceiba grandiflora

In the tropical dry forest of the central Pacific coast of Mexico the pollination and reproductive success of the bombacaceous tree Ceiba grandiflora was negatively affected by habitat disruption. Two of the three bat species that function as effective pollinators for this species ( Glossophaga soricina and Musonycteris harrisoni) visited flowers found in trees in disturbed habitats significantly less than trees found in undisturbed habitats. A similar pattern was observed for the effective bat pollinator, Leptonycteris curasoae; however the difference was not significant. The three nectarivorous bats that functioned as effective pollinators of C. grandiflora also visited flowers to exclusively feed on pollen by biting or pulling off an anther (see Fig. S1 of Electronic Supplementary Material). The number of pollen grains deposited on stigmas from flowers in undisturbed areas was significantly greater than from flowers in disturbed habitats. The greater visitation rate and the greater number of pollen grains deposited on flowers from trees in undisturbed forest resulted in a significantly greater fruit set for trees in these areas. Our study demonstrates the negative effect that habitat disruption has on bat pollinators in tropical dry forest ecosystems and documents the negative consequences for the plants they pollinate.     

Geographic differentiation in the pollination system of the columnar cactus Pachycereus pecten -aboriginum

The pollination biology of the cactus Pachycereus pecten-aboriginum was studied in a tropical location in western Mexico (ca. 18° N latitude) to compare with data from a northern population (ca. 28° N latitude). Throughout this range, the nectar-feeding bat Leptonycteris curasoae is resident within the tropics but migratory in its northern range. The hypothesis was tested that if a predictable bat presence has been an important force in the evolution of pollination systems in columnar cacti, P. pecten-aboriginum will have a specialized pollination system within the tropics and a generalized pollination system in northern populations. In both areas, pollination experiments showed that P. pecten-aboriginum has a self-incompatible, hermaphroditic breeding system. In the tropical area, flowers open at night and close early in the morning. Nectar is secreted only during the night, and flowers are exclusively pollinated by three species of nectar-feeding bats, indicating a specialized pollination system. In contrast, anthesis and nectar secretion in northern populations occur during the night and day, allowing visitation and effective pollination by both nocturnal and diurnal pollinators. This study provides evidence of divergence mediated by pollinator predictability (resident vs. migrant), through shifts from short to long anthesis and nectar production periods from southern to northern populations.     

Pollination ecology of Agave macroacantha (Agavaceae) in a Mexican tropical desert. I. Floral biology and pollination mechanisms

In a study of sexual reproduction in long-lived semelparous plants, we observed Agave macroacantha in the tropical desert of Tehuacán-Cuicatlán, Mexico, describing duration of flowering, flower phenology, and nectar production patterns. We also performed two manipulative experiments evaluating (a) the seed production efficiency of different crossing systems (selfing, cross-pollination, apomixis, and control), and (b) the effect of different pollinators (diurnal exposure to pollinators, nocturnal exposure, exclusion, and control) on the seeds produced. Flowering occurred from early May to late July and had a mean duration of 29 days in the individual rosettes. The flowers were protandrous; anthesis occurred in the afternoon of the third day after floral opening, and the pistils matured in the afternoon of the fifth day. The stigmas remained receptive from dusk to the following morning. Pollination was mostly allogamous. Nectar was produced principally during the night, from the first stages of floral aperture until the stigmas wilted and flowering ceased. The flowers were visited during the day by hymenoptera, butterflies, and hummingbirds and during the night by bats and moths. Only the nocturnal visitors, however, were successful pollinators. Agave macroacantha is extremely dependent on nocturnal pollinators for its reproductive success.     

Comparative pollination biology of Venezuelan columnar cacti and the role of nectar-feeding bats in their sexual reproduction

The floral biology, reproductive system, and visitation behavior of pollinators of four species of columnar cacti, Stenocereus griseus, Pilosocereus moritzianus, Subpilocereus repandus, and Subpilocereus horrispinus, were studied in two arid zones in the north of Venezuela. Our results support the hypothesis that Venezuelan species of columnar cacti have evolved toward specialization on bat pollination. Additional information on the floral biology of a fifth species, Pilosocereus lanuginosus, was also included. All species showed the typical traits that characterize the pollination syndrome of chiropterophily. All species but Pilosocereus moritzianus were obligate outcrossers. Nectar and pollen were restricted to nocturnal floral visitors. Two species of nectar-feeding bats, Leptonycteris curasoae Miller and Glossophaga longirostris Miller, were responsible for practically all the fruit set in these cacti. Frequency of bat visitation per flower per night was highly variable within and between species of cactus, with average frequencies varying between 27 and 78 visits/flower/night. In general terms, the pattern of floral visitation through the night was significantly correlated with the pattern of nectar production and nectar sugar concentration for all species of cactus. Under natural pollination, fruit:flower ratios varied from 0.46 in Subpilocereus repandus to 0.76 in Stenocereus griseus. The efficiency of bat pollination in terms of seed:ovule ratio was high in all species, varying between 0.70 and 0.94.     

Geographic variation in reproductive success of Stenocereus thurberi (Cactaceae): Effects of pollination timing and pollinator guild

? Premise of the study: It has been proposed that species of columnar cacti from dry tropical areas depend on bats for their reproduction, whereas species from dry subtropical areas are also pollinated by other species. To test this hypothesis, we examined the effects of pollinator guild and of variation in time and space on the reproductive success of a widespread species. ? Methods: Changes in fruit set, seed set, and pollinator activity through time were recorded in three widely separated populations of Stenocereus thurberi. Breeding system and sources of pollination limitation were determined by controlled pollinator exclusions in each population. ? Key results: Significant differences were found in the timing of activity and in the effectiveness of pollinators among sites. In the northern and central populations, reproductive success depends on bats, whereas in the southern population a combination of pollinators was more effective. No difference between open and hand cross-pollination treatments was found in the northern and central populations, which suggests no pollen limitation. However, significant differences were detected in the southern population, which indicates temporal differences in pollinator abundance or arrival time. ? Conclusions: Local variation in pollinator assemblages and reproductive success could greatly affect the evolution of pollination systems. The pattern of generalist pollination in the southernmost populations and specialized pollination in the central and northern populations contradicts the hypothesis of latitudinal variation. In the absence of nocturnal pollinators, the accumulated nectar can sustain visits by diurnal pollinators, a bet-hedging strategy that increases the chances of fruit set in some populations.     

Effect of habitat disturbance on pollination biology of the columnar cactus Stenocereus quevedonis at landscape‐level in central Mexico

Stenocereus quevedonis (‘pitire’) is a columnar cactus endemic to central Mexico, grown for its edible fruit. Phenology, pollination biology and behaviour of flower visitors of this species were compared in six conserved and disturbed sites, hypothesising that: (i) pitire pollination is self‐incompatible, requiring animal vectors; (ii) higher incidence of radiation on plants in cleared forest may lead to a higher number of flowers per pitire plant and longer blooming season, and disturbing and differential spatial availability of flower resources may determine differential attraction of pollinators to conserved and disturbed areas; (iii) if pitire pollination system is specialised, reproductive success would decrease with pollinator scarcity, or other species may substitute for main pollinators. In all sites, pitire reproduction started in January, flowering peak occurring in April, anthesis duration was 15 h and predominantly nocturnal (9 h), pollen was released at 23:00 h, nectar was produced throughout anthesis, and breeding system was self‐incompatible. Flower production per plant was similar in disturbed and conserved sites, but flower availability was higher (because of higher tree density) and longer in disturbed sites. Pollination is nocturnal, the most frequent legitimate pollinator being the bat Leptonycteris yerbabuenae; diurnal pollination is rare but possible, carried out by bee species. Fruit and seed set in control and nocturnal pollination treatments at disturbed sites were higher than in conserved sites. Frequency of L. yerbabuenae visits was similar among site types, but more visits of complementary nocturnal and diurnal pollinators were recorded in disturbed sites, which could explain differences in reproductive success.     

Pollination biology of two chiropterophilous agaves in Arizona

I studied the pollination biology of two closely related species of agave, Agave palmeri and A. chrysantha (Agavaceae), which exhibit several chiropterophilous (bat-pollinated) traits. Floral studies, floral visitor observations, and pollination studies were conducted over four summers at six different sites to examine floral traits and determine the relative importance of diurnal vs. nocturnal pollinators. Agave chrysantha appears to have developed minor shifts in several floral characters that enhance diurnal pollination. Although floral shifts towards diurnal pollination were fewer in A. palmeri, stigmas were diurnally receptive and copious floral rewards were available in the morning, indicating that some adaptations exist to allow for multiple pollinators. Differences in fruit and seed set between naturally day- and night-pollinated umbels for both species were either not significant or significantly higher in day-pollinated plants. Bats were not important pollinators of A. chrysantha, and the mutualistic relationship between A. palmeri and the lesser long-nosed bat was found to be asymmetric. "Bat-adapted" floral traits appear to be flexible enough to respond to the climatic and pollinator unpredictability experienced by agaves at the northern edge of their distribution. This variability may be a more important factor affecting evolution of floral characters than a particular pollinator.     

First record of bat-pollination in the species-rich genus Tillandsia (Bromeliaceae)

Background and Aims

Bromeliaceae is a species-rich neotropical plant family that uses a variety of pollinators, principally vertebrates. Tillandsia is the most diverse genus, and includes more than one-third of all bromeliad species. Within this genus, the majority of species rely on diurnal pollination by hummingbirds; however, the flowers of some Tillandsia species show some characteristics typical for pollination by nocturnal animals, particularly bats and moths. In this study an examination is made of the floral and reproductive biology of the epiphytic bromeliad Tillandsia macropetala in a fragment of humid montane forest in central Veracruz, Mexico.

Methods

The reproductive system of the species, duration of anthesis, production of nectar and floral scent, as well as diurnal and nocturnal floral visitors and their effectiveness in pollination were determined.

Key Results

Tillandsia macropetala is a self-compatible species that achieves a higher fruit production through outcrossing. Nectar production is restricted to the night, and only nocturnal visits result in the development of fruits. The most frequent visitor (75 % of visits) and the only pollinator of this bromeliad (in 96 % of visits) was the nectarivorous bat Anoura geoffroyi (Phyllostomidae: Glossophaginae).

Conclusions

This is the first report of chiropterophily within the genus Tillandsia. The results on the pollination biology of this bromeliad suggest an ongoing evolutionary switch from pollination by birds or moths to bats.     

A physiological perspective on nectar-feeding adaptation in phyllostomid bats

Nectar-feeding animals increase their food intake when nectar sugar concentration decreases. However, some species present physiological constraints that limit their energy intake when nectar is diluted. We hypothesized that gut capacities of bats affect the ability of these animals to acquire and store energy, modifying how they use food resources in the field. We measured the food intake and changes in body mass of the members of an assemblage of nectar-feeding bats (Choeronycteris mexicana, Leptonycteris yerbabuenae, and Glossophaga soricina) feeding on sucrose solutions of different concentrations (146, 292, 438, 584, 730, 876, and 1,022 mmol L(-1)). The three bat species presented differences in their food intake and their capacity to store energy. While C. mexicana was able to maintain a constant energy intake at all concentrations tested, G. soricina and L. yerbabuenae decreased their sugar/energy intake at the lowest sugar concentrations. Choeronycteris mexicana also increased body mass independent of sugar concentration, while G. soricina and L. yerbabuenae did not. On the basis of our results, we generated a model relating gut capacities and the use of food resources in the field. Our model's predictions and field data support the idea that digestive traits affect the way these animals use the food resources present in their environment.     

Geographic variation in the breeding system and the evolutionary stability of trioecy in Pachycereus pringlei (Cactaceae)

The Sonoran Desert columnar cactus Pachycereus pringlei has a geographically variable, non-hermaphroditic breeding system. It is trioecious (separate males, females and hermaphrodites) in the northern two-thirds of its range in Sonora, Mexico, and in the southern three-quarters of its range in Baja California, Mexico, and is gynodioecious (separate females and hermaphrodites) elsewhere. Trioecy occurs near known maternity roosts of its major pollinator, the nectar-feeding bat Leptonycteris curasoae; gynodioecy occurs>50km from known bat roosts. The observed geographic patterns cannot be explained by limited gene flow or by the geographic distributions of diurnal avian pollinators. Our field observations plus a theoretical analysis suggest that the abundance of chiropteran pollinators plays an important role in the maintenance of trioecy in this plant. Under pollinator limitation, trioecy can be a stable breeding system in this species. This revised version was published online in July 2006 with corrections to the Cover Date.     

A generalized pollination system in the tropics: bats, birds and Aphelandra acanthus

Background and Aims

A number of different types of flower-visiting animals coexist in any given habitat. What evolutionary and ecological factors influence the subset of these that a given plant relies on for its pollination? Addressing this question requires a mechanistic understanding of the importance of different potential pollinators in terms of visitation rate (pollinator ‘quantity’) and effectiveness at transferring pollen (pollinator ‘quality’) is required. While bat-pollinated plants typically are highly specialized to bats, there are some instances of bat-pollinated plants that use other pollinators as well. These generalized exceptions tend to occur in habitats where bat ‘quantity’ is poor due to low or fluctuating bat densities.

Methods

Aphelandra acanthus occurs in tropical cloud forests with relatively high densities of bat visitors, yet displays a mix of floral syndrome characteristics, suggesting adaptation to multiple types of pollinators. To understand its pollination system better, aspects of its floral phenology and the ‘quantity’ and ‘quality’ components of pollination by its floral visitors are studied here.

Key Results

Flowers were found to open and senesce throughout the day and night, although anther dehiscence was restricted to the late afternoon and night. Videotaping reveals that flowers are visited nocturnally by bats and moths, and diurnally by hummingbirds. Analysis of pollen deposition shows that bats regularly transfer large amounts of conspecific pollen, while hummingbirds occasionally transfer some pollen, and moths rarely do so.

Conclusions

Hummingbirds and bats were comparable in terms of pollination ‘quantity’, while bats were the most effective in terms of ‘quality’. Considering these components together, bats are responsible for approx. 70 % of A. acanthus pollination. However, bats also transferred remarkably large amounts of foreign pollen along with the conspecific grains (three of four grains were foreign). It is suggested that the negative effects of interspecific pollen transfer may decrease bat ‘quality’ for A. acanthus, and thus select for generalization on multiple pollinators instead of specialization on bats.Key words: Specialization, generalization, pollinator effectiveness, hummingbirds, floral syndrome, bat pollination, chiropterophily, ornithophily, cloud forest, heterospecific pollen transfer     

Relative importance of diurnal and nocturnal pollinators for reproduction in the early spring flowering shrub Stachyurus praecox (Stachyuraceae)

Generalized pollination systems may be favored in early spring flowering plants, as during this period pollinator activity is unpredictable. Many previous studies have concentrated on the importance of diurnal visitors in pollination, and consequently, information on the contribution of nocturnal visitors to pollination in early spring is limited. This study was conducted to evaluate the relative importance of diurnal and nocturnal pollinators in the early spring flowering dioecious shrub Stachyurus praecox (Stachyuraceae), in two temperate forests in central Japan. Visitors to the female and male flowers were observed during day and night, and their relative contributions to seed set were compared. The pollinator observations revealed that the diurnal and nocturnal insects visited both male and female flowers, and that the main flower visitors were diurnal small bees and flies as well as nocturnal settling moths. The diurnal and nocturnal flower visitors also acted as pollinators, as the pollen grains of S. praecox were attached to the insects collected from the female flowers. Pollination experiments demonstrated that the contributions of diurnal pollinators to the seed set were higher than those of the nocturnal pollinators. The results of this study indicate that S. praecox has a generalized pollination system, comprising both diurnal insects and nocturnal settling moths. Although the roles of diurnal insects are more important in the pollination of S. praecox, nocturnal settling moths may have a complementary role in early spring.     

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.