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.     

Does intraspecific size variation in bumblebees allow colonies to efficiently exploit different flowers?

Abstract.  1. It has long been known that foraging bumblebee workers vary greatly in size, within species, and within single nests. This phenomenon has not been adequately explained. Workers of their relatives within the Apidae exhibit much less size variation.
2. For the bumblebee Bombus terrestris size, as measured by thorax width, was found to correspond closely with tongue length, so that larger bees are equipped to feed from deeper flowers.
3. The mean size of worker bees attracted to flowers was found to differ between plant species, and larger bees with longer tongues tended to visit deeper flowers.
4. Finally, handling time depended on the match between corolla depth and tongue length: large bees were slower than small bees when handling shallow flowers, but quicker than small bees when handling deep flowers.
5. Size variation within bumblebees may be adaptive, since it enables the colony as a whole to efficiently exploit a range of different flowers. Possible explanations for the marked differences in size variation exhibited by bumblebees compared with Apis species and stingless bees (Meliponinae) are discussed.     

Proboscis length and resource utilization in two Uruguayan bumblebees: Bombus atratus Franklin and Bombus bellicosus Smith (Hymenoptera: Apidae)

Bumblebees (Bombus sp.) are eusocial insects with an annual life cycle whose use as pollinator of crops has gained great importance in modern agriculture. Several authors have found that resource use in Bombus species is usually based on the correlation between the proboscis length of the bumblebees and the corolla depth of the flowers. The aim of this study was to determine proboscis length of Bombus atratus and B. bellicosus, two Uruguayan bumblebees, and verify the resource exploitation testing two cultivated species, the red clover and the bird's foot trefoil. Bumblebee foraging activity was recorded in two culture conditions: in a red clover and bird's foot trefoil mixed meadow, and in contiguous plots of these legumes, and the proboscis length of collected foragers was determined. Both species of bumblebees exploited red clover and bird's foot trefoil although they did it in different proportions in all instances tested. The results indicated that the choice of the resources in B. atratus and B. bellicosus was influenced by their proboscis length. Bombus atratus has a longer proboscis and preferably visited red clover, possibly obtaining nectar easier and faster than B. bellicosus, which has a shorter proboscis. Bombus bellicosus used both resources without any clear preference.     

The extremely long-tongued neotropical butterfly Eurybia lycisca (Riodinidae): proboscis morphology and flower handling

Few species of true butterflies (Lepidoptera: Papilionoidea) have evolved a proboscis that greatly exceeds the length of the body. This study is the first to examine the morphology of an extremely long butterfly proboscis and to describe how it is used to obtain nectar from flowers with very deep corolla tubes. The proboscis of Eurybia lycisca (Riodinidae) is approximately twice as long as the body. It has a maximal length of 45.6?mm (mean length 36.5?mm?±?4.1?S.D., N?=?20) and is extremely thin, measuring only about 0.26?mm at its maximum diameter. The proboscis has a unique arrangement of short sensilla at the tip, and its musculature arrangement is derived. The flower handling times on the preferred nectar plant, Calathea crotalifera (Marantaceae), were exceptionally long (mean 54.5?sec?±?28.5?S.D., N?=?26). When feeding on the deep flowers remarkably few proboscis movements occur. The relationship between Eurybia lycisca and its preferred nectar plant and larval host plant, Calathea crotalifera, is not mutualistic since the butterfly exploits the flowers without contributing to their pollination. We hypothesize that the extraordinarily long proboscis of Eurybia lycisca is an adaptation for capitalizing on the pre-existing mutualistic interaction of the host plant with its pollinating long-tongued nectar feeding insects.     

Flies and concealed nectar sources: morphological innovations in the proboscis of Bombyliidae (Diptera)

Bee-flies (Bombyliidae) have morphological adaptations of the mouthparts to particular floral traits. To investigate this the short, plesiomorphic proboscis of Hemipenthes morio was compared with the long, apomorphic proboscis of Bombylius major . A novel feeding position enables B. major to use flowers that open to the side as additional nectar sources. The new horizontal feeding position is enabled by the prolonged ventral base of the proboscis. Bombylius major exploits deep corolla tubes with an elongate proboscis, and an increased efficiency in both the suction pumps and the sealing mechanisms of the proboscis. The exploitation of narrow corolla tubes is made possible by the shift from a sponging feeding mode, exhibited by H. morio , to the exclusively sucking mode in B. major . Besides quantitative changes in the proportions of the different proboscis components, labellar movements as well as the structures of saliva distribution are changed along with this shift. The labial musculature of B. major does not significantly differ from the plesiomorphic state, since both examined species do not only feed on nectar, but also on pollen.     

The flower and blossom morphology of Asteraceae correlates with composition of their pollinators

The correlation between flower morphology and share of different insect groups visiting them was studied for 15 Asteraceae species. We measured length and width of corolla tube of 100 flowers of each plant species and determined proportions of main groups of anthophilous insects during all blooming period. According to corolla length species under study ranged more or less uniformly from 2.16 mm (Tripleurospermum inodorum) up to 21.06 mm (Cirsium heterophyllum). The correlation between share of long-tongued bees (mainly bumblebees) among all visitors of inflorescens and corolla length was positive (r = 0.737, P < 0.01) while for short-tongued flies (Syrphidae, Muscidae, Calliphoridae) it was negative (r = -0.869, P < 0.01). It is interesting, that the point of crossing of regression lines (12 mm) approximately coincides with change in inflorescences coloration. Plants with corolla length less than 10 mm have yellow or white inflorescences that are visited primarily by flies, while the plants with longer corolla have violet or dark blue inflorescences, by bumblebees. The dependence of proportion of short-tongued solitary bees (Andrenidae, Halictidae) on a corolla length was non-linear. It increased with increase in corolla length in an interval of 2.16-6.26 mm (r = 0.930, P < 0.1), but decreased for longer corollas (r = -0.680, P < 0.05). The correlation between corolla length and proportions of beetles and butterflies were insignificant.     

Flower choice copying in bumblebees

We tested a hypothesis originating with Darwin that bees outside the nest exhibit social learning in flower choices. Naive bumblebees, Bombus impatiens, were allowed to observe trained bees or artificial bees forage from orange or green flowers. Subsequently, observers of bees on green flowers landed more often on green flowers than non-observing controls or observers of models on orange flowers. These results demonstrate that bumblebees can change flower choice by observations of non-nest mates, a novel form of social learning in insects that could provide unique benefits to the colony.     

Scaling of nectar foraging in orchid bees

Morphology influences the rate at which foraging bees visit nectar flowers, the quantity of nectar they must consume to fuel their activities, and, consequently, the profitability of flower species. Because feeding time is a major determinant of visitation rate, I used a biomechanical model to examine how energy intake rate (E) varies with sucrose concentration, body mass (M), and proboscis length in orchid bees (Apidae: Euglossini). Under geometric scaling, the optimal sugar concentration (Smax) should be largely independent of body size, and E proportional to M1.0. In a comparative study of 30 orchid bee species ranging from 50 to 800 mg, Smax fell between 35% and 40% w/w, but E proportional to M0.54, significantly less than model predictions. Proboscis length and radius scale geometrically with body mass, but proboscis length exhibits substantial size-independent variation, particularly in small bees. One cost of a long proboscis is a reduction in both E and Smax in accordance with the scaling model. This finding highlights a difference between the lapping mechanism used by bumblebees and the suction mechanism used by orchid bees. A field study confirms that orchid bees harvest nectars with between 34% and 42% sucrose, independent of body size.     

Secondary contact and adaptation to local pollinator assemblages mediate geographical variation in corolla length in Isodon shikokianus

Adaptation to local pollination regimes and secondary contact of allopatrically differentiated populations with respect to pollination ecology may result in geographical variation in floral traits. We examined the contributions of these two processes in Isodon shikokianus, which showed remarkable geographical variation in corolla tube length in western Japan. Corolla tube length varied among 17 study populations located within a relatively narrow area, and covaried with altitude and distribution of two bumblebee pollinators with different tongue lengths: the longer corolla was found at lower altitudes where the long-tongued pollinator was more abundant, and vice versa. Additionally, bumblebee species preferentially visited flowers that fit their tongue lengths. Population genetic analysis based on 11 microsatellite loci revealed that populations with long and short corolla tubes constituted genetically distinct groups. Migration rates were low between the groups, but high within each group. These results indicate that two genetically differentiated groups made secondary contact and hybridized, and gene flow between the groups was limited. Thus, the geographical variation in corolla tube length in I. shikokianus may be a result of past allopatric differentiation and subsequent secondary contact of populations with different corolla tube lengths. The variation in corolla tube length within a narrow area may be maintained by selection owing to the altitudinally structured pollinator assemblages. Altitudinal differences in relative abundance of two pollinators and their assortative visitation with respect to corolla tube length may contribute to reproductive isolation between the two groups.     

Nectarless flowers with deep corolla tubes in Pedicularis: does long pistil length provide an arena for male competition?

Pollinator‐mediated selection does not seem to have a direct influence on the evolution of a long corolla tube in a nectarless flower. We hypothesized that the long pistil length of the nectarless flower with a deep corolla tube provided an opportunity for male competition. Pedicularis siphonantha, a nectarless and partially self‐incompatible lousewort with substantial variation in corolla tube length, was used to test the hypothesis. We tested whether and how corolla tube length affected seed production per capsule and seed germination rate with different pollination treatments. Flowers were hand‐pollinated with pollen from one self donor and one outcross donor and mixed pollen grains consisting of equal amounts from the two donor types, respectively. Additionally, seeds from open‐pollinated flowers with different corolla tube lengths were collected separately for measurement of germination rate. Pollination treatment and corolla tube length significantly affected number of seeds per capsule. Moreover, a significant positive relationship between seeds per capsule and corolla tube length was found when mixed hand pollination was conducted. Seeds of self hand‐pollinated flowers had a lower germination rate than those from outcross‐pollinated flowers. Under open pollination, seeds from flowers with longer corolla tubes tended to have higher germination rate. In P. siphonantha, outcross pollen may have a higher probability of contributing to the next generation when transferred to flowers with longer corolla tubes. The pistil length, therefore, should be seen as a female choice mechanism, which provides an arena for male‐to‐male competition. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 526–532.     

Pollinator Restriction in the Narrow-tube Flower Type of Mertensia ciliata (James) G. Don (Boraginaceae)

Abstract Mertensia ciliata (Boraginaceae) includes two flower types with different corolla tube widths, wide and narrow. The former is pollinated by both queens and worker bumblebees, while the latter type is pollinated exclusively by bumblebee workers. Morphological comparisons between the flowers and the bumblebees showed that the relationship between the width of the corolla tube mouth and the head width of the bumblebee is a primary factor restricting pollinators to workers in the narrow-tube type. Length of the proboscides and corolla tube are of secondary importance for this restriction, since some queens are not able to reach the bottom of a narrow corolla tube even if their proboscis is extended fully.     

Structure in seven bumblebee communities in eastern Finland in relation to resource availability

The structure of seven local bumblebee communities was studied in eastern Finland. The number of species in the study sites varied from 5 to 10, 11 being the number in the species pool. Most of the species (queens) had proboscis lengths of 8–11 mm. When floral resources were analysed on the basis of corolla tube depths, a group was found between 4 and 8 mm. In terms of flower utilization, species with similar proboscises had higher pairwise niche overlaps than species differing by their proboscis lengths.
Spacing between neighbouring species along the proboscis length dimension was not more uniform in the realized communities than what was expected on the basis of random draws from the local species pool. The results were the same for all species observed in the communities and for the abundant species only (frequency >5%), although competition among species in the latter group is expected to be more intense.
When the structure of bumblebee communities and of floral resources was expressed in terms of diversity of proboscis lengths and corolla tube depths, respectively, a positive correlation was found. Data suggest that species with similar proboscis tend to co-occur on fields with availability of appropriate corolla tubes.     

Are long corolla tubes in Pedicularis driven by pollinator selection?

The evolution of long corolla tubes has been hypothesized to be driven by long-tongued pollinators.Corolla tubes in Pedicularis species can be longer than 10 cm which may function as flower stalks to increase visual attractiveness to pollinators because these species provide no nectar and are pollinated by bumblebees. The corolla tube length was manipulated(shorter or longer) in two Pedicularis species in field to examine whether longer tubes are more attractive to pollinators and produce more seeds than short tubes. Our results did not support the pollinator attraction hypothesis, leaving the evolution of long tubes in Pedicularis remains mysterious.     

Morphological variation in relation to flower use in bumblebees

To understand resource partitioning in a bumblebee community, we analyzed various morphological characters. A total of 1269 individuals of six bumblebee species, Bombus ardens, B. hypocrita, B. diversus, B. ignitus, B. honshuensis and B. beaticola, were examined and principal component analysis showed that the bumblebee species were clearly differentiated. Glossa, prementa and head lengths were positively correlated with the second component, and a longer proboscis was associated with a narrower body, which may help bees to intrude into and access deep‐lying nectar sources. Bombus diversus, with a long proboscis and narrow body, preferred flowers with a long corolla tube, whereas B. hypocrita and B. ignitus, which have short proboscises and wide bodies, visited flowers with short corollas or dish‐shaped flowers. Two pairs of consubgeneric species that have similar morphological characteristics, B. ardens and B. beaticola, and B. hypocrita and B. ignitus, divided flower resources by habitat selection and seasonal partitioning. For resource partitioning among bumblebee species, not only morphology but also other factors, such as habitat and seasonal preference, flower use, foraging behavior, and interspecific interactions, are responsible.     

Why are there so many species of bumble bees at Dungeness?

WILLIAMS, P. H., 1989. Why are there so many species of bumble bees at Dungeness? Dungeness is unique in the British Isles in that it has more species of bumble bees than any other locality. Three ideas about what governs the number of species at a locality are examined by locking at patterns of flower visits at Dungeness in comparison with those at Shoreham, a species-poor locality also in Kent. The species of bumble bees that are present at Dungeness but absent from Shoreham show no association in their distributions among 2 km grid-squares in Kent with the species of food-plants that they prefer at Dungeness, nor is there any correlation between the diversity of bees and diversity of food-plants at Dungeness and Shoreham. From the information available, Dungeness is most likely to have more species of bumble bees because it has a particularly high density of the more nectar-rich flowers that bumble bees can use. Bumble bees feed most profitably from deep flowers because these contain more nectar than shallow flowers, although direct access to deeper flowers is ultimately limited by the length of each bee's proboscis. The distribution of worker proboscis lengths among species in the species-pool in Kent is clumped about a median of 7.9 mm. The best foraging conditions for the maximum number of species should be provided when flowers of similar depths are present in sufficiently large numbers for all foragers to make near-optimal flower choices. Although there is no difference in median between the distributions of the bees' proboscis lengths and the depths of the flowers they use at Dungeness, at Shoreham the flower depths used are shorter than the proboscis lengths. Among the food-plants at Dungeness, high densities of Teucrium scorodonia and Echium vulgare are likely to be especially important.     

The Role of Flower Width in Hummingbird Bill Length‐Flower Length Relationships1

Observations of hummingbirds feeding at flowers longer or shorter than their bills seem to contradict the view that bill lengths of hummingbirds evolved in concert with the lengths of their flowers. Recent experiments, however, indicate that a hummingbird's ability to feed at artificial flowers of different lengths depends on the widths of the flowers. We examined if the broad range of flower lengths visited by many hummingbird species can be explained by the widths of the flowers. We predicted that both short‐ and long‐billed hummingbirds would include long, wide flower species in their diets, but that short‐billed hummingbirds would not include long, narrow flower species because nectar in these species might be beyond the reach of their bills. If so, the slope of the regression for flower width versus flower length should be smaller for flower species visited by longer‐billed hummingbirds relative to those visited by shorter‐billed hummingbirds. Analyses of data sets for some North American and Monteverde hummingbirds and their food plants were consistent with this prediction, and bill lengths were significantly correlated with the slopes of the regressions of flower width versus length for seven hummingbird species. Comparisons of observed flower use by some Monteverde hummingbird species to flower assemblages generated at random suggest that these significant regressions were not simply a result of allometric relationships between flower lengths and widths, but in some cases reflected active choice by the birds. The two hummingbird–flower data sets also differed significandy in the scaling of corolla width relative to corolla length. In particular, the Monteverde data set contained a large number of long, narrow flower species, which we suggest is a consequence of a different floral evolutionary history and association with long‐billed hummingbird species. The evolutionary effects of hummingbirds and their flowers upon one another are more complex than has generally been realized, and a consideration of corolla length jointly with other floral characters may improve our understanding of hummingbird‐flower relationships.     

The spatial distribution of nonrewarding artificial flowers affects pollinator attraction

Many species of orchids that do not offer food rewards to pollinators bloom in clusters, early in the season, and are polymorphic for corolla colour. Previous studies suggest that the foraging behaviour of insect pollinators may select for early blooming and colour polymorphism. I tested whether pollinator behaviour can also favour aggregated flowering in these species, in a two-stage laboratory experiment on na?ve bumblebees, Bombus terrestris (L.). In the first stage, the bees were allowed to forage on three colours of artificial flowers that contained sucrose rewards. In the second stage, I added nonrewarding flowers of a fourth colour and recorded the bees' visits to them. The four types of artificial flowers were either arranged in spatially distinct clusters, or were randomly intermingled. I used two reward schedules for each spatial arrangement: constant refilling of reward-containing flowers and probabilistic refilling. Bees that foraged on clustered flowers flew more often to the nonrewarding patch, and made more visits to nonrewarding flowers, than bees that foraged on intermingled flowers. This tendency was obtained both in the constant reward and in the probabilistic reward schedules. The results support the hypothesis that pollinator attraction may select for clustered, synchronized blooming in flowers that do not contain nectar and pollen rewards. Copyright 2000 The Association for the Study of Animal Behaviour.     

Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon

We compared pollen removal and deposition by hummingbirds and bumblebees visiting bird-syndrome Penstemon barbatus and bee-syndrome P. strictus flowers. One model for evolutionary shifts from bee pollination to bird pollination has assumed that, mostly due to grooming, pollen on bee bodies quickly becomes unavailable for transfer to stigmas, whereas pollen on hummingbirds has greater carryover. Comparing bumblebees and hummingbirds seeking nectar in P. strictus, we confirmed that bees had a steeper pollen carryover curve than birds but, surprisingly, bees and birds removed similar amounts of pollen and had similar per-visit pollen transfer efficiencies. Comparing P. barbatus and P. strictus visited by hummingbirds, the bird-syndrome flowers had more pollen removed, more pollen deposited, and a higher transfer efficiency than the bee-syndrome flowers. In addition, P. barbatus flowers have evolved such that their anthers and stigmas would not easily come into contact with bumblebees if they were to forage on them. We discuss the role that differences in pollination efficiency between bees and hummingbirds may have played in the repeated evolution of hummingbird pollination in Penstemon.     

Interaction between oil-collecting bees and seven species of Plantaginaceae

Oil-bee/oil-flower mutualism evolved through multiple gains and losses of the ability to produce floral oil in plants and to collect it in bees. Around 2000 plant species are known to produce floral oils that are collected by roughly 450 bee species, which use them for the construction of nests and for the larval food. The Plantaginaceae contain several Neotropical species that produce floral oils, the main reward offered by these plants. In the genera Angelonia, Basistemon, Monopera and Monttea, mainly associated with Centris bees, the floral oil is produced in trichomes that are located in the inner corolla. The pollinators of a few species in this neotropical clade of Plantaginaceae are known, and the role of flower morphology as well as the requirements from pollinators and the role of other groups of bees in the pollination of these flowers remains unclear. In this paper we provide a list of the flower visitors of seven Plantaginaceae species (six Angelonia species and Basistemon silvaticus) analyzing their behavior to highlight the legitimate pollinators and illustrating little known aspects of flower morphology and oil-collecting apparatuses of the bees. Two general morphological patterns were observed in the Angelonia flowers: deep corolla tube with short lobes, and short corolla tube with long lobes. Corolla tubes of different length result in pollen adherence to different parts of the insect body. The six Angelonia species and B. silvaticus flowers were visited by 25 oil-collecting bee species (10 Centris, 11 Tapinotaspidini and 4 Tetrapedia species), the majority acting as legitimate visitors. The flowers were also visited by illegitimate bee pollinators, which collected pollen but do not transfer it to the female organ. Specialized collectors of Plantaginaceae floral oils present modifications on the first pair of legs, mainly in the basitarsi but also extended to the tarsomeres. The new records of Tapinotaspidini and Centridini species acting as specialized pollinators of Plantaginaceae suggest that there is a geographic variation in the pollinators of the same plant species, and that the evolutionary scenario of the historical relationships between oil-collecting bees and floral oil producing plants is more complex than previously considered.     

DOWN THE TUBE: POLLINATORS, PREDATORS, AND THE EVOLUTION OF FLOWER SHAPE IN THE ALPINE SKYPILOT, POLEMONIUM VISCOSUM

Abstract We address how a conflict between pollinator attraction and avoidance of flower predation influences the evolution of flower shape in Polemonium viscosum. Flower shape in P. viscosum is the product of an isometric relationship between genetically correlated (r_A= 0.70) corolla flare and length. Bumblebee pollinators preferentially visit flowers that are more flared and have longer tubes, selecting for a funnel‐shaped corolla. However, flower shape also influences nectar‐foraging ants that sever the style at its point of attachment to the ovary. Surveys of ant damage show that plants having flowers with flared, short corollas are most vulnerable to ant predation. Consistent with this result, the ratio of corolla length to flare is significantly greater in a krummholz (high predation risk) population than in a tundra (low predation risk) population. To explicitly test whether the evolution of a better defended flower would exact a cost in pollination, we created tubular flowers by constricting the corolla during development. Performance of tubular flowers and natural controls was compared for defensive and attractive functions. In choice trials, ants entered control flowers significantly more often than tubular ones, confirming that the evolution of tubular flowers would reduce the risk of predation. However, in a bumblebee‐pollinated population, tubular flowers received significantly less pollen and set fewer seeds than controls. A fitness model incorporating these data predicts that in the absence of the genetic correlation between corolla length and flare, intermittent selection for defense could allow tubular flowers to spread in the krummholz population. However, in the tundra, where bumblebees account for nearly all pollination, the model predicts that tubular flowers should always confer a fitness disadvantage.