Floral isolation between Aquilegia formosa and Aquilegia pubescens

The acquisition of floral nectar spurs is correlated with increased species diversity across multiple clades. We tested whether variation in nectar spurs influences reproductive isolation and, thus, can potentially promote species diversity using two species of Aquilegia, Aquilegia formosa and Aquilegia pubescens, which form narrow hybrid zones. Floral visitors strongly discriminated between the two species both in natural populations and at mixed-species arrays of individual flowers. Bees and hummingbirds visited flowers of A. formosa at a much greater rate than flowers of A. pubescens. Hawkmoths, however, nearly exclusively visited flowers of A. pubescens. We found that altering the orientation of A. pubescens flowers from upright to pendent, like the flowers of A. formosa, reduced hawkmoth visitation by an order of magnitude. In contrast, shortening the length of the nectar spurs of A. pubescens flowers to a length similar to A. formosa flowers did not affect hawkmoth visitation. However, pollen removal was significantly reduced in flowers with shortened nectar spurs. These data indicate that floral traits promote floral isolation between these species and that specific floral traits affect floral isolation via ethological isolation while others affect floral isolation via mechanical isolation.     

Flower reshaping in the transition to hummingbird pollination in Loasaceae subfam. Loasoideae despite absence of corolla tubes or spurs

Many angiosperm lineages present transitions from bee to hummingbird pollination. The flower design in most of these lineages includes either corolla tubes or nectar spurs, structures that commonly experienced an elongation with the acquisition of hummingbird pollination. It is proposed that this increases the fit between the bird head and flower structures, and isolates or partially blocks bees from the interaction. But can this transition occur if the ancestral flower design lacks tubes or spurs? Here we focus on the transition from bee to hummingbird pollination in the Loasaceae subfamily Loasoideae. Loasoideae flowers have radial corollas with separated petals; therefore, they do not display corolla tubes nor nectar spurs. These flowers also present a whorl of nectar scales and staminodes, unique to the subfamily, which is involved in flower–pollinator fit and in nectar harvesting. To explore flower shape adaptation to hummingbird pollination, we tested for correspondence between pollinators and flower shape in Loasoideae. In order to achieve this, we first compared the evolutionary history of flower phenotype and pollination mode, and then used stochastic character mapping and geometric-morphometric variables in a comparison of alternative evolutionary models. The results of our study suggest that the transition from bee to bird pollination was accompanied by changes in the shape of the staminodial complex, along with the evolution of relatively closed corollas. Moreover, while bird pollination seems to be the end point in the evolution of pollination syndromes in many angiosperm lineages, rodent pollinated flowers probably evolved from ancestral bird pollinated flowers in Loasoideae. Our findings suggest that the evolution of bird pollinated flowers from ancestral bee pollinated flowers does not require the presence of corolla tubes or spurs, and can take place as long as the flower design includes structures participating in flower–pollinator fit.     

Pollinators and nectar robbers cause directional selection for large spur circle in Impatiens oxyanthera (Balsaminaceae)

Nectar spurs have an important role in floral evolution and plant–pollinator coadaptation. The flowers of some species possess spurs curving into a circle. However, it is unclear whether spur circle diameter is under direct selection pressure from different sources, such as pollinators and nectar robbers. In this study, we quantified selection on some floral traits, such as spur circle diameter in Impatiens oxyanthera (Balsaminaceae) using phenotypic selection analysis and compared the relative importance of pollinators and nectar robbers as selective agents using mediation analysis. The study showed that pollinators caused significant selection on corolla length, spur curvature and spur circle diameter while nectar robbers only imposed strong selection on spur circle diameter. Pollinators favored flowers with large corolla, curly spurs and large spur circle while nectar robbers preferred flowers with small spur circle. More pollinator visits resulted in higher female reproductive success, while robbery reduced female fitness. Conflicting selection on spur traits from pollinators and nectar robbers was not found. Mediation analysis showed that selection on floral traits through nectar robbing was stronger than selection through pollination. The results suggested that pollinators and nectar robbers jointly mediated the directional selection for large spur circle, and nectar robbers caused stronger selection than pollinators on floral traits.     

Effects of fire frequency on oak litter decomposition and nitrogen dynamics

Rapid speciation within some plant families has been attributed to the evolution of floral spurs and to the effect of spur length on plant reproductive success. The flowers of Impatiens capensis (jewelweed) possess a long, curved spur in which nectar is produced and stored. Spur length and curvature varies among plants within one population. Here I document that spur shape is variable in natural populations, variation within plants is less than variation among plants, and spur shape is correlated with components of female and male reproductive success. The apparent natural selection is weakly directional in 1 of 2 years, with greatest seed production and pollen removal occurring in flowers with the greatest spur curvature. Bee pollinator visit length is longest at flowers with highly curved spurs, and they leave less nectar in these spurs than in flowers with straighter spurs. Spur angle evolution may be limited, at least in part, by opposing selection by nectar-robbers who prefer to visit flowers with greater spur curvature. Other factors that might contribute to the maintenance of spur angle variation are temporal variation in the strength of selection and potential genetic correlations of spur shape with other traits under selection.     

Long Tongues and Loose Niches: Evolution of Euglossine Bees and Their Nectar Flowers1

I examined relationships between tongue length of orchid bees (Apidae: Euglossini) and nectar spur length of their flowers in the genera Calathea, Costus, and Dimerocostus using phylogenetically independent contrasts. Long‐tubed flowers have specialized on one or several species of long‐tongued euglossine bees, but long‐tongued bees have not specialized on long‐tubed flowers. Whereas long tongues may have evolved to provide access to a wider variety of nectar resources, long nectar spurs may be a mechanism for flowers to conserve nectar resources while remaining attractive to traplining bee visitors.     

Ineffectiveness of nectar scent in generating bumblebee visits to flowers of Impatiens textori

To clarify if bumblebees can recognize nectar through its scent in Impatiens textori flowers, we examined the behavior of Bombus diversus on nectarless flowers in which the spurs had been artificially removed. Bumblebee visits to both natural flowers and spur‐cut flowers were captured using a long‐term video recording system. Visiting behavior and frequency were compared between the two flower types. Many bumblebees visited both types of flower, and their visit frequencies were not significantly different. However, the length of stay on each flower type did differ, with the bumblebees remaining on the spur‐cut flowers for a significantly shorter time than on the natural flowers. Our results suggest that bumblebees cannot detect the absence of nectar in I. textori flowers before probing them. Therefore, the nectar scent of I. textori does not serve to attract bumblebees although the presence of nectar will detain bumblebees on flowers for longer periods.     

Hawkmoth pollination of aerangoid orchids in Kenya, with special reference to nectar sugar concentration gradients in the floral spurs

The African orchid flora has a high proportion of species with long-spurred white flowers. Few data exist to test the prediction that this floral syndrome pattern reflects an important role for hawkmoth pollination in the evolution and ecology of these orchids. The pollination biology of five aerangoid orchid species (Rangaeris amaniensis, Aerangis brachycarpa, A. confusa, A. thomsonii, and A. kotschyana) was investigated in Kenya. Four of these have long spurs (>10 cm) and were pollinated by Agrius convolvuli and Coelonia fulvinotata. Aerangis confusa, which has relatively short spurs (ca. 4 cm), was pollinated by the short-tongued hawkmoths Hippotion celerio and Daphnis nerii. Nectar frequently filled the entire spur in some of the study species, even at anthesis. Sugar concentration of the nectar of four species was found to vary from ca. 1% at the mouth of the spur to 20% at the tip. Gradients were expressed more strongly in species with long, straight spurs. Species with spirally twisted spurs showed both steep and shallow nectar gradients. These gradients, previously unknown in plants, may function as a "sugar trail," enticing long-tongued hawkmoths to probe deeply into spurs without incurring the cost of filling an entire spur with concentrated nectar. In addition, the most concentrated nectar is kept out of reach of short-tongued pollinators.     

An examination of nectar production in 34 species of Dendrobium indicates that deceptive pollination in the orchids is not popular

Nectar, the most common floral reward, is generally used to determine whether an orchid species involves deceptive pollination. Estimates of the deceptive pollination systems with nectarless flowers have ranged from one quarter to one third of the nearly 30 000 species of orchids. These estimates, however, are biased towards temperate-zone, usually terrestrial, orchids. Here we investigated nectar production and property in 34 epiphytic orchid species of the Southeast Asian genus Dendrobium. Twenty-one species were observed producing nectar. The amount and sugar concentration (in bagged flowers) of 12 species varied from 0.45 to 2.78 μL and from 8.1% to 31.1%. The nectar was sucrose-dominant, typical of bee-pollinated flowers. Reconstruction of phylogenetic relationship indicated that transition of nectar secretion occurred in the genus. Spur length was positively correlated with flower size but species with relatively long spurs tended to produce small volume of nectar. Nectar production was strikingly variable among and within individuals in some species, suggesting that a vital measurement of bagged and fresh flowers is needed. Given that the quantitative measurement of nectar or floral reward in orchid species remains scarce, an estimate of deceptive pollination systems awaits further survey in diverse genera.     

Relationship between floral tube length and nectar robbing in Duranta erecta L. (Verbenaceae)

Although nectar robbing is a common phenomenon in plant species with tubular flowers or flowers with nectar spurs, the potential effect of this illegitimate interaction on plant reproductive success has not received the deserved attention. In the present study, we analysed the functional relationship between flower morphology and nectar robbing, and examined the reproductive consequences of the interaction in a population of Duranta erecta (Verbenaceae) on the island of Cuba. The results show that nectar robbing is conducted by the carpenter bees Xylocopa cubaecola and affects up to 44% of flowers in the studied population. However, not all the flowers have the same probability of being robbed. The chance of flowers being robbed increases with flower length and flower diameter. Moreover, nectar robbing significantly decreases the chance that flowers will set fruit. Also, the impact of nectar robbing on the probability of flowers to set fruits is dependent on the plant. We suggest that nectar robbing may represent an opposite selective force that balances the selection for longer corollas often imposed by pollinators specializing in visiting tubular flowers. Such a relationship with nectar robbers would have obvious implications for the evolution of tubular or closed flowers. This preliminary finding deserves further research in light of the ecological and evolutionary consequences of nectar robbing in tubular flowers.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 392–398.     

Bumblebee visits to Impatiens spp.: pattern and efficiency

Summary Three Japanese species of Impatiens, which secrete nectar continuously in long spurs, were visited by Bombus diversus workers consecutively throughout the day. B. diversus workers showed characteristic patterns of behavior in flower use, flower choice, and patch departure. (1) Bumblebees stayed longer on a flower which had been unvisited for a while than on a flower which had been visited recently. (2) Bumblebees preferred visiting flowers which had been unvisited for a while to visiting those which had been visited recently, and to visiting those which had been unvisited for a long period. (3) Bumblebees had a higher probability of leaving a patch after they had stayed on a flower for a short period than after they had stayed for a longer period. The bumblebees appeared to perceive both remotely and proximately chemical cues deposited by other foraging individuals, which indicated nectar rewards in a flower, and thus obtained a higher nectar intake than the mean amount of nectar left in a flower.     

Bird pollination in South African species ofSatyrium (Orchidaceae)

Field observations showed that three South African orchid species,Satyrium carneum, S. coriifolium andS. princeps, are pollinated by sunbirds. Foraging sunbirds insert their bills into the labellum chamber of the flowers and suck nectar from the labellum spurs with their tongues. The column overarches the entrance to the labellum and pollinaria become affixed to the upper mandible of the bill. Birds often attempt to remove pollinaria by rubbing their bills against a branch, but are mostly unsuccessful due to the large plate-like viscidia which attach the pollinaria very firmly to the bill. Other modifications for bird pollination in theseSatyrium species may include the red, carmine or orange colour of the flowers, sturdy inflorescence stems used for perching and large amounts of dilute nectar in the spurs. EachSatyrium species was pollinated by several species of sunbird, and despite some differences in flowering time, occasional hybrids occur at a site whereS. carneum andS. coriifolium share the same sunbird pollinators.     

Specialized pollination in the African milkweed Xysmalobium orbiculare: a key role for floral scent in the attraction of spider-hunting wasps

Specialized pollination by prey-hunting wasps is poorly documented in rewarding plants. Furthermore, the mechanisms of achieving specialization are not clear since flowers typically produce exposed nectar and have no morphological adaptations (such as long spurs) to exclude non-pollinating visitors. We investigated the pollination of Xysmalobium orbiculare and explored the functional roles of floral scent and nectar in attracting pollinators and deterring nectar robbers. Floral visitor observations showed that this milkweed is visited almost exclusively by pompilid wasps in the genus Hemipepsis. These wasps were the only insects to carry pollinia, and a cage experiment confirmed their effectiveness in removing and inserting pollinia on flowers. Hand-pollinations showed that plants are genetically self-incompatible and thus reliant on pollinators for seed set. Palatability experiments with honeybees showed that nectar is distasteful to non-pollinating insects and is therefore likely to play a functional role in deterring nectar thieves. Choice experiments in the field showed that the wasp pollinators are attracted primarily by floral scent rather than visual cues. Analysis of spectral reflectance of flowers revealed that flowers are dull colored and are unlikely to stand out from the background vegetation. We conclude that X. orbiculare is specialized for pollination by spider-hunting wasps in the genus Hemipepsis and utilizes floral scent to selectively attract its pollinators and unpalatable nectar to deter non-pollinating visitors.     

Effective pollinia transfer by settling moths’ legs in an orchid Habenaria aitchisonii

A great diversity of flower morphology in orchids has long been thought to be selected by diverse pollinators. Habenaria Willd. (Orchidaceae) species are generally characterized by long nectar spurs and pollinated by long‐tongued insects (Lepidoptera), the mechanical fit between the spur and pollinator proboscis length being supposedly caused by “arms race” reciprocal selection. Here, we report that flowers of Habenaria aitchisonii Rchb. f. with nectar spurs (approximately 9 mm) were pollinated by three species of settling noctuid moths whose proboscises varied in length from 10 to 16 mm. When a settling moth crawled on the spikes and probed the flowers for nectar, pollinia were placed on the moths’ legs rather than on other body parts. Our 5‐year survey of pollinia movement and 3‐year supplemental pollination experiments indicated that fruit and seed production in this orchid were not often pollen‐limited at flower level. In a natural population in Shangri‐La, Southwest China, the proportions of pollinia removal and deposition on stigmas by moth legs were 93.8% and 83.5%, respectively. This finding of efficient pollen transfer by the pollinators’ legs in H. aitchisonii adds a new example of diverse pollinia placement on pollinators (here settling moths) in the Orchidaceae.     

Robber-like pollinators: overwintered queen bumblebees foraging on Corydalis ambigua

ABSTRACT.

• 1 The behaviour of nectar-collecting Bombus hypocrita sapporensis Cockerell queens was observed on a population of a spring ephemeral plant Corydalis ambigua Cham, et Schlecht.
• 2 Daily patterns of activity and behaviour changed with the progress of flowering. Activity peaked shortly before sunset early in the flowering season but approximately at noon towards the end of flowering. In the peak flowering period the queens tended to visit nearby plants and to change direction often, whereas early or late in the flowering period they flew further between visits and were less likely to change direction.
• 3 Each plant was visited 0 to 24 times (mean 9.4 ±SD 5.2) by the queens during the whole flowering season.
• 4 The queens collected nectar, rarely through the front of the flowers but mostly through the spurs perforated by themselves or predecessors. At the beginning of the flowering season the illegitimate foragers often visited the front of the flowers before moving to the spurs; later, most queens quickly learned to land directly on the spurs.
• 5 Even the 59.7% of plants that were visited only by illegitimate foragers set seeds. Close observation confirmed that the illegitimate foragers opened the inner petals enclosing anthers and stigma frequently when visiting the front of the flowers before robbing, or occasionally when walking about on the flowers or collecting nectar through the perforated spurs.

     

THE POLLINATION ECOLOGY OF AQUILEGIA ELEGANTULA AND A. CAERULEA (RANUNCULACEAE) IN COLORADO

Aquilegia elegantula Greene and A. caerulea James occur in montane and subalpine habitats in the southern Rocky Mountains of western North America. The red and yellow flowers of A. elegantula are nodding, odorless, protogynous, and secrete a concentrated (44%) sucrose nectar in the floral spurs. Seed set in flowers under pollinator exclosures was 12% while seed set in open-pollinated flowers was 65%. The flowers of A. elegantula are pollinated primarily by the Broad-tailed Hummingbird (Selasphorus platycercus [Swainson]) and by at least three species of pollen-foraging bumblebees, of which Bombus occidentalis Greene is the most common. The blue and white flowers of A. caerulea are erect, mildly fragrant, protandrous, and secrete a 26% sucrose nectar. Seed set in caged flowers in the field averaged 39%. in uncaged flowers 54%. The most important pollinators of A. caerulea are the crepuscular hawkmoth, Hyles (=Celerio) lineata (Fabricius) and ten species of pollen-foraging Bombus. The most abundant bumblebee species, B. occidentalis, is also a frequent nectar thief. Differences in pollination systems alone probably do not constitute an effective anti-hydridization mechanism between A. elegantula and A. caerulea, but do serve to reinforce differences in habitat and flowering time that distinguish the two species.     

The bumblebee Bombus ardens ardens (Hymenoptera: Apidae) visits white clover in orchards before Oriental persimmon blooms

Flowers on the ground of orchards can provide substantial resources for wild pollinators of orchard trees. Few studies, however, have examined the relative importance of groundcover flowers to orchard pollination by analyzing pollen on the body surface of pollinators. Oriental persimmon trees bloom within the longer blooming period of white clover, which is occasionally found as a flowering plant on the ground of persimmon orchards in Japan. The present study compared the insect species assemblage collected on persimmon flowers with that on clover. Before persimmon bloomed, Bombus ardens ardens and Apis cerana japonica were the major visitors of clover flowers. Once persimmon bloomed, the former was the most abundant bee that visited persimmon flowers over the flowering period. Apis mellifera was captured only on clover flowers. We found numerous clover pollen grains on the body surface of bumblebees captured on persimmon flowers, but far fewer persimmon pollen grains on bees that visited clover. These findings show that B. ardens ardens utilized the clover flowers under the orchards before persimmon bloomed.     

Lack of floral nectar reduces self-pollination in a fly-pollinated orchid

One explanation for the widespread absence of floral nectar in many orchids is that it causes pollinators to visit fewer flowers on a plant, and thus reduces self-pollination. This, in turn, could increase fitness by reducing inbreeding depression in progeny and promoting pollen export. The few previous investigations of this hypothesis have all involved bee-pollinated orchids and some have given contradictory results. We studied the effects of adding artificial nectar (sucrose solution) to the spurs of a non-rewarding long-proboscid fly-pollinated orchid, Disa pulchra. Addition of nectar significantly increased the number of flowers probed by flies (2.6-fold), the time spent on a flower (5.4-fold), the number of pollinia removed per inflorescence (4.8-fold) and the proportion of removed pollen involved in self-pollination (3.5-fold). The level of self-pollination increased dramatically with the number of flowers probed by flies. Experimental self-pollination resulted in fruits with only half as many viable seeds as those arising from cross-pollination. Pollinators were more likely to fly long distances (>40 cm) when departing from non-rewarding inflorescences than when departing from rewarding ones. These findings provide support for the idea that floral deception serves to reduce pollinator-mediated self-pollination.     

The diversification of Halenia (Gentianaceae): ecological opportunity versus key innovation

The plant genus Halenia (Gentianaceae) consists of herbs growing in temperate and tropical alpine habitats and most species possess flowers in which nectar is produced in spurs. This probably helps reward only specialized long-tongued pollinators, and a narrow pollinator/flower relationship is thought to accelerate diversification rates (a key innovation). To test the pattern of diversification of Halenia against the unspurred sister group we reconstructed phylogenetic relationships among 22 species plus outgroups using nuclear ITS and chloroplast rpl16 intron sequence data. We show that Halenia originated in East Asia and migrated via North America into Central America. From there, it colonized South America three times independently, probably within the last million years. Significant changes in diversification rates were found during the evolution of Halenia using a sister group method, a likelihood method, and a diversity-through-time plot. In contrast to other studies, we could not observe a direct speciation rate effect of the evolution of nectar spurs in comparison with the unspurred sister group of Halenia. Rather, increases in diversification occurred following the colonization of Central and South America by spurred progenitor taxa. This later switch in diversification may have resulted from the availability of new geographical and ecological opportunities, or from the availability of more and different pollinators in these regions. Following the latter hypothesis, the nectar spurs were a preadaption and functioned as a key innovation only in this new biotic environment. After an initial rapid increase, a reduction in diversification rate was observed in Central America, probably illustrating density dependence of speciation rates. Finally, we found preliminary evidence for the key innovation hypothesis in geologically young spurred and unspurred lineages of Halenia in South America.     

The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio

It has been suggested that the absence of floral rewards in many orchid species causes pollinators to probe fewer flowers on a plant, and thus reduces geitonogamy, i.e. self-pollination between flowers, which may result in inbreeding depression and reduced pollen export. We examined the effects of nectar addition on pollinator visitation and pollen transfer by tracking the fate of colour-labelled pollen in Anacamptis morio, a non-rewarding orchid species pollinated primarily by queen bumble-bees. Addition of nectar to spurs of A. morio significantly increased the number of flowers probed by bumble-bees, the time spent on an inflorescence, pollinarium removal and the proportion of removed pollen involved in self-pollination through geitonogamy, but did not affect pollen carryover (the fraction of a pollinarium carried over from one flower to the next). Only visits that exceeded 18 s resulted in geitonogamy, as this is the time taken for removed pollinaria to bend into a position to strike the stigma. A mutation for nectar production in A. morio would result in an initial 3.8-fold increase in pollinarium removal per visit, but also increase geitonogamous self-pollination from less than 10% of pollen depositions to ca. 40%. Greater efficiency of pollen export will favour deceptive plants when pollinators are relatively common and most pollinaria are removed from flowers or when inbreeding depression is severe. These findings provide empirical support both for Darwin's contention that pollinarium bending is an anti-selfing mechanism in orchids and for the idea that floral deception serves to maximize the efficiency of pollen export.     

Nectar robbing,forager efficiency and seed set: Bumblebees foraging on the self incompatible plant Linaria vulgaris (Scrophulariaceae)

In southern England, Linaria vulgaris (common yellow toadflax) suffers from high rates of nectar robbery by bumblebees. In a wild population of L. vulgaris we found that 96 % of open flowers were robbed. Five species of bumblebee were observed foraging on these flowers, although short-tongued species (Bombus lapidarius, B. lucorum and B. terrestris) robbed nectar whilst longer-tongued ones behaved as legitimate pollinators (B. hortorum and B. pascuorum). Nectar rewards were highly variable; on average there was less nectar in robbed than in unrobbed flowers, but this difference was not statistically significant. The proportion of flowers containing no nectar was significantly higher for robbed flowers compared with unrobbed flowers. Secondary robbers and legitimate pollinators had similar handling times on flowers and, assuming they select flowers at random to forage on, received approximately the same nectar profit per minute, largely because most flowers had been robbed. There was no significant difference in the number of seeds in pods of robbed flowers and in pods of flowers that were artificially protected against robbing. However, more of the robbed flowers set at least some seed than the unrobbed flowers, possibly as a consequence of the experimental manipulation. We suggest that nectar robbing has little effect on plant fecundity because legitimate foragers are present in the population, and that seed predation and seed abortion after fertilization may be more important factors in limiting seed production in this species.