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

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

A test of phenotypic selection on petal form in the wild carnation,Dianthus inoxianus

Floral phenotypes are considered a product of pollinator‐mediated selection, which also has the side effect of decreasing floral variation within species. Correlates of flower visibility and function were studied in a carnation species (Dianthus inoxianus), which has crepuscular anthesis and scent‐based pollination by the hawkmoth Hyles livornica. We also assessed constancy of flower form in nature and in cultivation and, using fruit set as an estimate of plant relative fitness, tested whether the main pollinator exerted phenotypic selection on floral traits. Petal claw, which is roughly equivalent to the average depth at which an insect's proboscis must be inserted to reach nectar, was remarkably constant among wild plants (coefficient of variation 8%). In contrast, the area of the visible part of the petal, and the intensity of a coloured dot pattern on the petal was very variable (respectively CV = 34% and 102%). Cultivation in a common environment revealed significant variation among genotypes as regards petal area, degree of laciniation and extension of the dot pattern, but not petal claw length, which remained steady. Petal area, shape and colour did not affect relative fitness during the year of study, but plants with intermediate petal claws (i.e. floral tubes) set significantly more fruit. Results are compatible with low response of the main pollinator to variation in visual traits (petal area, laciniation, colour) and high responsiveness to variation in other aspects (tube length). Inconsistent phenotypic selection by pollinators may add to other causes of floral variation in the genus Dianthus, the causes of which are discussed.     

Pollination syndromes in a specialised plant‐pollinator interaction: does floral morphology predict pollinators in Calceolaria?

Pollination syndromes are defined as suites of floral traits evolved in response to selection imposed by a particular group of pollinators (e.g., butterflies, hummingbirds, bats). Although numerous studies demonstrated their occurrence in plants pollinated by radically different pollinators, it is less known whether it is possible to identify them within species pollinated by one functional pollinator group. In such a framework, we expect floral traits to evolve also in response to pollinator subgroups (e.g., species, genera) within that unique functional group. On this, specialised pollination systems represent appropriate case studies to test such expectations. Calceolaria is a highly diversified plant genus pollinated by oil‐collecting bees in genera Centris and Chalepogenus. Variation in floral traits in Calceolaria has recently been suggested to reflect adaptations to pollinator types. However, to date no study has explicitly tested that observation. In this paper, we quantitatively test that hypothesis by evaluating the presence of pollination syndromes within the specialised pollination system formed by several Calceolaria and their insect pollinators. To do so, we use multivariate approaches and explore the structural matching between the morphology of 10 Calceolaria taxa and that of their principal pollinators. Our results identify morphological matching between floral traits related to access to the reward and insect traits involved in oil collection, confirming the presence of pollinator syndromes in Calceolaria. From a general perspective, our findings indicate that the pollination syndrome concept can be also extended to the intra‐pollinator group level.     

Contrasting pollination ecology of Disepalum species (Annonaceae): evolutionary loss of the floral chamber and partial breakdown of protogyny associated with a shift in pollination system

Disepalum comprises two monophyletic sister subgenera, Enicosanthellum and Disepalum, with strikingly different floral morphologies: the former has two whorls of unfused sepals, forming a partially enclosed floral chamber, whereas the latter possesses a single whorl of congenitally fused petals and lacks a floral chamber. The pollination ecologies of representative species are reported, including assessments of floral phenology, pollinators and floral thermogenesis. Disepalum pulchrum (subgenus Enicosanthellum) has hermaphroditic flowers with a pollination chamber and is protogynous with prolonged anthesis; it is pollinated by nitidulid beetles and drosophilid flies. Disepalum anomalum (subgenus Disepalum) is also hermaphroditic with prolonged anthesis, but has incomplete protogyny due to overlapping pistillate and staminate phases; it is pollinated by meliponine bees, which are attracted by the pollen, but which are only able to transfer pollen to receptive stigmas during the overlap phase. Alternative evolutionary hypotheses are evaluated, including the possibility that the ancestor of the subgenus Disepalum lineage may have experienced a profound genetic mutation, possibly involving genes responsible for organ merism and fusion, resulting in the loss of the pollination chamber and hence favouring different floral visitors. The breakdown in protogyny required for effective pollination is likely to have had significant ramifications on population genetic diversity.     

Divergence on floral traits and vertebrate pollinators of two endemic Encholirium bromeliads

Shifts in pollen vectors favour diversification of floral traits, and differences in pollination strategies between congeneric sympatric species can contribute to reproductive isolation. Divergence in flowering phenology and selfing could also reduce interspecific crossing between self‐compatible species. We investigated floral traits and visitation rates of pollinators of two sympatric Encholirium species on rocky outcrops to evaluate whether prior knowledge of floral characters could indicate actual pollinators. Data on flowering phenology, visitation rates and breeding system were used to evaluate reproductive isolation. Flowering phenology overlapped between species, but there were differences in floral characters, nectar volume and concentration. Several hummingbird species visited flowers of both Encholirium spp., but the endemic bat Lonchophylla bokermanni and an unidentified sphingid only visited E. vogelii. Pollination treatments demonstrated that E. heloisae and E. vogelii were partially self‐compatible, with weak pollen limitation to seed set. Herbivores feeding on inflorescences decreased reproductive output of both species, but for E. vogelii the damage was higher. Our results indicate that actual pollinators can be known beforehand through floral traits, in agreement with pollination syndromes stating that a set of floral traits can be associated with the attraction of specific groups of pollinators. Divergence on floral traits and pollinator assemblage indicate that shifts in pollination strategies contribute to reproductive isolation between these Encholirium species, not divergence on flowering phenology or selfing. We suggest that hummingbird pollination might be the ancestral condition in Encholirium and that evolution of bat pollination made a substantial contribution to the diversification of this clade.     

Reproductive biology of Syagrus coronata (Arecaceae): sex‐biased insect visitation and the unusual case of scent emission by peduncular bracts

• Several monoecious species of palms have developed complex strategies to promote cross‐pollination, including the production of large quantities of floral resources and the emission of scents that are attractive to pollinators. Syagrus coronata constitutes an interesting model with which to understand the evolution of plant reproductive strategies in a monoecious species adapted to seasonally dry forests.
• We monitored blooming phenology over 1 year, during which we also collected and identified floral visitors and putative pollinators. We identified potential floral visitor attractants by characterizing the scent composition of inflorescences as well as of peduncular bracts, during both male and female phases, and the potential for floral thermogenesis.
• Syagrus coronata produces floral resources throughout the year. Its inflorescences are predominantly visited by a diverse assortment of small‐sized beetles, whose richness and abundance vary throughout the different phases of anthesis. We did not find evidence of floral thermogenesis. A total of 23 volatile compounds were identified in the scent emitted by the inflorescences, which did not differ between male and female phases; whereas the scent of the peduncular bracts was composed of only 4‐methyl guaiacol, which was absent in inflorescences.
• The composition of floral scent chemistry indicates that this palm has evolved strategies to be predominantly pollinated by small‐sized weevils. Our study provides rare evidence of a non‐floral scent emitting structure involved in pollinator attraction, only the second such case specifically in palms. The peculiarities of the reproductive strategy of S. coronata might play an important role in the maintenance of pollination services and pollen dispersion.

     

The evolution of key functional floral traits in the early divergent angiosperm family Annonaceae

Potential key functional floral traits are assessed in the species‐rich early divergent angiosperm family Annonaceae. Pollinators (generally beetles) are attracted by various cues (particularly visual, olfactory, and thermogenic), with pollinators rewarded by nectar (generally as stigmatic exudate), heat, and protection within the partially enclosed floral chamber. Petals sometimes function as pollinator brood sites, although this could be deceptive. Annonaceae species are self‐compatible, with outcrossing promoted by a combination of protogyny, herkogamy, floral synchrony, and dicliny. Pollination efficiency is enhanced by pollen aggregation, changes in anthesis duration, and pollinator trapping involving a close alignment between petal movements and the circadian rhythms of pollinators. Most Annonaceae flowers are apocarpous, with syncarpy restricted to very few lineages; fertilization is therefore optimized by intercarpellary growth of pollen tubes, either by stigmatic exudate (suprastylar extragynoecial compitum) or possibly the floral receptacle (infrastylar extragynoecial compitum). Although Annonaceae lack a distinct style, the stigmas in several lineages are elongated to form “pseudostyles” that are hypothesized to function as sites for pollen competition. Flowers can be regarded as immature fruits in which the ovules are yet to be fertilized, with floral traits that may have little selective advantage during anthesis theoretically promoting fruit and seed dispersal. The plesiomorphic apocarpous trait may have been perpetuated in Annonaceae flowers as it promotes the independent dispersal of fruit monocarps (derived from separate carpels), thereby maximizing the spatial/temporal distance between seedlings. This might compensate for the lack of genetic diversity among seeds within fruits arising from the limited diversity of pollen donors.     

Crane flies and microlepidoptera also function as pollinators in Epidendrum (Orchidaceae: Laeliinae): the reproductive biology of E. avicula

Crane flies and microlepidoptera have been recorded as pollinators in unrelated orchid groups, but these insects have never been recorded in Epidendroideae, the most species‐rich orchid subfamily, which includes one of the most diverse genera among Orchidaceae, Epidendrum. Based on data on phenology, floral morpho‐anatomy, pollinators, pollination mechanisms and breeding system, the reproductive biology of E. avicula was studied in south‐eastern Brazil. Epidendrum avicula possess osmophores that produce a citric fragrance at night. The flowers attract Tipulidae flies and several families of microlepidoptera that drink the nectar produced in a tube formed by the adnation of the labellum and column. As is common in Epidendrum, after removing the pollinarium, both crane flies and micro‐moths get trapped by the proboscis, which frightens the insects and inhibits any possible intent to immediately visit another flower. The behavior of the pollinators on flowers, plus the retention of the anther cap by the pollinarium, results in a reduction in the occurrence of geitonogamy. Because E. avicula is self‐incompatible, the consequence of pollinator behavior and the floral mechanisms tend to reduce the pollen loss. As far as we know, this is the first study to report the reproductive biology of a species of Epidendroideae pollinated by crane flies and microlepidoptera. Based on more recent concepts of plant–pollinator interactions, although E. avicula is pollinated by several species belonging to two distinct orders, suggesting an unspecialized pollination system is involved, nectar‐seeking microlepidoptera and Tipulidae flies can be recognized as a single functional group.     

Temporal and sexual variation of leaf-produced pollinator-attracting odours in the dwarf palm

Information on intra-specific variation in pollinator-attracting floral traits provides clues to selective pressures imposed by pollinators. However, these traits also reflect constraints related to floral phenology or morphology. The specific weevil pollinator Derelomus chamaeropsis of the dioecious Mediterranean dwarf palm Chamaerops humilis is attracted by volatile compounds that leaves, and not flowers, release during anthesis. Production of these olfactory cues is thus probably not constrained by any other floral function. This provides the opportunity to study variation of a floral trait that is not produced by a floral organ. We studied volatile compounds emitted by leaves of 12 individual C. humilis over the whole flowering season. The quantity of volatile compounds emitted by leaves reached a maximum when plants required pollinator visits. The relationship between odour emission and floral phenology was slightly different between male and female plants, probably reflecting differences in the exact time at which females and males benefit from pollinator visitation. Male plants produced higher quantities of volatile compounds than females. Odour composition was highly variable among individuals but did not differ between male and female plants. In this system, female C. humilis are pollinated by deceit and pollinators should be selected to avoid visiting them. The absence of sexual difference in blend composition may thus prevent pollinators from discriminating between male and female plants.An erratum to this article can be found at     

Bees explain floral variation in a recent radiation of Linaria

The role of pollinators in floral divergence has long attracted the attention of evolutionary biologists. Although abundant studies have reported the effect of pollinators on flower‐shape variation and plant speciation, the influence of pollinators on plant species differentiation during rapid radiations and the specific consequences of shifts among similar pollinators are not well understood. Here, we evaluate the association between pollinators and floral morphology in a closely related and recently diversifying clade of Linaria species (sect. Supinae subsect. Supinae). Our approach combined pollinator observations, functional floral morphometric measures and phylogenetic comparative analyses. The fauna visiting Linaria species was determined by extensive surveys and categorized by a modularity algorithm, and the size and shape of flowers were analysed by means of standard and geometric morphometric measures. Standard measures failed to find relationships between the sizes of representative pollinators and flowers. However, discriminant function analyses of geometric morphometric data revealed that pollination niches are finer predictors of flower morphologies in Linaria if compared with phylogenetic relationships. Species with the most restrictive flowers displayed the most slender spurs and were pollinated by bees with larger proboscides. These restrictive flower shapes likely appeared more than once during the evolutionary history of the study group. We show that floral variation can be driven by shifts between pollinators that have been traditionally included in a single functional group, and discuss the consequences of such transitions for plant species differentiation during rapid radiations.     

Are pollinators the agents of selection on flower colour and size in irises?

Plant–pollinator interactions are believed to play a major role in the evolution of floral traits. Flower colour and flower size are important for attracting pollinators, directly influencing reproduction, and thus expected to be under pollinator‐mediated selection. Pollinator‐mediated selection is also proposed to play a role in maintaining flower colour polymorphism within populations. However, pigment concentrations, and thus flower colour, are also under selective pressures independent of pollinators. We quantified phenotypic pollinator‐mediated selection on flower colour and size in two colour polymorphic Iris species. Using female fitness, we estimated phenotypic selection on flower colour and size, and tested for pollinator‐mediated selection by comparing selection gradients between flowers open to natural pollination and supplementary pollinated flowers. In both species, we found evidence for pollen limitation, which set the base for pollinator‐mediated selection. In the colour dimorphic Iris lutescens, while pigment concentration and flower size were found to be under selection, this was independent of pollinators. For the polymorphic Iris pumila, pigment concentration is under selective pressure by pollinators, but only for one colour morph. Our results suggest that pollinators are not the main agents of selection on floral traits in these irises, as opposed to the accepted paradigm on floral evolution. This study provides an opposing example to the largely‐accepted theory that pollinators are the major agent of selection on floral traits.     

Matching floral and pollinator traits through guild convergence and pollinator ecotype formation

Background and Aims

Pollinator landscapes, as determined by pollinator morphology/behaviour, can vary inter- or intraspecifically, imposing divergent selective pressures and leading to geographically divergent floral ecotypes. Assemblages of plants pollinated by the same pollinator (pollinator guilds) should exhibit convergence of floral traits because they are exposed to similar selective pressures. Both convergence and the formation of pollination ecotypes should lead to matching of traits among plants and their pollinators.

Methods

We examined 17 floral guild members pollinated in all or part of their range by Prosoeca longipennis, a long-proboscid fly with geographic variation in tongue length. Attractive floral traits such as colour, and nectar properties were recorded in populations across the range of each species. The length of floral reproductive parts, a mechanical fit trait, was recorded in each population to assess possible correlation with the mouthparts of the local pollinator. A multiple regression analysis was used to determine whether pollinators or abiotic factors provided the best explanation for variation in floral traits, and pollinator shifts were recorded in extralimital guild member populations.

Key Results

Nine of the 17 species were visited by alternative pollinator species in other parts of their ranges, and these displayed differences in mechanical fit and attractive traits, suggesting putative pollination ecotypes. Plants pollinated by P. longipennis were similar in colour throughout the pollinator range. Tube length of floral guild members co-varied with the proboscis length of P. longipennis.

Conclusions

Pollinator shifts have resulted in geographically divergent pollinator ecotypes across the ranges of several guild members. However, within sites, unrelated plants pollinated by P. longipennis are similar in the length of their floral parts, most probably as a result of convergent evolution in response to pollinator morphology. Both of these lines of evidence suggest that pollinators play an important role in selecting for certain floral traits.     

Evolutionary relationships among pollinators and repeated pollinator sharing in sexually deceptive orchids

The mechanism of pollinator attraction is predicted to strongly influence both plant diversification and the extent of pollinator sharing between species. Sexually deceptive orchids rely on mimicry of species‐specific sex pheromones to attract their insect pollinators. Given that sex pheromones tend to be conserved among related species, we predicted that in sexually deceptive orchids, (i) pollinator sharing is rare, (ii) closely related orchids use closely related pollinators and (iii) there is strong bias in the wasp lineages exploited by orchids. We focused on species that are pollinated by sexual deception of thynnine wasps in the distantly related genera Caladenia and Drakaea, including new field observations for 45 species of Caladenia. Specialization was extreme with most orchids using a single pollinator species. Unexpectedly, seven cases of pollinator sharing were found, including two between Caladenia and Drakaea, which exhibit strikingly different floral morphology. Phylogenetic analysis of pollinators using four nuclear sequence loci demonstrated that although orchids within major clades primarily use closely related pollinator species, up to 17% of orchids within these clades are pollinated by a member of a phylogenetically distant wasp genus. Further, compared to the total diversity of thynnine wasps within the study region, orchids show a strong bias towards exploiting certain genera. Although these patterns may arise through conservatism in the chemical classes used in sex pheromones, apparent switches between wasp clades suggest unexpected flexibility in floral semiochemical production. Alternatively, wasp sex pheromones within lineages may exhibit greater chemical diversity than currently appreciated.     

Intraspecific divergence and convergence of floral tube length in specialized pollination interactions

Floral tubes are often thought to be a consequence of adaptive specialization towards pollinator morphology. We explore floral tube length evolution within Tritoniopsis revoluta (Iridaceae), a species with considerable geographical tube length variation. We ask whether tube lengths of T. revoluta populations are associated with pollinator proboscis lengths, whether floral divergence occurs in the presence of different pollinators and whether floral convergence occurs between distantly related populations pollinated by the same pollinator. Finally, we ask whether tube length evolution is directional. Shifts between morphologically different pollinators were always associated with shifts in floral morphology, even when populations were very closely related. Distantly related populations had similar tube lengths when they were pollinated by the same pollinator. Shifts in tube length tended to be from short to long, although reversals were not infrequent. After correcting for the population-level phylogeny, there was a strong positive, linear relationship between floral tube length and pollinator proboscis length, suggesting that plants are functionally specialized on different pollinators at different sites. However, because tube length evolution in this system can be a bidirectional process, specialization to the local pollinator fauna is unlikely to result in evolutionary or ecological dead-ends such as canalization or range limitation.     

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

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

Pollination of New CaledonianWinteraceae: Opportunistic shifts or parallel radiation with their pollinators?

Flower visitors on 12 species of New CaledonianWinteraceae were studied. The visitors were two species of ancestral moths (Sabatinca; Micropterigidae), three species of weevils (Palontus; Curculionidae), and a species of thrips. Behavior observations and pollen records suggest that the beetles and occasionally the moths serve as pollinators ofZygogynum and Exospermum, andBelliolum is pollinated primarily by thrips. The floral volatiles are simple in composition, usually dominated by short esters. Preliminary experiments showed that ethyl acetate elicited alighting, and a distinctive huddling behavior was elicited by artificially mixed fragrance. The host associations of otherSabatinca andPalontus spp. do not support the hypothesis that theWinteraceae have radiated in association with their pollinators. The available evidence supports the notion of opportunistic isolated host colonizations at some point in the radiation of the pollinator groups.     

Florivory indirectly decreases the plant reproductive output through changes in pollinator attraction

Species often interact indirectly with each other via their traits. There is increasing appreciation of trait‐mediated indirect effects linking multiple interactions. Flowers interact with both pollinators and floral herbivores, and the flower‐pollinator interaction may be modified by indirect effects of floral herbivores (i.e., florivores) on flower traits such as flower size attracting pollinators. To explore whether flower size affects the flower‐pollinator interaction, we used Eurya japonica flowers. We examined whether artificial florivory decreased fruit and seed production, and also whether flower size affected florivory and the number of floral visitors. The petal removal treatment (i.e., artificial florivory) showed approximately 50% reduction in both fruit and seed set in natural pollination but not in artificial pollination. Furthermore, flower size increased the number of floral visitors, although it did not affect the frequency of florivory. Our results demonstrate that petal removal indirectly decreased 75% of female reproductive output via decreased flower visits by pollinators and that flower size mediated indirect interactions between florivory and floral visitors.     

Equal and Opposite Effects of Floral Offer and Spatial Distribution on Fruit Production and Predispersal Seed Predation in Xanthosoma daguense (Araceae)1

Inflorescences of the terrestrial aroid Xanthosoma daguense in the Andes of Colombia are visited by Dinastinae and Nitidulidae beetles. Plants produce one inflorescence at a time, which is pollinated during the first night of opening. Dynastine beetles act as pollinators, whereas Nitidulids lay eggs in the inflorescence and the larvae damage the seeds. We explored the effects of floral offer and distance among inflorescences on the number of pollinator visits, fruit production, and predispersal seed predation. Number of Dynastine visits per inflorescence tended to increase with increasing distances among inflorescences, but fruit predation increased when inflorescences were more clumped. Both pollinator visitation rates and predispersal seed predation were low at high floral offer. Fruit set increased when inflorescences were visited by two or more Dynastines, but the proportion of fruits damaged by Nitidulid larvae was equivalent to the increase in fruit production due to more Dinastine visits. The net result was a similar number of undamaged fruits in all infructescences produced, independent of the number of Dinastine visits. Our results revealed that both pollinators and predators responded to the number of available inflorescences and their spatial distribution, but they had opposing effects on the infructescences. Thus, our study suggests that the interaction of two ecological processes, pollination and predispersal seed predation, may cancel each other's effects under natural conditions.     

Looks matter: changes in flower form affect pollination effectiveness in a sexually deceptive orchid

Many species of the sexually deceptive genus Ophrys are characterized by insect‐like flowers. Their form has been traditionally considered to play an important role in pollinator attraction and manipulation. Yet, the evolution of the floral form remains insufficiently understood. We hypothesize that pollinator‐mediated selection is essential for driving floral form evolution in Ophrys, but that form components are being subjected to varying selection pressures depending on their role in mediating interactions with pollinators. By using the Eucera‐pollinated Ophrys leochroma as a model, our aim has been to assess whether and in what manner pollination effectiveness is altered by experimental manipulation of the flower form. Our results show that floral form plays an essential and, so far, underestimated role in ensuring effective pollination by mechanically guiding pollinators towards the reproductive structures of the flower. Pollinators are significantly less effective in interacting with flowers having forms altered to resemble those of species pollinated by different hymenopteran genera. Further, those components used by pollinators as gripping points were found to be more effective in ensuring pollinia transfer than those with which pollinators do not directly interact. Thus, mechanically active and inactive components appear to be under different selection pressures. As a consequence, mechanically active components of the flower form could reflect adaptations to the interaction with particular pollinator groups, whereas mechanically inactive components can vary more freely. Disentangling selection patterns between the functionally different components of flower form may provide valuable insights into the mechanisms driving the morphological diversification of sexually deceptive pollination systems.