The role of pollinators in floral diversification in a clade of generalist flowers

Pollinator‐mediated evolutionary divergence has seldom been explored in generalist clades because it is assumed that pollinators in those clades exert weak and conflicting selection. We investigate whether pollinators shape floral diversification in a pollination generalist plant genus, Erysimum. Species from this genus have flowers that appeal to broad assemblages of pollinators. Nevertheless, we recently reported that it is possible to sort plant species into pollination niches varying in the quantitative composition of pollinators. We test here whether floral characters of Erysimum have evolved as a consequence of shifts among pollination niches. For this, we quantified the evolutionary lability of the floral traits and their phylogenetic association with pollination niches. As with pollination niches, Erysimum floral traits show weak phylogenetic signal. Moreover, floral shape and color are phylogenetically associated with pollination niche. In particular, plants belonging to a pollination niche dominated by long‐tongued large bees have lilac corollas with parallel petals. Further analyses suggest, however, that changes in color preceded changes in pollination niche. Pollinators seem to have driven the evolution of corolla shape, whereas the association between pollination niche and corolla color has probably arisen by lilac‐flowered Erysimum moving toward certain pollination niches for other adaptive reasons.     

SELECTION ON POLEMONIUM BRANDEGEEI (POLEMONIACEAE) FLOWERS UNDER HUMMINGBIRD POLLINATION: IN OPPOSITION,PARALLEL, OR INDEPENDENT OF SELECTION BY HAWKMOTHS?

Particular floral phenotypes are often associated with specific groups of pollinators. However, flowering plants are often visited, and may be effectively pollinated by more than one type of animal. Therefore, a major outstanding question in floral biology asks: what is the nature of selection on floral traits when pollinators are diverse? This study examined how hummingbirds selected on the floral traits of Polemonium brandegeei, a species pollinated by both hummingbirds and hawkmoths. In array populations of P. brandegeei, we measured pollen movement, and female (seeds set) and male (seeds sired) fitness under hummingbird pollination. We then compared the patterns of selection by hummingbirds with our previous study examining selection by hawkmoths. We documented contrasting selection on sex organ positioning through female function, with hummingbirds selecting for stigmas exserted beyond the anthers and hawkmoths selecting for stigmas recessed below the anthers. Furthermore, hummingbirds selected for longer and wider corolla tubes, and hawkmoths selected for narrower corolla tubes. Therefore, contrasting selection by hawkmoths and hummingbirds may account for variation in sex organ arrangements and corolla dimensions in P. brandegeei. We documented how floral traits under selection by multiple pollinators can result in either an intermediate “compromise” between selective pressures (sex organs) or apparent specialization (corolla tube length) to one pollinator.     

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.     

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.     

马先蒿属花冠形态的多样性与传粉式样的关系

马先蒿属(Pediculais)是有花植物中花冠形态多样化最为集中的属。该属主要的传粉者是熊蜂属(Bormbus)昆虫;在北美,熊蜂和蜂鸟是马先蒿植物一些种类有效的传粉者;也发现壁蜂(Osmia)为其传粉。不同的传粉机制要求某一特定的取食式样储藏和释放花粉。本文讨论了花冠类型的进化趋势与传粉式样和花粉形态的关系。传粉者的选择压力是决定花冠多样化的重要因素之一;花冠类型与传粉者和传粉行为紧密相关。马先蒿植物和传粉者的相互依赖与其花冠类型、功能和物候互相适应,但花冠类型与花粉形态两者之间似乎没有明显的一一对应关系。通过北美、日本和喜马拉雅不同地理分布马先蒿种类的比较研究表明,具有相同花冠类型的种类有着相同的传粉方式,花冠形态与传粉式样存在紧密的协同进化关系。     

Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators

An adaptive role of corolla shape has been often asserted without an empirical demonstration of how natural selection acts on this trait. In generalist plants, in which flowers are visited by diverse pollinator fauna that commonly vary spatially, detecting pollinator-mediated selection on corolla shape is even more difficult. In this study, we explore the mechanisms promoting selection on corolla shape in the generalist crucifer Erysimum mediohispanicum Polatschek (Brassicaceae). We found that the main pollinators of E. mediohispanicum (large bees, small bees and bee flies) discriminate between different corolla shapes when offered artificial flowers without reward. Importantly, different pollinators prefer different shapes: bees prefer flowers with narrow petals, whereas bee flies prefer flowers with rounded overlapping petals. We also found that flowers with narrow petals (those preferred by bees) produce both more pollen and nectar than those with rounded petals. Finally, different plant populations were visited by different faunas. As a result, we found spatial variation in the selection acting on corolla shape. Selection favoured flowers with narrow petals in the populations where large or small bees are the most abundant pollinator groups. Our study suggests that pollinators, by preferring flowers with high reward, exert strong selection on the E. mediohispanicum corolla shape. The geographical variation in the pollinator-mediated selection on E. mediohispanicum corolla shape suggests that phenotypic evolution and diversification can occur in this complex floral trait even without specialization.     

Convergence of anti-bee pollination mechanisms in the Neotropical plant genus <Emphasis Type="Italic">Drymonia</Emphasis> (Gesneriaceae)

The neotropical plant genus Drymonia displays a remarkable variety of floral shapes and colors. One feature that is particularly important to coevolution with pollinators involves the variable shapes and widths of corolla tubes. To evaluate the evolutionary context for changes in corolla shape, we constructed a phylogeny of 50 of the 75 species of Drymonia using molecular markers from plastid (trnK-matK) and nuclear regions (ITS and ETS). Mapping tube shapes on the phylogeny supports open, bell-shaped (campanulate) corolla shape as the ancestral character state for Drymonia, with multiple independent origins of constriction in the corolla tube. Corollas with constrictions take one of three tube shapes: a constricted flower opening and throat with a large, expanded pouch on the lower surface (hypocyrtoid); a constricted flower opening and throat lacking an expanded pouch on the lower surface (urceolate); or a constricted opening and throat where the sides of the corolla appear laterally compressed. Fieldwork demonstrates euglossine bees (mostly Euglossa spp. and Epicharis spp.) visit campanulate corollas while hummingbirds visit corollas that are constricted. Results support eight independent origins of constricted corolla tubes from ancestors with campanulate corolla tubes: 3 hypocyrtoid clades, 3 laterally compressed clades, and 3 urceolate clades (one of which represents a shift from a hypocyrtoid ancestor). Constricted corollas are associated with shifts from the ancestral condition of poricidal anther dehiscence, which presents pollen to pollinators in multiple small doses, to the derived condition of longitudinal anther dehiscence, which presents all pollen to pollinators simultaneously. The association of hummingbird pollination with constricted corolla tubes suggests that narrowing evolved as a barrier mechanism that prohibits the visitation of flowers by bees.     

Anther evolution: pollen presentation strategies when pollinators differ

Male-male competition in plants is thought to exert selection on flower morphology and on the temporal presentation of pollen. Theory suggests that a plant's pollen dosing strategy should evolve to match the abundance and pollen transfer efficiency of its pollinators. Simultaneous pollen presentation should be favored when pollinators are infrequent or efficient at delivering the pollen they remove, whereas gradual dosing should optimize delivery by frequent and wasteful pollinators. Among Penstemon and Keckiella species, anthers vary in ways that affect pollen release, and the morphology of dried anthers reliably indicates how they dispense pollen. In these genera, hummingbird pollination has evolved repeatedly from hymenopteran pollination. Pollen production does not change with evolutionary shifts between pollinators. We show that after we control for phylogeny, hymenopteran-adapted species present their pollen more gradually than hummingbird-adapted relatives. In a species pair that seemed to defy the pattern, the rhythm of anther maturation produced an equivalent dosing effect. These results accord with previous findings that hummingbirds can be more efficient than bees at delivering pollen.     

Plant–hummingbird interactions in the West Indies: floral specialisation gradients associated with environment and hummingbird size

Floral phenotype and pollination system of a plant may be influenced by the abiotic environment and the local pollinator assemblage. This was investigated in seven plant–hummingbird assemblages on the West Indian islands of Grenada, Dominica and Puerto Rico. We report all hummingbird and insect pollinators of 49 hummingbird-pollinated plant species, as well as six quantitative and semi-quantitative floral characters that determine visitor restriction, attraction and reward. Using nonmetric multidimensional scaling analysis, we show that hummingbird-pollinated plants in the West Indies separate in floral phenotypic space into two gradients—one associated with the abiotic environment and another with hummingbird size. Plants pollinated by large, long-billed hummingbirds had flowers with long corolla tube, large amounts of nectar and showy orange-red colouration. These attracted few or no insect species, whereas plants pollinated by small, short-billed hummingbirds were frequently pollinated by insects, particularly lepidopterans. The separation of plants related to environmental factors showed that species in the wet and cold highlands produced large amounts of dilute nectar, possessed no or a weak odour, and were associated with few insects, particularly few hymenopterans, compared to plants in the dry and warm lowlands. The most specialised hummingbird-pollinated plants are found in the West Indian highlands where they are pollinated by mainly large, long-billed hummingbirds. At the other extreme, highly generalised plants growing in the dry and warm lowlands are pollinated by small, short-billed hummingbirds and numerous insect species. This illustrates that, even within the hummingbird-pollinated flora, pollination syndrome and the degree of specialisation may vary tremendously depending on pollinator morphology and environment. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

RATES OF FLORAL EVOLUTION: ADAPTATION TO BUMBLEBEE POLLINATION IN AN ALPINE WILDFLOWER,POLEMONIUM VISCOSUM

Animal pollinators are thought to shape floral evolution, yet the tempo of this process has seldom been measured. I used the prediction equation of quantitative genetics, R = h²S , to predict the rate at which a change in pollinator abundance may have caused divergence in floral morphology of the alpine skypilot, Polemonium viscosum. A selection experiment determined the rate at which such divergence can actually proceed. Corolla flare in this species increases by 12% from populations pollinated by a wide assemblage of insect visitors to those pollinated only by bumblebees. To simulate the evolutionary process giving rise to this change, I used a pollinator selection experiment. Plants with broad flowers set significantly more seeds than plants with narrow flowers under bumblebee pollination but had equivalent fecundity when visited by other insects or hand-pollinated. Bumblebee-mediated selection for broad corolla flare intensified from 0.07 at seed set to 0.17 at progeny establishment. Maternal parent-offspring regression yielded a confidence interval of 0.22–1.00 for trait heritability. Given these parameter estimates, the prediction equation shows that broadly flared flowers of bumblebee-pollinated P. viscosum could have evolved from narrower ones in a single generation. This prediction is matched by an observed 9% increase in offspring corolla flare after a single bout of bumblebee-mediated selection, relative to offspring of unselected controls. Findings show that plant populations can adapt rapidly to abrupt changes in pollinator assemblages.     

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

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

Pollination and phenology of flowers in the canopy of two contrasting rain forest types in Amazonia,Colombia

The main objective of this investigation was to study the pollination characteristics of two types of Amazonian rain forest at plant community level. Seasonally inundated forest was compared with upland (tierra firme) forest. The study focused on plant species in the canopy. The pollination spectra show that in both forests most canopy trees and lianas are pollinated by small bees, large bees, butterflies or by small, relatively unspecialized insects. In the upland forest small bees are the most important pollinators (32% of all species of trees and lianas are pollinated by them), whereas large bees are predominant in the floodplain (22%). Other pollinators, like hummingbirds, bats, moths, and beetles are less common (>10%), but always somewhat more important in the flood plain than in the upland forest. Bees are the most common pollinators of epiphytes. In the flood plain forest, flies are also important as epiphyte pollinators (19%), whereas in the upland forest hummingbirds pollinate more epiphytes. The phenological patterns are quite similar in both the upland and the flood plain. We found a peak in flowering in the transition period between the wet and the dry season. Flowering activity was lowest during the wet season. Differentiation in sexual systems was correlated with life form. Dioecy and monoecy were found mostly among tree species. Most species of all life forms though were hermaphroditic. No difference with respect to the relative importance of sexual systems was found between the two forest types.     

Reproductive biology of a hummingbird‐pollinated Billbergia: light influence on pollinator behaviour and specificity in a Brazilian semi‐deciduous forest

• Ornithophily has evolved in parallel several times during evolution of angiosperms. Bird pollination is reported for 65 families, including Bromeliaceae. One of the most diverse bromeliad is Billbergia, which comprises species pollinated mainly by hummingbirds.
• Based on investigations on flowering phenology, morpho‐anatomy, volume and concentration of nectar, pollinators and breeding system, this paper explores the reproductive biology and pollinator specificity of B. distachia in a mesophytic semi‐deciduous forest of southeastern Brazil.
• The results have show that B. distachia is pollinated by a single species of hermit hummingbird, Phaethornis eurynome, which search for nectar produced by a septal nectary, where the secretory tissue is located above the placenta. The species is self‐incompatible. The combination of pollinator specificity, due to long corolla tubes that exclude visitation of short‐billed hummingbirds, complete self‐incompatibility and non‐territorial behaviour of pollinators, it is very important to reduce pollen loss and increase gene flow within population.
• Our results indicate that studies on pollination biology and reproduction are essential to understand the evolutionary history of pollination systems of plants since, at least in Billbergia, variation in the pollinator spectrum has been recorded for different habitats among Brazilian forests. Furthermore, according to our data, foraging of Phaethornis on flowers is independent of air temperature and humidity, while the main factor influencing hummingbird visitation is daylight. Considering current knowledge on climatic parameters influencing hummingbird foraging, pollination and reproductive biology of Neotropical flora and environment of the hermit hummingbird in tropical forests, new insights on plant–pollinator interaction are provided.

     

Pollinator shifts,contingent evolution,and evolutionary constraint drive floral disparity in Salvia (Lamiaceae): Evidence from morphometrics and phylogenetic comparative methods

Switches in pollinators have been argued to be key drivers of floral evolution in angiosperms. However, few studies have tested the relationship between floral shape evolution and switches in pollination in large clades. In concert with a dated phylogeny, we present a morphometric analysis of corolla, anther connective, and style shape across 44% of nearly 1000 species of Salvia (Lamiaceae) and test four hypotheses of floral evolution. We demonstrate that floral morphospace of New World (NW) Salvia is largely distinct from that of Old World (OW) Salvia and that these differences are pollinator driven; shifts in floral morphology sometimes mirror shifts in pollinators; anther connectives (key constituents of the Salvia staminal lever) and styles co-evolved from curved to linear shapes following shifts from bee to bird pollination; and morphological differences between NW and OW bee flowers are partly the legacy of constraints imposed by an earlier shift to bird pollination in the NW. The distinctive staminal lever in Salvia is a morphologically diverse structure that has evolved in concert with both the corolla and style, under different pollinator pressures, and in contingent fashion.     

The evolution of bat pollination: a phylogenetic perspective

Background

Most tropical and subtropical plants are biotically pollinated, and insects are the major pollinators. A small but ecologically and economically important group of plants classified in 28 orders, 67 families and about 528 species of angiosperms are pollinated by nectar-feeding bats. From a phylogenetic perspective this is a derived pollination mode involving a relatively large and energetically expensive pollinator. Here its ecological and evolutionary consequences are explored.

Scope and Conclusions

This review summarizes adaptations in bats and plants that facilitate this interaction and discusses the evolution of bat pollination from a plant phylogenetic perspective. Two families of bats contain specialized flower visitors, one in the Old World and one in the New World. Adaptation to pollination by bats has evolved independently many times from a variety of ancestral conditions, including insect-, bird- and non-volant mammal-pollination. Bat pollination predominates in very few families but is relatively common in certain angiosperm subfamilies and tribes. We propose that flower-visiting bats provide two important benefits to plants: they deposit large amounts of pollen and a variety of pollen genotypes on plant stigmas and, compared with many other pollinators, they are long-distance pollen dispersers. Bat pollination tends to occur in plants that occur in low densities and in lineages producing large flowers. In highly fragmented tropical habitats, nectar bats play an important role in maintaining the genetic continuity of plant populations and thus have considerable conservation value.     

Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae)

Inga species present brush‐type flower morphology allowing them to be visited by distinct groups of pollinators. Nectar features in relation to the main pollinators have seldom been studied in this genus. To test the hypothesis of floral adaptation to both diurnal and nocturnal pollinators, we studied the pollination ecology of Inga sessilis, with emphasis on the nectar secretion patterns, effects of sequential removals on nectar production, sugar composition and the role of diurnal and nocturnal pollinators in its reproductive success. Inga sessilis is self‐incompatible and pollinated by hummingbirds, hawkmoths and bats. Fruit set under natural conditions is very low despite the fact that most stigmas receive polyads with sufficient pollen to fertilise all ovules in a flower. Nectar secretion starts in the bud stage and flowers continually secreting nectar for a period of 8 h. Flowers actively reabsorbed the nectar a few hours before senescence. Sugar production increased after nectar removal, especially when flowers were drained during the night. Nectar sugar composition changed over flower life span, from sucrose‐dominant (just after flower opening, when hummingbirds were the main visitors) to hexose‐rich (throughout the night, when bats and hawkmoths were the main visitors). Diurnal pollinators contributed less than nocturnal ones to fruit production, but the former were more constant and reliable visitors through time. Our results indicate I. sessilis has floral adaptations, beyond the morphology, that encompass both diurnal and nocturnal pollinator requirements, suggesting a complementary and mixed pollination system.     

The role of nectar production, flower pigments and odour in the pollination of four species of Passiflora (Passifloraceae) in south-eastern Brazil

The pollination biology of four species of passionflower was studied in south-eastern Brazil, specifically the importance of chemical features of floral nectar, pigments and odours. All species required pollinators to produce fruits: P. alata was pollinated by bees, P. speciosa by hummingbirds, and P. galbana and P. mucronata by bats. Pollinators consumed nectar as a food source. The activity of vertebrate pollinators reflected resource availability: they foraged when large amounts of nectar were available and when quantitative resource predictability was greater. The nectar of the vertebrate-pollinated species was richer in cholesterol and phospholipids, and had a potassium-sodium ratio higher than 1.0. For all species, the light absorption of flowers was paralleled by the pollinators' visual spectral sensitivity. This first report on Passiflora floral volatile compounds showed that there was a greater chemical class diversity among the species pollinated by animals with an acute olfactory sense, such as bees and bats. Benzenoid alcohols were the most represented compounds. The fragrances contained compounds that occur in other plant species and in the exocrine secretions of bees. This study shows a strong association between pollinators and the attracting and rewarding features of flowers.     

Evolution of a non-flying mammal-dependent pollination system in Asian Mucuna (Fabaceae)

Pollinator shifts are often related to speciation in angiosperms, and the relationship between them has been discussed in several plant taxa. Although limited information on plants pollinated by non-flying mammals in Central and South America and Africa is available, related research has not been conducted in Asia. Herein, I summarize the available knowledge of pollination in Asian Mucuna (Fabaceae), a genus mainly distributed in the tropics, and discuss the evolution of plants pollinated by non-flying mammals in Asia. Nineteen pollinator species have been recorded and pollination systems have been categorized into four types. An examination of the relationship between Mucuna species and their pollinators from the lineage perspective revealed that all species in Mucuna, subgenus Macrocarpa, which are distributed in Asia, are pollinated exclusively by non-flying mammals. Additionally, plants pollinated by non-flying mammals were found to have diverged from bat-pollinated and non-flying mammal-pollinated plants, while plants pollinated by non-flying mammals have evolved multiple times. This is a unique example of evolutionary transition. I hypothesize that the diversification of squirrel species in tropical Asia may have led to the speciation and diversification of Mucuna in Asia. Furthermore, the behavioural and ecological characteristics of bats and birds in Asia differ from the characteristics of those in other regions, implying that Asian Mucuna species do not rely on bat or bird pollinators. The adaptation of floral characteristics to pollinators is not well understood in Asia. Mammal-pollinated plants in Asia may have evolved differently from those in other regions and have unique pollination systems.     

Diurnal and nocturnal pollination of Marginatocereus marginatus (Pachycereeae: Cactaceae) in Central Mexico

BACKGROUND AND AIMS: Chiropterophillous and ornithophillous characteristics can form part of a single reproductive strategy in plants that have flowers with diurnal and nocturnal anthesis. This broader pollination strategy can ensure seed set when pollinators are scarce or unpredictable. This appears to be true of hummingbirds, which presumably pollinate Marginatocereus marginatus, a columnar cactus with red nocturnal and diurnal flowers growing as part of dense bat-pollinated columnar cacti forests in arid regions of central Mexico. The aim of this study was to study the floral biology of M. marginatus, and evaluate the effectiveness of nocturnal vs. diurnal pollinators and the contribution of each pollinator group to overall plant fitness. METHODS: Individual flower buds were marked and followed to evaluate flower phenology and anthesis time. Flowers and nectar production were measured. An exclusion experiment was conducted to measure the relative contribution of nocturnal and diurnal pollinators to seed set. KEY RESULTS: Marginatocereus marginatus has red hermaphroditic flowers with nocturnal and diurnal anthesis. The plant cannot produce seeds by selfing and was pollinated during the day by hummingbirds and during the night by bats, demonstrating that both pollinator groups were important for plant reproduction. Strong pollen limitation was found in the absence of one of the pollinator guilds. CONCLUSIONS: Marginatocereus marginatus has an open pollination system in which both diurnal and nocturnal pollinators are needed to set seeds. This represents a fail-safe pollination system that can ensure both pollination, in a situation of low abundance of one of the pollinator groups (hummingbirds), and high competition for nocturnal pollinators with other columnar cacti that bloom synchronously with M. marginatus in the Tehuacan Valley, Mexico.     

Surprising absence of association between flower surface microstructure and pollination system

• The epidermal cells of flowers come in different shapes and have different functions, but how they evolved remains largely unknown. Floral micro‐texture can provide tactile cues to insects, and increases in surface roughness by means of conical (papillose) epidermal cells may facilitate flower handling by landing insect pollinators. Whether flower microstructure correlates with pollination system remains unknown.
• Here, we investigate the floral epidermal microstructure in 29 (congeneric) species pairs with contrasting pollination system. We test whether flowers pollinated by bees and/or flies feature more structured, rougher surfaces than flowers pollinated by non‐landing moths or birds and flowers that self‐pollinate.
• In contrast with earlier studies, we find no correlation between epidermal microstructure and pollination system. The shape, cell height and roughness of floral epidermal cells varies among species, but is not correlated with pollinators at large. Intriguingly, however, we find that the upper (adaxial) flower surface that surrounds the reproductive organs and often constitutes the floral display is markedly more structured than the lower (abaxial) surface.
• We thus conclude that conical epidermal cells probably play a role in plant reproduction other than providing grip or tactile cues, such as increasing hydrophobicity or enhancing the visual signal.