Staminal Lever Research Articles

Mixed mating patterns in morphologically diverse bumblebee-pollinated Salvia species from China

Abstract Flowers of Salvia are characterized by a diversity of staminal lever types mediating pollen transfer. In the East Asian subgenus Glutinaria, species have been categorized based on their distinct flower and stamen morphologies. A hypothesized advantage of degraded-lever types suggests they may optimize pollinator foraging time, increase visitation rates, and potentially trigger autonomous self-pollination. However, this hypothesis remains untested. Here, Salvia castanea, S. miltiorrhiza, and S. liguliloba were selected as test species representing the three major flower and stamen types of the East Asian sages. We compared the species with regard to their inflorescence architecture, floral display, nectar reward, pollinator efficiency, and seed set. We found that S. liguliloba had a degraded-lever type that significantly reduced pollinator foraging time did not significantly increase pollination efficiency. These species have a mixed mating pattern with high seed set, no pollen- or pollinator limitation, and no inbreeding depression. We conclude that the diversity of floral traits is addressed to pollinators, whereas reproductive success emerges from a complex interplay of factors encompassing floral characteristics, pollination efficiency, plant life history, or/and other biotic and abiotic factors. For this reason, the link between floral morphological traits and mating systems should not overestimated.

Evolution of anther connective teeth in sages (Salvia, Lamiaceae) under bee and hummingbird pollination

Salvia (Lamiaceae) is a sub-cosmopolitan genus of about 1000 species that often employ a “staminal lever mechanism” that is thought to have spurred species diversification within the genus. The function and evolution of ventral outgrowths or connective teeth, associated with the lever mechanism in some species of Salvia, is often unclear despite the wealth of pollination observations across the genus and the major role that pollinators play in driving diversification within the genus. We document the role of these teeth in pollination studies of bee-pollinated Salvia farinacea, examine connective teeth across other bee- and hummingbird-pollinated species of New World subg. Calosphace, and provide an evolutionary scenario for the connective teeth in context of the staminal lever. Our observations show that the larger teeth function as pressure points at the floral entrance and, when pressed by a pollinator, facilitate movement of the lever. Multiple shifts in pollinator within subg. Calosphace may have resulted in further modifications of the connective and possible further losses and independent origins of connective teeth in Calosphace. Other distantly related subgenera (e.g., Sclarea, Glutinaria) display morphologically and spatially different protuberances on the connective, suggesting that connective teeth only evolved near the base of subg. Calosphace.

Hiding in plain sight: Integrative analyses uncover a cryptic Salvia species in Europe

AbstractSalvia is the most species‐rich genus of the family Lamiaceae, currently numbering almost 1000 species. The diagnostic feature of the genus is the unique staminal lever mechanism that allows for specific pollination modes. We encountered an unusual Salvia form in the field, in SE Romania, which resembles S. austriaca but features a radically different lever mechanism. This form proved to be geographically widespread on the Pontic steppe, never occurring in sympatry with S. austriaca. We used an integrative approach, employing morphometric and phylogenomic (RADseq) analyses, to study this unusual form. The taxon's floral morphology proved to be consistently and subtly different from that of S. austriaca, and similarly, Bayesian species delimitation using genome‐wide SNP data indicated species‐level differences. Our results provide compelling evidence that points toward the discovery of an unrecognized species. This species has been overlooked for centuries, misidentified as S. austriaca, a closely related taxon. The new species differs from S. austriaca in key features of floral structure, habitat preference, and distribution. The potential range of this cryptic species, its pollination biology, ecology, and phylogeography are discussed.

Floral biology in the endemic Iranian Salvia majdae - implications for taxonomy, character evolution and conservation

Salvia (Lamiaceae), one of the largest plant genera, was not monophyletic as originally circumscribed. To recognize Salvia as a monophyletic genus, five small genera have been placed within Salvia s.l. including the monotypic genus Zhumeria. Little is known about the floral biology of Salvia majdae (syn. Z. majdae), an aromatic medicinal shrub species endemic to dry montane areas in the Hormozgan Province in southern Iran. Floral and ecological features of the species are provided as a basis for more detailed discussion about its taxonomic treatment and conservation. S. majdae produces flowers in the axils of the uppermost leaves as racemes. Unlike most Salvia species, flowers are weakly monosymmetric and lack the typical upper lip that usually hides the pollen-sacs. Each flower has four protruding stamens, the abaxial pair is always fertile, and the adaxial one is mostly sterile. Anthers are bithecate and immobile, the connective is slightly widened but not separating the thecae from each other as in most Salvia species. A staminal lever mechanism is lacking and, contrary to most Salvia flowers, pollen is ventrally transferred. Floral longevity is about three days. Flowers are protandrous on the first day and present both pollen and receptive stigmas on the second day. Controlled pollination experiments confirm self-compatibility of the species. Butterflies, bees and flies visited flowers and were likely attracted by scent and the conspicuous, dark violet color of the flowers. Medium-sized bees (Anthophora spp.) are probably the main pollinators, but pollen transfer by bee flies and occasionally by butterflies cannot be excluded. A moderate pollen/ovule ratio (∼2600:1), high pollen viability (∼90%), relatively high fruit set (75%), and moderate seed set (51%) indicate that the species successfully reproduces sexually. Herbivores strongly contributed to reduced seed set as they destroyed parts of the reproductive organs. The presence of only few seedlings and young plants in the field suggests that environmental pressures are acting on the species demography. To protect the species, we recommend harvest reduction by local people, propagating the plant in nurseries for medicinal purposes, and restocking their natural habitat with young plants. Flower morphology of S. majdae differs considerably from those of its closest Salvia relatives. The species represents a number of plesiomorphic characters which may either represent the ancestral stage or a reversal evolved from a more derived Salvia flower. We discuss these alternatives pointing to the problems linked with the present taxonomic treatment of Salvia s.l.

Phylogeny and staminal evolution of Salvia (Lamiaceae, Nepetoideae) in East Asia.

Salvia is the largest genus within Lamiaceae, with about 980 species currently recognized. East Asia, with approx. 100 species, is one of the three major biodiversity centres of Salvia. However, relationships within this lineage remain unclear, and the staminal lever mechanism, which may represent a key innovation within the genus, has been understudied. By using six genetic markers and nearly comprehensive taxon sampling, this study attempts to elucidate relationships and examine evolutionary trends of staminal development within the East Asia (EA) Salvia clade. Ninety-one taxa of EA Salvia were sampled and 34 taxa representing all other major lineages of Salvia were included for analysis. Two nuclear [internal transcribed spacer (ITS) and external transcribed spacer (ETS)] and four chloroplast (psbA-trnH, ycf1-rps15, trnL-trnF and rbcL) DNA markers were used for phylogenetic analysis employing maximum parsimony (MP), maximum likelihood (ML) and BEAST, with the latter also used to estimate divergence times. All Salvia species native to East Asia form a clade, and eight major subclades (A-G) were recognized. Subclade A, comprising two limestone endemics (S. sonchifolia and S. petrophila), is sister to the remainder of EA Salvia. Six distinct stamen types were observed within the EA clade. Stamen type A, with two fully fertile posterior thecae, only occurs in S. sonchifolia and may represent the ancestral stamen type within EA Salvia. Divergence time estimates showed that the crown of EA Salvia began to diversify approx. 17.4 million years ago. This study supports the adoption of a broadly defined Salvia and treats EA Salvia as a subgenus, Glutinaria, recognizing eight sections within this subgenus. Stamen type A is ostensibly plesiomorphic within EA Salvia, and the other five types may have been derived from it. Staminal morphology has evolved in parallel within the EA Salvia, and staminal structure alone is inadequate to delimit infrageneric categories.

Salvia apiana — A carpenter bee flower?

Salvia apiana has unique mask flowers restricting access to nectar by a bulged lower lip. Stamens and style protrude the flower tube. Most interesting, the staminal lever mechanism usually characterizing bee flowers in Salvia L. is lacking. In the present study, we aim to understand the peculiar pollination mechanism and to identify the pollinators and breeding system of the species. Field experiments were conducted at three natural localities in Southern California and the Rancho Santa Ana Botanical Garden, Claremont. Pollinator behavior was documented on video and interpreted considering frequency, handling time, percentage of successfully touching pollen and stigma, pollen deposition site on the pollinator's body and duration of stay per inflorescence. Hand-pollination and bagging experiments were conducted to identify breeding system and seed set. Salvia apiana is self-compatible. The pollen/ovule ratio of 11,000:1 points to xenogamy, but our experiments indicate that the plant suffers from pollinator limitation at the study sites. The most frequent pollinators were honeybees (Apis mellifera), which, however, are too small and light to handle the flower correctly. They only occasionally transfer pollen increasing geitonogamy. We identified Bombus vosnesenskii, Xylocopa tabaniformis and X. varipuncta as rare pollinators. These large bees were able to press the lower lip down thereby lowering the stamens and positioning the pollen sacs close to the bee's body. The largest bee, X. varipuncta, was found to fit best to the flower. Due to its foraging behavior, it particularly contributes to outcrossing. Though honeybees are the most frequent pollinators, we conclude that S. apiana is a carpenter bee flower. The species most likely suffers under the low number of Xylocopa bees which might result from the present dominance of honeybees, introduced to California three hundred years ago.

Phenotypic selection on the staminal lever mechanism in Salvia digitaloides (Labiaceae)

The staminal lever mechanism of pollination in Salvia has been considered as a key innovation, which was proposed to contribute to adaptive radiation of the genus. Considering its sophisticated interaction with pollinators, we hypothesized that relevant floral traits in the lever mechanism might be subject to intense selection in natural populations. In the present study, Salvia digitaloides was employed to investigate phenotypic selection on the floral traits. The results indicated that there were large variations in the floral structural traits and spatial position of the stigma. No significant selection was detected on the plausible key trait, i.e. the stamen lever length. Strong stabilizing selection acted consistently on the size of corolla entrance; that is, the intermediate corolla entrance was at a selective advantage. Both corolla length and style exsertion were subject to opposite directional selection in both years; and corolla entrance height was subject to disruptive selection, which was attributed to divergent adaptation of the trait to different body-sized pollinators. Furthermore, correlational selection acted on a few pairs of traits which described corolla entrance size and stigma position. Flower production was consistently subject to significantly positive directional selection in both years. In conclusion, it was most likely that floral traits involved in the staminal lever mechanism evolved in a functionally integrated manner for the enhancement of pollination efficiency in the natural population of S. digitaloides.

Evolutionary response of staminal lever mechanism of different species in Salvia to spatial variation in pollinators

Aims Floral diversification in animal-pollinated species was widely believed to be driven by pollinator-mediated natural selection in response to the geographical mosaic of pollinators. Our objective was to explore the evolutionary response of staminal lever mechanism in Salvia to variation in pollinator assemblage in a spatial context. Methods We employed three species (four populations) and conducted comparative studies on pollinator-flower interactions in different populations through investigating pollinator assemblage and measuring floral traits and body size of pollinators. Important findings Floral traits investigated, including corolla length, staminal lever length and other structural traits, exhibited distinct differences among populations. These corresponded with variations in composition of pollinators and the main pollinator and its body size in each population. The two types of pollination modes in each population were ventral pollination and dorsal pollination, which was the effective one. The main pollinator’s body length was significantly positively correlated with staminal lever length and negatively correlated with corolla length in spatial context. Both corolla entrance height and stigma height were related to variation in body thickness of the main pollinator among populations. In conclusion, the vulnerability of lever-like stamens and other relevant floral traits to the geographical mosaic of pollinators implies the key role that the staminal lever plays in pollination, and its high evolutionary plasticity might have contributed to adaptive radiation of species in Salvia.

Functional implications of the staminal lever mechanism in Salvia cyclostegia (Lamiaceae)

Flower morphology and inflorescence architecture affect pollinator foraging behaviour and thereby influence the process of pollination and the reproductive success of plants. This study explored possible ecological functions of the lever-like stamens and the floral design in Salvia cyclostegia. Flower construction was experimentally manipulated by removing either the lower lever arms or the upper fertile thecae of the two stamens from a flower. The two types of manipulated individuals were intermixed with the control ones and randomly distributed in the population. Removing the sterile lower lever arms significantly reduced handling time per flower of the main pollinator, Bombus personatus. Interestingly, this manipulation did not increase the number of flowers probed per plant visit, but instead reduced it, i.e. shortened the visit sequence of the bumble-bees. Both loss of staminal lever function by removing lower lever arms and exclusion of self pollen by removing upper fertile thecae significantly reduced seed set per flower and seed set per plant. Both the manipulations interacted significantly with inflorescence size for the effect on female reproductive output. Though the intact flowers demand a long handling time for pollinators, the reversible staminal lever is of advantage by promoting dispersal of pollen and thus the male function. The particular floral design in S. cyclostegia contributes to the floral constancy of B. personatus bumble-bees, with the lower lever arms acting as an optical cue for foraging cognition.

Floral Diversity and Pollen Transfer Mechanisms in Bird-pollinated Salvia Species

Bird-pollinated (ornithophilous) Salvia species (sages) transfer pollen either by means of a staminal lever mechanism or by immovable stamens. As the distribution of the two modes within the genus is not known, we present a survey of all ornithophilous sages. The main focus is given to floral diversity especially with respect to functional lever morphology. Thereby the hypothesis is tested that, due to a pollinator shift from bees to birds, the lever mechanism became unnecessary. To get a general idea about the diversity of pollen transfer mechanisms, 186 ornithophilous Salvia species were classified according to the functional morphology of the stamen and the need for a lever movement. To test the functionality of the staminal levers and the fitting between flowers and birds the process of pollen transfer was examined by pollinator observations and tested by inserting museum skins and metal rods into fresh flowers. The diversity of pollen transfer mechanisms is represented by eight case studies illustrating three main groups. In group I (approx. 50 %) the staminal lever mechanism is necessary to open access to nectar and to enable the transfer of pollen that is hidden in the upper lip. In group II (approx. 34 %) pollen is freely accessible and the lever mechanism is reduced in different ways and to different degrees. In group III (approx. 4 %) the lever works as in group I, but pollen is freely accessible as in II. The remaining approx. 13 % are not clearly classified. It is considered that the driving force behind the diverse modes of reduction is the necessity to increase the distance between nectar and pollen, thereby ensuring pollen deposition on the bird's feathered head. This is achieved several times in parallel by corolla elongation and/or exposure of the pollen-sacs. As soon as pollen is freely accessible, the lever movement loses its significance for pollination.

New Insights into the Functional Morphology of the Lever Mechanism of Salvia pratensis (Lamiaceae)

The functional morphology of Salvia pratensis flowers was re-investigated, after new insights revealed that pollen dispensing is one of the main functions of the staminal lever. In particular, no detailed information was available regarding the process of pollen transfer and the forces arising between the pollen-bearing thecae and the pollinating bee's body. The assumption was made that these forces play a significant role in pollen dispensing. The functional morphology of S. pratensis flowers and the interaction between flowers and bees (Apis mellifera) were studied by reconstructing stress and strains by using qualitative and semi-quantitative theoretical analysis. Flowers were manipulated to study the spatial arrangement of the filament and lever, and of the head and proboscis of the visiting bee inside the tube. Photographs and films of bee visits on flowers were used to analyse the interaction of pollinator and staminal lever. The spoon-shaped lower lever of S. pratensis has a small hole through which a bee introduces its proboscis into the corolla tube. Although mentioned for the first time by Kerner von Marilaun in 1891, presented here is the first drawing and the first photograph showing this interaction in detail. The analysis of the interaction of flower visitor and the lever mechanism revealed that the position of bees on different flowers is spatially very similar. Flower morphology constrains postures of legitimately nectar-probing bees within narrow bounds. A theoretical discussion on structural elements and force progression in the flower allows the principles of lightweight architecture in flower morphology to be recognized. The staminal lever of S. pratensis is a pollen-dispensing device. It seems to influence the amount of pollen deposited on pollinators by determining the forces arising between the pollinator and the pollen. The relevant forces occur either during the first, dynamic phase or during the second, almost static phase of a flower visit.

Staminal Evolution in the Genus Salvia (Lamiaceae): Molecular Phylogenetic Evidence for Multiple Origins of the Staminal Lever

The genus Salvia has traditionally included any member of the tribe Mentheae (Lamiaceae) with only two stamens and with each stamen expressing an elongate connective. The recent demonstration of the non-monophyly of the genus presents interesting implications for staminal evolution in the tribe Mentheae. In the context of a molecular phylogeny, the staminal morphology of the various lineages of Salvia and related genera is characterized and an evolutionary interpretation of staminal variation within the tribe Mentheae is presented. Two molecular analyses are presented in order to investigate phylogenetic relationships in the tribe Mentheae and the genus Salvia. The first presents a tribal survey of the Mentheae and the second concentrates on Salvia and related genera. Schematic sketches are presented for the staminal morphology of each major lineage of Salvia and related genera. These analyses suggest an independent origin of the staminal elongate connective on at least three different occasions within the tribe Mentheae, each time with a distinct morphology. Each independent origin of the lever mechanism shows a similar progression of staminal change from slight elongation of the connective tissue separating two fertile thecae to abortion of the posterior thecae and fusion of adjacent posterior thecae. A monophyletic lineage within the Mentheae is characterized consisting of the genera Lepechinia, Melissa, Salvia, Dorystaechas, Meriandra, Zhumeria, Perovskia and Rosmarinus. Based on these results the following are characterized: (1) the independent origin of the staminal lever mechanism on at least three different occasions in Salvia, (2) that Salvia is clearly polyphyletic, with five other genera intercalated within it, and (3) staminal evolution has proceeded in different ways in each of the three lineages of Salvia but has resulted in remarkably similar staminal morphologies.

Hummingbird pollination in Salvia haenkei (Lamiaceae) lacking the typical lever mechanism

While in most Salvia species pollen is transferred by the `staminal lever mechanism', in some species the `levers' are inactive. This is also found in the bird pollinated S. haenkei from Bolivia. To understand pollen transfer in a species lacking the lever mechanism we carried out field investigations and confirmed our observations by means of morphometric measurements of both the flowers and museum skins of the observed hummingbird species. The tubular corolla forces the birds (Sappho sparganura, Colibri coruscans, Patagona gigas, Oreotrochilus adela) into a specific position thereby causing pollen transfer from the exserted pollen-sacs to the bird's feathers and bills. The staminal levers are well developed but cannot be moved because the sterile arms are closely attached to the upper face of the corolla leaving no space for any movement. We assume that the reduction of the lever mechanism reflects an adaptation to bird pollination.

The staminal lever mechanism in Salvia L. (Lamiaceae): a key innovation for adaptive radiation?

Floral key innovations play a significant role in the discussion of adaptive radiation in plants. The paper brings together a brief review of morphological key innovations in plants, elucidating their evolutionary significance in flower–pollinator interactions, and new data on Salvia, a genus being examined as an example for presumed adaptive radiation. We hypothesize that the characteristic staminal lever mechanism functions as a key innovation. It is defined as a functional unit including the modification of stamens to lever-like structures, their reversible movement, and the organization of the remaining floral structures involved in the process of pollen transfer. We follow the assumption that structure and functioning of the staminal levers play a major role in the process of pollen deposition on the pollinator's body, and that minute changes of both their proportions and their interactions with pollinators may have significant consequences for the pollination system. The functioning of the staminal lever mechanism is tested by field investigations, biomechanical experiments and pollination simulations. First results are presented, and possible modes of allopatric and sympatric speciation are discussed, based on morphometry of Salvia flowers and pollinators as well as on the operating mode of the staminal lever mechanism. Special attention is given to species-specific patterns of pollen deposition on the pollinator's body. We assume that, depending on the precision of the lever movement, sympatric Salvia species flowering during overlapping periods and sharing the same pollinating species may be either mechanically isolated from each other or able to hybridize. The latter may result in speciation, as may spontaneous mutations influencing the flower-pollinator interaction, e.g. by significant changes in morphometry of the staminal lever system and/or other flower structures. As a consequence, Salvia individuals may deposit pollen on a different part of the pollinator's body, or even adapt to a new pollinator species, both resulting in reproductive isolation from the parental population.

The Staminal Lever Mechanism in Salvia L. (Lamiaceae) ‐ a Review

Abstract: The genus Salvia encompasses about 900 species distributed world‐wide. It is characterized by the famous staminal lever mechanism of the flower which is one of the best known examples of a nototribic pollination mechanism. We hypothesize that structure and functioning of the staminal levers play a major role as key structures in speciation. To cope with the complex evolutionary processes involved, a number of different methodological approaches are needed. The present paper summarizes the literature referring to structural and functional diversity, breeding systems, systematics and evolution in Salvia.