Ancient or recent? Insights into the temporal evolution of the Bruniaceae

AbstractThe Bruniaceae are a South African plant family endemic to the Cape Floristic Region with one geographic outlier (Raspalia trigyna) in the Natal Province. Recent molecular phylogenetic analyses have cast new light upon inter- and intra-generic relationships within the family. The present work uses those data to gain insights into the temporal evolution of Bruniaceae by inferring a molecular clock. For calibration, the inferred age of Berzelia cordifolia (3–5My) was used, based on its distribution restricted to the geologically young limestone area around Bredasdorp. The results are consistent with the purported Cretaceous age of the family (‘palaeoendemics’), but also suggest that m…

Flower-like meristem conditions and spatial constraints shape architecture of floral pseudanthia in Apioideae

Abstract Background Pseudanthia are multiflowered units that resemble single flowers, frequently by association with pseudocorollas formed by enlarged peripheral florets (ray flowers). Such resemblance is not only superficial, because numerous pseudanthia originate from peculiar reproductive meristems with flower-like characteristics, i.e. floral unit meristems (FUMs). Complex FUM-derived pseudanthia with ray flowers are especially common in Apiaceae, but our knowledge about their patterning is limited. In this paper, we aimed to investigate both the genetic and morphological basis of their development. Results We analysed umbel morphogenesis with SEM in six species representing four clades…

Insights Into the Inside – A Quantitative Histological Study of the Explosively Moving Style in Marantaceae

This study aims to identify the histological basis for the extraordinary, fast movement of the style in Marantaceae. Although this explosive pollination mechanism was subject of many studies, quantitative measurements to document volumetric changes have never been conducted. Based on physical parameters and limitations (poroelastic time), the movement itself is by far too fast to be explained by turgor changes solely. Therefore, we address the hypothesis that the style contains elastic structures to store energy allowing the fast movement. We provide an experimental approach in Goeppertia bachemiana to identify histological differences of styles in various states, i.e., steady, unreleased, …

Plant Morphology: The Historic Concepts of Wilhelm Troll, Walter Zimmermann and Agnes Arber

Recent molecular systematic and developmental genetic findings have drawn attention to plant morphology as a discipline dealing with the phenotypic appearance of plant forms. However, since different terms and conceptual frameworks have evolved over a period of more than 200 years, it is reasonable to survey the history of plant morphology; this is the first of two papers with this aim. The present paper deals with the historic concepts of Troll, Zimmermann and Arber, which are based on Goethe's morphology. Included are contrasting views of ‘unity and diversity’, ‘position and process’, and ‘morphology and phylogeny’, which, in part, are basic views of current plant morphology, phylogenetic…

Why Africa matters: evolution of Old World Salvia (Lamiaceae) in Africa

BACKGROUND AND AIMS Salvia is the largest genus in Lamiaceae and it has recently been found to be non-monophyletic. Molecular data on Old World Salvia are largely lacking. In this study, we present data concerning Salvia in Africa. The focus is on the colonization of the continent, character evolution and the switch of pollination systems in the genus. METHODS Maximum likelihood and Bayesian inference were used for phylogenetic reconstruction. Analyses were based on two nuclear markers [internal transcribed spacer (ITS) and external transcribed spacer (ETS)] and one plastid marker (rpl32-trnL). Sequence data were generated for 41 of the 62 African taxa (66 %). Mesquite was used to reconstru…

Breeding system and fruit set in African Marantaceae

Abstract Marantaceae are a pantropically distributed family of perennial herbs and lianas in the understory of tropical rainforests. They are characterized by a unique pollen transfer mechanism. To understand its functional significance and evolution, field investigations have been conducted in Gabon. Data from 28 (of 35) species from Central Africa are achieved. The pollen–ovule ratio (34–140:1; exception Sarcophrynium 2.5:1) falls into the range of facultative autogamous species. All investigated species were proven to be self-compatible; however, only two were autogamous. Natural fruit set was generally low (10.9 ± 10%). The highest natural fruit set was found in Marantochloa purpurea (2…

Editorial: From Meristems to Floral Diversity: Developmental Options and Constraints

Consistent phenological shifts in the making of a biodiversity hotspot: the Cape flora

Abstract Background The best documented survival responses of organisms to past climate change on short (glacial-interglacial) timescales are distributional shifts. Despite ample evidence on such timescales for local adaptations of populations at specific sites, the long-term impacts of such changes on evolutionary significant units in response to past climatic change have been little documented. Here we use phylogenies to reconstruct changes in distribution and flowering ecology of the Cape flora - South Africa's biodiversity hotspot - through a period of past (Neogene and Quaternary) changes in the seasonality of rainfall over a timescale of several million years. Results Forty-three dist…

Nectar protection in arid-adapted flowers of Zygophyllaceae-Zygophylloideae

Abstract The survival of plants in arid areas depends on efficient adaptation to extreme environments. The protection against nectar loss is an important challenge for flowers in arid environments. Flowers of arid-adapted Zygophyllaceae subfamily Zygophylloideae are characterized by a peculiar structure called staminal scales (SS). The special arrangement of SS around the perigynous disc nectary (DN) suggests their adaptive function for protection against nectar loss. We aim to test the protective function of SS and to understand the synorganised evolution of SS and DN in relation to nectar protection. We, first, manipulate flowers by removal of SS in two representatives of Zygophylloideae.…

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

† Background and Aims 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. † Methods 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 a…

Ontogenetic and phylogenetic diversification of the hooded staminode in Marantaceae

The flowers of Marantaceae are known for their unique pollination mechanism mediated by an explosive style movement. The mechanism is based on the highly modified elements of the inner androecial whorl, i.e., the single half-fertile anther and the fleshy and hooded staminodes. We investigated 67 species across 24 genera to elucidate which parts of the hooded staminode are shared by all species, thus likely under strong selection pressure, and which are allowed to vary. We treated hooded staminodes as character syndromes and grouped them based on gross similarities. We identified characters underlying the similarity and investigated their diversity and developmental pathways. All hooded stam…

Training experiments with Bombus terrestris and Apis mellifera on artificial ‘ Salvia ’ flowers

Abstract Many bee flowers demand physical force from their pollinators. An example is Salvia with lever-like anthers restricting access to nectar. Though the needed force is generally low, it is largely unknown how far even low forces affect flower preference and foraging behaviour of bees. In the present paper, we introduce a method to measure the response of bees to a force mechanism. We explain the construction of artificial flowers mimicking the lever mechanism of a Salvia flower and the procedure to train honeybees and bumblebees to the models. We document the behaviour of the bees on models without barriers and on those with low forces aiming at the same time to determine the bees’ se…

Patterns of flower development in Apiaceae–Apioideae

Abstract Apiaceae is a large family characterized by uniform flowers. However, early ontogenetic studies revealed unexpected diversity in flower development. In the present paper, we investigate eight species representing six tribes of subfamily Apioideae to address diversity in developmental patterns. One focus is on the developmental divergence of sex morphs in andromonoecious species. Scanning electron microscopic studies were conducted on six herbaceous species: Chaerophyllum bulbosum , Daucus carota , Dorema aucheri , Ferula hezarlalehzarica , Orlaya grandiflora , Pastinaca sativa , and two woody species, i.e., Bupleurum fruticosum and Seseli ghafoorianum . Our results confirm the exis…

A combination of dichogamy and herkogamy mediates reproductive success in the desert shrub Zygophyllum fabago

Abstract Zygophyllum fabago is a species within the arid-adapted family Zygophyllaceae. The species is characterized by the co-occurrence of dichogamy and herkogamy. In order to understand the effect of these two complementary anti-selfing mechanisms in reproductive success, we conducted a detailed study of floral biology in Z. fabago. Our results indicated an incomplete separation of the female and male phases which is referred to as partial dichogamy. We found two floral morphs with distinct stigma position: the Central-morph (C-morph) and the Lateral-morph (L-morph). The stigma-stamen distance in the L-morph was significantly larger than in the C-morph in early, mid, and late male stages…

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

† Background and Aims 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. † Methods 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 th…

The unique pseudanthium of Actinodium (Myrtaceae) - morphological reinvestigation and possible regulation by CYCLOIDEA-like genes

Background Genes encoding TCP transcription factors, such as CYCLOIDEA-like (CYC-like) genes, are well known actors in the control of plant morphological development, particularly regarding the control of floral symmetry. Despite recent understanding that these genes play a role in establishing the architecture of inflorescences in the sunflower family (Asteraceae), where hundreds of finely organized flowers are arranged to mimic an individual flower, little is known about their function in the development of flower-like inflorescences across diverse phylogenetic groups. Here, we studied the head-like pseudanthium of the Australian swamp daisy Actinodium cunninghamii Schau. (Myrtaceae, the …

Space matters: meristem expansion triggers corona formation in Passiflora

Background and aims Flower meristems differ from vegetative meristems in various aspects. One characteristic is the capacity for ongoing meristem expansion providing space for new structures. Here, corona formation in four species of Passiflora is investigated to understand the spatio-temporal conditions of its formation and to clarify homology of the corona elements. Methods One bird-pollinated species with a single-rowed tubular corona (Passiflora tulae) and three insect-pollinated species with three (P. standleyi Killip), four (P. foetida L. ‘Sanctae Martae’) and six (P. foetida L. var. hispida) ray-shaped corona rows are chosen as representative examples for the study. Flower developmen…

Pollination syndromes in African Marantaceae

† Background and Aims The Marantaceae (550 spp.) is the most derived family in the order Zingiberales and exhibits a complex explosive pollination mechanism. To understand the evolutionary significance of this unique process of pollen transfer, comparative morphological and ecological studies were conducted in Gabon. † Methods During a total stay of 11 months, 31 species of Marantaceae were investigated at different sites in Gabon. The study included analyses of floral diversity, observations on the pollinator spectrum as well as ecological measurements (e.g. nectar sugar concentration and volume). † Key Results Analyses reveal five flower types based on flower size and pigmentation, spatia…

Andromonoecy and developmental plasticity in Chaerophyllum bulbosum (Apiaceae–Apioideae)

Background and Aims: Andromonoecy, the presence of hermaphrodite and male flowers in the same individual, is genetically fixed or induced, e.g. by fruit set. Little is known about the forces triggering andromonoecy in the Apiaceae. In the present study, a natural population of the protandrous Chaerophyllum bulbosum was investigated to elucidate architectural constraints and effects of resource reallocation. Methods: Three sets of plants (each n ¼ 15) were treated by hand pollination, pollinator exclusion and removal of low-order inflorescences. Fifteen untreated plants were left as controls. Key Results: Untreated plants produce umbels up to the third branch order, with increasing proportio…

Floral synorganization and its influence on mechanical isolation and autogamy in Marantaceae

The flowers of Marantaceae (∼ 550 species) exhibit a highly derived pollination mechanism within Zingiberales, with a rapid and irreversible style movement based on a close synorganization of different floral parts. Given the complexity of the structure, we assume that little variation is possible if functionality is to be maintained. To test this, we investigated how much floral diversity exists in the clade and whether this diversity potentially influences the breeding system and placement of pollen on the pollinator. Flowers of 66 species covering the five major phylogenetic clades of the family were analysed. All species are similar in their basic flower construction: the fleshy stamino…

‘False resupination’ in the flower-pairs of Thalia (Marantaceae)

Abstract Resupination, i.e., the turn by 180°, arranges zygomorphic flowers in a suitable position for pollination. It is well-known from orchids, but also occurs in further angiosperm families. Within the genus Thalia L. (Marantaceae), T. dealbata has erect and T. geniculata pendulous inflorescences. Nevertheless, in both species the zygomorphic flower-pairs show the right position for pollination. Thus, resupination is expected in Marantaceae. To reconstruct spatial arrangement, flower development was investigated from meristem formation to anthesis. Early morphogenetic stages were analysed under the scanning electron microscope, late stages were documented by time-lapse records. Gravity …

Evolution in African Marantaceae - Evidence from Phylogenetic, Ecological and Morphological Studies

Abstract The Marantaceae (∼530 spp.) are one of the most species rich families within the order Zingiberales which incites the search for evolutionary factors favoring speciation. A positive influence on their divergence is ascribed to their unique explosive pollination mechanism which has been proposed to be a key innovation. To test this hypothesis phylogenies of the two major African clades (Sarcophrynium and the Marantochloa clade) were established based on data from nuclear (ITS, 5S) and chloroplast (trnL/trnL-F) DNA for an almost complete taxon sample. The phylogeny was used to parsimoniously reconstruct morphological and ecological traits and geographic distribution patterns. The res…

Salvia apiana — A carpenter bee flower?

Abstract 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 depos…

Towards an ontogenetic understanding of inflorescence diversity

Backgrounds and aims Conceptual and terminological conflicts in inflorescence morphology indicate a lack of understanding of the phenotypic diversity of inflorescences. In this study, an ontogeny-based inflorescence concept is presented considering different meristem types and developmental pathways. By going back to the ontogenetic origin, diversity is reduced to a limited number of types and terms. Methods Species from 105 genera in 52 angiosperm families are investigated to identify their specific reproductive meristems and developmental pathways. Based on these studies, long-term experience with inflorescences and literature research, a conceptual framework for the understanding of infl…

The Search for Common Origin: Homology Revisited

Understanding the evolution of biodiversity on Earth is a central aim in biology. Currently, various disciplines of science contribute to unravel evolution at all levels of life, from individual organisms to species and higher ranks, using different approaches and specific terminologies. The search for common origin, traditionally called homology, is a connecting paradigm of all studies related to evolution. However, it is not always sufficiently taken into account that defining homology depends on the hierarchical level studied (organism, population, and species), which can cause confusion. Therefore, we propose a framework to define homologies making use of existing terms, which refer to …

Time to split Salvia s.l. (Lamiaceae) - New insights from Old World Salvia phylogeny.

Abstract Aims Salvia L. is widely known as the largest genus in the mint family. A morphological modification of the androecium (lever-like stamens) was used to support this genus. However, molecular data revealed that Salvia is polyphyletic. Since phylogenetic studies largely underrepresented Old World Salvia species, we filled this gap and combined new data with existing sequences. The aim of our study was the identification of well-supported clades that provide the basis for evolutionary and taxonomic conclusions. Methods We included ITS data (internal transcribed spacer) from 220 Salvia species, 86 of which were sequenced for the first time. Additionally, the highly variable plastid mar…

The shoot concept of the flower: Still up to date?

Abstract The shoot concept of the flower suggests that flowers correspond to vegetative short-shoots except the fact that their lateral appendages are floral and not vegetative leaves. However, in view of the different properties of vegetative and flower meristems, this concept should be questioned. Differential meristem activity resulting in tubes, hypanthia and inferior ovaries, continuous meristem expansion providing space for stamen fascicles and additional structures and the process of (repeated) fractionation using a given space completely, are characteristics of flower meristems hardly explainable with the shoot concept. Linking instead flower development with recent findings in mole…

Bilabiate Flowers: The Ultimate Response to Bees?

† Background and Aims Bilabiate flowers have evolved in many lineages of the angiosperms, thus representing a convincing example of parallel evolution. Similar to keel blossoms, they have obviously evolved in order to protect pollen against pollen-collecting bees. Although many examples are known, a comprehensive survey on floral diversity and functional constraints of bilabiate flowers is lacking. Here, the concept is widened and described as a general pattern. † Methods The present paper is a conceptional review including personal observations of the authors. To form a survey on the diversity of bilabiate blossoms, a search was made for examples across the angiosperms and these were combi…

Floral ontogeny, petal diversity and nectary uniformity in Bruniaceae

Bruniaceae are a small family subendemic to the Cape Floristic Region. Flowers are actinomorphic, choripetalous, pentamerous and tetracyclic. The petals show diverse adaxial swellings, which have been quoted as an example of diplophylly. Developmental studies confirm the true choripetaly of the flowers, thus pointing to an affinity to the Apiales within the euasterids II. They reject, however, the hypothesis of diplophylly as the petal swellings grow out rather late and are not vascularized. According to the position, size and shape of the swellings, six petal types are distinguished, which in part have phylogenetic information. Nectaries occur on the upper part of the ovary. Nectar is exuded …

Testing the ontogenetic base for the transient model of inflorescence development

† Backgrounds and Aims: Current research in plant science has concentrated on revealing ontogenetic processes of key attributes in plant evolution. One recently discussed model is the ‘transient model’ successful in explaining some types of inflorescence architectures based on two main principles: the decline of the so called ‘vegetativeness’ (veg) factor and the transient nature of apical meristems in developing inflorescences. This study examines whether both principles find a concrete ontogenetic correlate in inflorescence development. † Methods: To test the ontogenetic base of veg decline and the transient character of apical meristems the ontogeny of meristematic size in developing inf…

Open and closed inflorescences: more than simple opposites

The absence of a terminal flower in inflorescences (‘open inflorescences’) is currently explained by the maintenance of putative stem-cells in the central zone (CZ) of the inflorescence meristem (IM) governed by the CLAVATA– WUSCHEL regulatory loop. Disruption of this regulatory pathway, as in Arabidopsis TERMINAL FLOWER LOCUS 1 mutants, leads to terminal flower production. However, recent studies in other taxa reveal novel mechanisms of inflorescence termination; for example, the SEPALLATA-like MADS-box floral identity gene GERBERA REGULATOR OF CAPITULUM DEVELOPMENT 2 in Gerbera excludes the retention of a CZ as an ontogenetic cause for the openness of these inflorescences. Moreover, compa…

Pollination biology in Roepera (Zygophyllaceae): How flower structure and shape influence foraging activity

The foraging behavior of bees is a complex phenomenon that depends on numerous physical features of flowers. Of particular importance are accessibility of floral rewards, floral proportions, symmetry and orientation. The flowers of Roepera are characterized by the presence of staminal scales (SS), which play an important role in nectar protection. We studied two species of Roepera with different symmetry and flower orientation, which are mainly visited by honeybees (Apis mellifera). We aimed to show how the foraging behavior of honey bees is affected by the function of SS, floral symmetry and orientation. The foraging behavior was documented by video photography. Handling time, access to ne…

Early ontogeny defines the diversification of primary vascular bundle systems in angiosperms

AbstractUnderstanding vascular bundle systems in angiosperms is a challenge. On the one hand, the vascular tissue is extremely important in reconstructing the evolution and survivability of plants, but on the other hand, it forms a complicated three-dimensional system of controversially discussed phylogenetic and ontogenetic origin. To increase clarity, in this paper we briefly summarize histological, phylogenetic and molecular aspects of primary vascular bundle formation in angiosperms, adding histological data on early stages of vascular bundle formation, proposing a concept combining the different views and providing simplified illustrations to improve the understanding of primary vascul…

Live imaging of developmental processes in a living meristem of Davidia involucrata (Nyssaceae)

Morphogenesis in plants is usually reconstructed by scanning electron microscopy and histology of meristematic structures. These techniques are destructive and require many samples to obtain a consecutive series of states. Unfortunately, using this methodology the absolute timing of growth and complete relative initiation of organs remain obscure. To overcome this limitation, an in vivo observational method based on Epi-Illumination Light Microscopy (ELM) was developed and tested with a male inflorescence meristem (floral unit) of the handkerchief tree Davidia involucrata Baill. (Nyssaceae). We asked whether the most basal flowers of this floral unit arise in a basipetal sequence or, altern…

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

Abstract 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…

Bird pollination in South African Salvia species

Abstract Approximately one-fourth of the more than 900 world-wide distributed Salvia species (Lamiaceae) is ornithophilous. With few exceptions they occur in the New World, being predominantly pollinated by hummingbirds. In the Old World only Salvia africana-lutea and the recently described Salvia thermarum, both from the Cape Province of South Africa, were observed to be pollinated by sunbirds and white-eyes. Among the 23 South African Salvia species Salvia lanceolata is a further candidate for being bird pollinated. For the first time we describe and illustrate its pollination by Nectarinia chalybea and Zosterops pallidus. We compare the ornithophilous syndrome of the three mentioned Salv…

The plasticity of breeding system in arid-adapted Zygophylloideae

Abstract The assurance of reproductive success is an important challenge for arid-adapted plants. Self-compatibility is suggested as a mechanism to compensate for the inadequate breeding opportunities in extreme environments. Zygophylloideae is an arid-adapted subfamily which has successfully radiated in different ranges of arid habitats. In order to study the significance of selfing for the reproductive success of the Zygophylloideae, we calculated pollen ovule ratios (P/O) and conducted bagging experiments for autogamy and xenogamy in eleven representative members of Zygophylloideae and three species of the sister subfamilies Tribuloideae and Larreoideae. Our results revealed an extremely…

Vascular bundle modifications in nodes and internodes of climbing Marantaceae

AbstractNodes are interfaces between stems and leaves. Vascular bundles originate here and elongate into leaves and internodes. In Marantaceae, internodal bundles are highly diverse, including inverted bundles in the climbing genus Haumania. The objective of this paper is to characterize bundle forms, their position across the stem and their connection to leaves and short shoots in Haumania spp. and other unrelated African branch-angle climbers in the family (Hypselodelphys, Trachyphrynium). We question whether bundle inversion is a genus-specific trait in Haumania or related to the climbing growth form. Vascular bundles in internodes are scattered across the stem diameter in a characterist…

Pollination efficiency and pollen limitation in bistaminate vs tetrastaminate Lamiaceae