Laticifer distribution in fig inflorescence and its potential role in the fig-fig wasp mutualism

Although in Moraceae the presence of laticifers is considered to be a synapomorphy, little is known about the distribution and morphology of this type of secretory structure in the reproductive organs of its species. Ficus, the largest genus of Moraceae, is characterized by an inflorescence known as syconium and by an obligate mutualistic interaction with pollinating wasps. The objectives of the present study were to evaluate the distribution and morphology of laticifers in syconia of 36 species belonging to different Ficus sections and to survey traits of taxonomic and adaptive value for the group. Syconia containing flowers in a receptive state were collected, fixed and processed for anatomical analysis. All species studied have branched laticifers distributed in the syconium receptacle, in the ostiolar bracts and in the pedicel of staminate flowers. Almost all species show laticifers in the pedicel of shorter-styled flowers. Laticifers also occur in the pedicel of longer-styled flowers in most Ficus sections, except F. curtipes (Conosycea section) and more than 75% of the studied species of the Americanae section. Laticifers are observed in the sepals of 25 of the 36 species studied and occasionally in the pistil. The presence of laticifers in the pedicel of shorter-style flowers and its absence in the pistil suggest that the distribution of this secretory structure in the fig flower was selected by pressures imposed by the fig-fig wasp mutualism. The laticifers in the pedicel of shorter-styled flowers may confer protection to the developing wasp larvae against natural enemies. However, the absence of laticifers in the pistil of most Ficus species studied was probably selected by the mutualistic relationship with the agaonid pollinating wasps since the latex could interfere with oviposition through the style, with the larval development of the pollinating fig wasps, and the emergence of pollinator offspring from their galls.     

The reproductive biology of two poorly known relatives of the fig (Ficus) and insights into the evolution of the fig syconium

We conducted the first detailed investigation of the floral architecture and reproductive biology of two species from the genus Dorstenia, which are poorly known relatives of Ficus (Moraceae). Our aims were to extend and refine knowledge of the understudied genus Dorstenia and to explore possible insights into the evolution of the fig syconium. We characterised four key stages of floral development using light microscopy, scanning electron microscopy and histological staining. Reproductive biology was found to be complex and species‐specific. Both study species are monoecious and produce an inflorescence of minute male and female flowers. Protogyny, associated with a spatial separation of male and female flowers and asynchronous stamen development, was species‐specific, as was seed set. Our results reveal novel insights into the complex reproductive biology of an under‐studied genus in the family Moraceae. We propose that exploring the reproductive biology of Dorstenia and other poorly known Ficus relatives will provide insights into the evolution of the fig syconium – the unique reproductive structure of this economically and ecologically important genus.     

Secretory structures at syconia and flowers of Ficus enormis (Moraceae): A specialization at ostiolar bracts and the first report of inflorescence colleters

The fig (Ficus L.) infructescence, called syconium, is a receptacle with an apical opening, the ostiole, closed by bracts. The ostiolar bracts produce an exudate, which is rather conspicuous in some species. It has not been histochemically analyzed yet, and the structures responsible for its production are still unknown. Some wild growing species of Ficus from Brazil produce high amounts of this ostiolar exudate. Ficus enormis (Mart. ex Miq.) Miq. grows as trees or shrubs in the Atlantic rainforest. Our goal was to identify the secretory structures present in the inflorescence and, to characterize histochemically the ostiolar tissues and exudates. Syconia samples of F. enormis were processed and stained according to the usual techniques in plant anatomy. The morphological analysis revealed different types of bracts, one type specialized in secretion, another showing transitional characteristics between secretory and non-secreting bracts, and a third one being non-secreting. They are designated as secretory ostiolar bracts, transitional bracts and wall bracts. The floral bracteoles, digital-shaped colleters present in the ostiole, at the syconium axis and at the flower receptacle, were also analyzed. All have similar structure, like finger-shaped secretory trichomes. The colleters present among ostiolar bracts may contribute to production and composition of the ostiole exudate.     

On the origin of the fig: phylogenetic relationships of Moraceae from ndhF sequences

The majority of species in the mulberry family (Moraceae) are figs (Ficus), marked by a specialized inflorescence (syconium) and an obligate mutualism with pollinating fig wasps. Because of the unique morphology of the syconium, it has been difficult to investigate the evolutionary position of the fig. We sequenced the chloroplast gene ndhF to examine relationships in Moraceae and to elucidate shifts in reproductive traits. The reclassification of tribes is warranted, and the limits of Artocarpeae, Moreae, and Castilleae are revised to reflect evolutionary relationships. The results point to ancestral dioecy in Moraceae and multiple origins of monoecy, androdioecy, and gynodioecy. Ancestral wind pollination gave way to insect pollination at least twice. Strong support for the sister-group relationship of a revised Castilleae with Ficus suggests that entomophily and involucral bracts encircling the flowers preceded the evolution of the syconium. Bracts surround flowers in Castilleae only during early development, but in Ficus the involucre and the receptacle enclose the fruit as well. Molecular dating suggests that fig pollination is at least 80-90 million years old. The diversity of Ficus relative to its sister group is a likely consequence of ancient specialization and cospeciation with pollinating fig wasps.     

Choice of flowers by foraging honey bees (Apis mellifera): possible morphological cues

Abstract.

• 1 Honey bees foraging for nectar on lavender (Lavandula stoechas) chose inflorescences with more of their flowers open. The number of open flowers predicted whether an inflorescence was visited by bees, inspected but rejected, or ignored. Inflorescences chosen arbitrarily by observers had numbers of open flowers intermediate between those of visited and ignored inflorescences.
• 2 Differences in morphological characters between types of inflorescence correlated with nectar volume and sugar weight per flower so that visited inflorescences had a disproportionately greater volume of nectar and weight of sugar per flower and greater variance in nectar volume.
• 3 Although there were significant associations between nectar content and the morphological characters of inflorescences, discriminant function analysis revealed discrimination on the basis of morphology rather than nectar content.
• 4 Visited inflorescences tended to have smaller than average flowers but bees tended to probe the largest flowers on visited inflorescences.
• 5 Choice of flowers within inflorescences is explicable in terms of the relationship between flower size and nectar content.

     

Diversity of inflorescences in the Boutelouinae subtribe (Poaceae: Chloridoideae: Cynodonteae)

The Boutelouinae subtribe is comprised of one monophyletic genus, Bouteloua, with 57 species inhabiting the semi-arid regions of the New World. The inflorescences show significant structural variations, which provides an interesting system to examine their morphological evolution and identify characters and processes that may help to understand the group systematics. The structure of inflorescences was studied in 25 species of Bouteloua. All the species covered under this study have truncated polytelic inflorescences. Structural variations in the inflorescence unit among species may be accounted for by: (1) symmetry of the inflorescence unit, (2) total number of long primary branches, (3) total number of spikelets per branch, (4) number of perfect flowers per spikelet, (5) number of rudimentary flowers, and (6) reproductive system. Homogenization and truncation processes account for the diversity of mature inflorescences that exists in Bouteloua. In this work, we discuss the systematic and taxonomic value of the inflorescence in the Boutelouinae subtribe.     

Chemical Characterization,Antioxidant and Cytotoxic Activities of the Edible Fruits of Brosimun gaudichaudii Trécul,a Native Plant of the Cerrado Biome

In Brazil, there is a large diversity of species of small edible fruits that are considered sources of nutrients and functional properties. They present a high innovation domain for the pharmaceutical, cosmetic and food industries due to their health-promoting properties. Edible fruits from Brosimum gaudichaudii (Moraceae) are widely consumed and used in folk medicine and in feed by the population of the Brazilian Cerrado. Nevertheless, detailed information on the chemical fingerprint, antiradical activity and safety aspects of these fruits is still unknown. Thus, the aim of this work was to investigate the bioactive compounds of hydroethanolic extracts of fruits from Brosimum gaudichaudii using high-performance liquid chromatography combined with mass spectrometry using electrospray ionization (HPLC ESI-MS). Eighteen different compounds, including flavonoids, coumarins, arylbenzofurans, terpenoids, stilbenes, xanthones and esters, were detected. Moreover, the study indicated that the hydroethanolic extract of fruits from B. gaudichaudii presented low scavenging activity against 2,2-diphenyl-1-picrylhydrazyl radicals (IC₅₀>800 μg mL⁻¹) and was cytotoxic (IC₅₀<30 μg mL⁻¹) in Chinese hamster ovary cells (CHO−K1) by an in vitro assay. This is the first report of the chemical profile, antioxidant activity and cytotoxic properties of the hydroethanolic extract of fruits from B. gaudichaudii.     

Thrips pollination of androdioecious Castilla elastica (Moraceae) in a seasonal tropical forest

Androdioecy is a rare sexual system in nature, as predicted theoretically. Among the androecious species reported so far, Castilla elastica (Moraceae) is unique in that flowers are unisexual and staminate and pistillate flowers on cosexual plants are produced on different inflorescences. In addition, inflorescence structure of staminate inflorescences on males and staminate and pistillate inflorescences on cosexes is markedly different. Staminate inflorescences on males are bivalvate, while staminate inflorescences on cosexes are "fig-like" and urceolate. Pistillate inflorescences are discoidal. The difference may reflect different roles and requirements of the three inflorescences in pollination and protection from herbivores. This study reports thrips pollination of C. elastica, demonstrated by a pollinator introduction experiment. Thrips pollination of the species may be an example of mutualism originating from plant-herbivore interactions. In the Moraceae, shifts from simple herbivores on flowers to pollinators might have occurred many times, evolving into diverse pollination systems including the fig-fig wasp mutualism. The family, of which little is known about pollination systems, provides interesting and unique opportunities to study evolution of pollination systems and roles of nonpollinating associates of inflorescences.     

Floral constraint resulting from intersexual mimicry in a gynodioecious fig tree

Fig trees (Ficus: Moraceae) are pollinated by female fig wasps (Agaonidae) whose larvae develop inside galled flowers of unusual inflorescences (figs). Most fig trees also support communities of non‐pollinating fig wasps. Figs of different species display great size variation and contain tens to tens of thousands of flowers. Around one‐half the species of fig trees have the gynodioecious breeding system, where female trees have figs that produce seeds and male trees have figs that support development of pollinators. Mutual mimicry between receptive male and female figs ensures that pollinators enter female figs, even though the insects will die without reproducing, but the need to give no sex‐specific cues to the pollinators may constrain differences in size between receptive male and female figs. We compared relationships between inflorescence size and some measures of reproductive success in male and female figs of Ficus montana grown under controlled conditions in the presence of the pollinator Kradibia tentacularis and its main parasitoid Sycoscapter sp. indesc. Female figs that contained more flowers produced more seeds, but male figs did not increase the production of female pollinator K. tentacularis fig wasps in proportion of the flower number. Although more flowers were galled by the pollinators in male figs containing more female flowers, the high larval mortality caused by parasitism and nutritional limitation prevented the increase in the production of adult female offspring. Selection may favor the increase in flower numbers within figs in female plants of F. montana, but contrarily constrain this attribute in male plants.     

Chaos of Wolbachia Sequences Inside the Compact Fig Syconia of Ficus benjamina (Ficus: Moraceae)

Figs and fig wasps form a peculiar closed community in which the Ficus tree provides a compact syconium (inflorescence) habitat for the lives of a complex assemblage of Chalcidoid insects. These diverse fig wasp species have intimate ecological relationships within the closed world of the fig syconia. Previous surveys of Wolbachia, maternally inherited endosymbiotic bacteria that infect vast numbers of arthropod hosts, showed that fig wasps have some of the highest known incidences of Wolbachia amongst all insects. We ask whether the evolutionary patterns of Wolbachia sequences in this closed syconium community are different from those in the outside world. In the present study, we sampled all 17 fig wasp species living on Ficus benjamina, covering 4 families, 6 subfamilies, and 8 genera of wasps. We made a thorough survey of Wolbachia infection patterns and studied evolutionary patterns in wsp (Wolbachia Surface Protein) sequences. We find evidence for high infection incidences, frequent recombination between Wolbachia strains, and considerable horizontal transfer, suggesting rapid evolution of Wolbachia sequences within the syconium community. Though the fig wasps have relatively limited contact with outside world, Wolbachia may be introduced to the syconium community via horizontal transmission by fig wasps species that have winged males and visit the syconia earlier.     

Papilionoid inflorescences revisited (Leguminosae-Papilionoideae)

Background and Aims

The inflorescence structure determines the spatiotemporal arrangement of the flowers during anthesis and is therefore vital for reproductive success. The Leguminosae are among the largest angiosperm plant families and they include some important crop plants. In papilionoid legumes, the raceme is the most common type of inflorescence. However, a range of other inflorescence types have evolved via various developmental processes. A (re-)investigation of inflorescences in Swainsona formosa, Cicer arietinum, Abrus precatorius, Hardenbergia violacea and Kennedia nigricans leads to new insights into reduction mechanisms and to a new hypothesis on the evolution of the papilionoid pseudoraceme.

Methods

Inflorescence morphology and ontogeny were studied using scanning electron microscopy (SEM).

Key Results

The inflorescence in S. formosa is an umbel with a rare type of pendulum symmetry which may be triggered by the subtending leaf. Inflorescences in C. arietinum are reduced to a single flower. An early formed adaxial bulge is the sterile apex of the inflorescence (i.e. the inflorescence is open and not terminated by a flower). In partial inflorescences of A. precatorius, the axis is reduced and its meristem is relocated towards the main inflorescence. Flower initiation follows a peculiar pendulum pattern. Partial inflorescences in H. violacea and in K. nigricans show reduction tendencies. In both taxa, initiated but early reduced bracteoles are present.

Conclusions

Pendulum symmetry in S. formosa is probably associated with distichous phyllotaxis. In C. arietinum, strong reduction tendencies are revealed. Based on studies of A. precatorius, the papilionoid pseudoraceme is reinterpreted as a compound raceme with condensed lateral axes. From an Abrus-like inflorescence, other types can be derived via reduction of flower number and synchronization of flower development. A plea is made for uniform usage of inflorescence terminology.Key words: Abrus precatorius, Cicer arietinum, Hardenbergia violacea, Kennedia nigricans, inflorescence, Leguminosae, Papilionoideae, pseudoraceme, Swainsona formosa     

Change of Floral Orientation within an Inflorescence Affects Pollinator Behavior and Pollination Efficiency in a Bee-Pollinated Plant,Corydalis sheareri

Vertical raceme or spike inflorescences that are bee-pollinated tend to present their flowers horizontally. Horizontal presentation of flowers is hypothesized to enhance pollinator recognition and pollination precision, and it may also ensure greater consistency of pollinator movement on inflorescences. We tested the hypotheses using bee-pollinated Corydalis sheareri which has erect inflorescences consisting of flowers with horizontal orientation. We altered the orientation of individual flowers and prepared three types of inflorescences: (i) unmanipulated inflorescences with horizontal-facing flowers, (ii) inflorescences with flowers turned upward, and (iii) inflorescences with flowers turned downward. We compared number of inflorescences approached and visited, number of successive probes within an inflorescence, the direction percentage of vertical movement on inflorescences, efficiency of pollen removal and seed production per inflorescence. Deviation from horizontal orientation decreased both approaches and visits by leafcutter bees and bumble bees to inflorescences. Changes in floral orientation increased the proportion of downward movements by leafcutter bees and decreased the consistency of pollinator movement on inflorescences. In addition, pollen removal per visit and seed production per inflorescence also declined with changes of floral orientation. In conclusion, floral orientation seems more or less optimal as regards bee behavior and pollen transfer for Corydalis sheareri. A horizontal orientation may be under selection of pollinators and co-adapt with other aspects of the inflorescence and floral traits.     

Floral display size in comfrey, Symphytum officinale L. (Boraginaceae): relationships with visitation by three bumblebee species and subsequent seed set

The fecundity of insect-pollinated plants may not be linearly related to the number of flowers produced, since floral display will influence pollinator foraging patterns. We may expect more visits to plants with more flowers, but do these large plants receive more or fewer visits per flower than small plants? Do all pollinator species respond in the same way? We would also expect foragers to move less between plants when the number of flowers per plant are large, which may reduce cross-pollination compared to plants with few flowers. We examine the relationships between numbers of inflorescence per plant, bumblebee foraging behaviour and seed set in comfrey, Symphytum officinale, a self-incompatible perennial herb. Bumblebee species differed in their response to the size of floral display. More individuals of Bombus pratorum and the nectar-robbing B.?terrestris were attracted to plants with larger floral displays, but B. pascuorum exhibited no increase in recruitment according to display size. Once attracted, all bee species visited more inflorescences per plant on plants with more inflorescences. Overall the visitation rate per inflorescence and seed set per flower was independent of the number of inflorescences per plant. Variation in seed set was not explained by the numbers of bumblebees attracted or by the number of inflorescences they visited for any bee species. However, the mean seed set per flower (1.18) was far below the maximum possible (4 per flower). We suggest that in this system seed set is not limited by pollination but by other factors, possibly nutritional resources.     

Inflorescences: concepts,function, development and evolution

Background

Inflorescences are complex structures with many functions. At anthesis they present the flowers in ways that allow for the transfer of pollen and optimization of the plant''s reproductive success. During flower and fruit development they provide nutrients to the developing flowers and fruits. At fruit maturity they support the fruits prior to dispersal, and facilitate effective fruit and seed dispersal. From a structural point of view, inflorescences have played important roles in systematic and phylogenetic studies. As functional units they facilitate reproduction, and are largely shaped by natural selection.

Scope

The papers in this Special Issue bridge the gap between structural and functional approaches to inflorescence evolution. They include a literature review of inflorescence function, an experimental study of inflorescences as essential contributors to the display of flowers, and two papers that present new methods and concepts for understanding inflorescence diversity and for dealing with terminological problems. The transient model of inflorescence development is evaluated in an ontogenetic study, and partially supported. Four papers present morphological and ontogenetic studies of inflorescence development in monophyletic groups, and two of these evaluate the usefulness of Hofmeister''s Rule and inhibitory fields to predict inflorescence structure. In the final two papers, Bayesian and Monte-Carlo methods are used to elucidate inflorescence evolution in the Panicoid grasses, and a candidate gene approach is used in an attempt to understand the evolutionary genetics of inflorescence evolution in the genus Cornus (Cornaceae). Taken as a whole, the papers in this issue provide a glimpse of contemporary approaches to the study of the structure, development, and evolution of inflorescences, and suggest fruitful new directions for research.     

INFLORESCENCE TYPES AND FRUITING PATTERNS IN HAMLIN AND VALENCIA ORANGES AND MARSH GRAPEFRUIT

The structural, flowering, and fruit-setting patterns of inflorescences of mature Hamlin and Valencia orange and Marsh grapefruit trees were studied for three years. Several development patterns were found, some of which were relatively consistent for the different varieties or years of study. The sequence of anthesis on an inflorescence was: apical flower first, then basal flower, then the subapical flower. Terminals on which the earlier flowers appeared tended to have more inflorescences than those on which flowers appeared later. Inflorescences on which earlier flowers appeared also produced more flowers than those which began flowering later. Inflorescences that began flowering later were more likely to have leaves or have a greater number of leaves than earlier inflorescences. More than half of the inflorescences carried no leaves, and most of these had one flower. No evidence of a relationship between number of flowers and length of the inflorescence was found. Fruit set occurred primarily during the latter part of the flowering period. Many fruit were set on inflorescences without leaves, but on the basis of percent of flowers setting fruit, inflorescences with leaves were more productive. The greatest fruit set occurred in the subapical position on the inflorescence. With growth changes these fruit often appeared to be developing in the apical position. These patterns generally differed little from year to year. Variations may have been due to the differences in the number of flowers produced by the trees. Results were also similar between Hamlin and Valencia oranges. Patterns on Marsh grapefruit resembled those for the oranges but were frequently less consistent.     

Morphology and anatomy of inflorescence and inflorescence axis in Paepalanthus sect. Diphyomene Ruhland (Eriocaulaceae,Poales) and its taxonomic implications

Paepalanthus sect. Diphyomene has inflorescences arranged in umbels. The underlying bauplan seems however to be more complex and composed of several distinct subunits. Despite appearing superficially very similar, the morphology and anatomy of the inflorescences can supply useful information for the understanding of the phylogeny and taxonomy of the group. Inflorescences of Paepalanthus erectifolius, Paepalanthus flaccidus, Paepalanthus giganteus, and Paepalanthus polycladus were analyzed in regard to branching pattern and anatomy. In P. erectifolius, P. giganteus and P. polycladus the structure is a tribotryum, with terminal dibotryum, and with pherophylls bearing lateral dibotrya. In P. flaccidus, the inflorescence is a pleiobotryum, with terminal subunit, and without pherophylls. Secondary inflorescences may occur in all species without regular pattern. Especially when grown in sites without a pronounced seasonality, the distinction between enrichment zone (part of the same inflorescence) and new inflorescences may be obscured. The main anatomical features supplying diagnostic and phylogenetic information are as follows: (a) in the elongated axis, the thickness of the epidermal cell walls and the cortex size; (b) in the bracts, the quantity of parenchyma cells (c) in the scapes, the shape and the presence of a pith tissue. Therefore, P. sect. Diphyomene can be divided in two groups; group A is represented by P. erectifolius, P. giganteus and P. polycladus, and group B is represented by P. flaccidus. The differentiation is based in both, inflorescence structure and anatomy. Group A presents a life cycle and anatomical features similar to species of Actinocephalus. Molecular trees also point that these two groups are closely related. However, inflorescence morphology and blooming sequence are different. Species of group B present an inflorescence structure and anatomical features shared with many genera and species in Eriocaulaceae. The available molecular and morphology based phylogenies still do not allow a precise allocation of the group in the bulk of basal species of Paepalanthus collocated in P. sect. Variabiles. The characters described and used here supply however important information towards this goal.     

The movement patterns of carpenter beesXylocopa micans and bumblebeesBombus pennsylvanicus onPontederia cordata inflorescences

The movement patterns of carpenter bees (Xylocopa micans) and bumblebees (Bombus pennsylvanicus) foraging for nectar on vertical inflorescences ofPontederia cordata were studied near Miami, Florida. The floral biology ofP. cordata is unique in several ways: (a) many short-lived flowers per inflorescence, (b) constant nectar production throughout the life span of each flower, and (c) abscence of vertical patterning of nectar and age of flowers. Inflorescences ranged between 3.5 and 15.8 cm long and had between 9 and 55 open flowers. Both carpenter bees and bumblebees arrived mostly on the bottom third of the inflorescence and left after visiting flowers on the top third of the inflorescence. The departure position from the inflorescence was higher up than observed in studies of other insect pollinators foraging on other speces of plants. This pattern of departure probably occurs in the absence of a vertical gradient of nectar or floral morphology.     

Culture-Free Survey Reveals Diverse and Distinctive Fungal Communities Associated with Developing Figs (Ficus spp.) in Panama

The ancient association of figs (Ficus spp.) and their pollinating wasps (fig wasps; Chalcidoidea, Hymenoptera) is one of the most interdependent plant–insect mutualisms known. In addition to pollinating wasps, a diverse community of organisms develops within the microcosm of the fig inflorescence and fruit. To better understand the multipartite context of the fig–fig wasp association, we used a culture-free approach to examine fungal communities associated with syconia of six species of Ficus and their pollinating wasps in lowland Panama. Diverse fungi were recovered from surface-sterilized flowers of all Ficus species, including gall- and seed flowers at four developmental stages. Fungal communities in syconia and on pollinating wasps were similar, dominated by diverse and previously unknown Saccharomycotina, and distinct from leaf- and stem endophyte communities in the same region. Before pollination, fungal communities were similar between gall- and seed flowers and among Ficus species. However, fungal communities differed significantly in flowers after pollination vs. before pollination, and between anciently diverged lineages of Ficus with active vs. passive pollination syndromes. Within groups of relatively closely related figs, there was little evidence for strict-sense host specificity between figs and particular fungal species. Instead, mixing of fungal communities among related figs, coupled with evidence for possible transfer by pollinating wasps, is consistent with recent suggestions of pollinator mixing within syconia. In turn, changes in fungal communities during fig development and ripening suggest an unexplored role of yeasts in the context of the fig–pollinator wasp mutualism.