Pollination Chamber Research Articles

Nectary and elaiophore work together in flowers of Xylopia aromatica (Annonaceae): structure indicates a role in pollination

Secretory structures that produce floral rewards have rarely been reported for Annonaceae. We identified a glandular region in Xylopia aromatica (Lam.) Mart., which consisted of a nectary and an elaiophore. This study aimed to describe the structure and secretory process of these glandular structures, which are highly correlated with the reproductive biology of this species. Anatomical and ultrastructural studies were performed prior to and during anthesis, focusing on the channel and pollination chamber. The floral nectary is placed in the roof of the chamber. It has a secretory epidermis and subglandular parenchyma and is immediately contiguous with the elaiophore, a portion that delimits the pollination channel and produces lipids. The release of nectar begins in the pistillate phase, while the elaiophore starts secreting prior to anthesis, both of which finishing during the staminate phase. Lipids form a sticky layer covering the channel surface, which provides access to the chamber. The cell machinery of the epidermis for both nectary and elaiophore is highly correlated with the exudates, despite their highly similar structure. Nectar attracts pollinators to the pollination chamber, whereas lipids seem to act in pollen adhesion to the body of pollinators. Both of exudates appear to act in complementary ways during pollination.

Nutritious tissue in petals of Annonaceae and its function in pollination by scarab beetles

ABSTRACT The feeding of pollinating dynastid-scarab beetles on nutritious tissue of Annonaceae flowers results in macroscopically visible gnawing marks on petals. In the present paper, we present and discuss examples of such gnawing marks on Annonaceae from the Cerrado and the Amazon Forest in Brazil. The localization of gnawing marks on the petals and the histochemistry of the nutritious tissues are emphasized. In some species, nutritious tissue is apparently distributed among all petals, while in other species it is more or less diffusely localized. There are also cases in which nutritious tissue occurs only on clearly localized regions of the inner petals. Petals of selected Amazon species were stained, and studied by light and scanning electron microscopy. The nutritious tissue consists of cells with mucilage-rich walls, which contain starch, lipids and/or tannins. Starch and lipids are not only energy-rich food for the beetles but are apparently also “fuel” for metabolic heating of the flowers, which is a further benefit for the pollinators inside the pollination chamber.

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

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

Notes on the floral anatomy of Deeringothamnus Small (Annonaceae): cortical vascular systems in a chaotic pattern

Floral anatomy of Deeringothamnus Small, an endemic and endangered annonaceous genus from Florida comprising 2 species, was studied. It is mainly distinguished by missing any sclerenchyma at anthesis – apart from anthers – and by a chaotic vasculature exhibiting a partial perianth-stamen cortical vascular system, appearing as an over-evolution of the pattern previously described in the neighbouring Asimina and other paracarpous and pseudosyncarpous genera. Such a pattern is amazingly similar to that previously recognized in the most basal annonaceaous genera, as e.g. Ambavia, and might be considered as a reversion to an ancestral state. These alterations toward decrease are related to the receptacle flatness and lack of pollination chamber, and seem parallel with the dwarf habit of this genus.

The reproductive biology of the early-divergent genus Anaxagorea (Annonaceae), and its significance for the evolutionary development of the family

Data of six studied Neotropical Anaxagorea species are analyzed and discussed with respect to the population structure, flowering phenology, flower morphology, anthesis, scent emission, thermogenesis, floral visitors, breeding system, fruit-set and seed dispersal. The probably reason for the patchy distribution of small populations of Anaxagorea species within lowland tropical forests is given. A novel explanation of the functional significance of ruminate endosperm is presented. Flowering of the species follows either the annual or the continuous flowering pattern. All studied species have diurnal, two-day lasting, protogynous anthesis; several species have thermogenic flowers. Self-compatibility appears to be the prevailing reproductive system in the genus. However, there is a strong tendency for effecting cross-pollination. Floral scent of Anaxagorea species contains fruit-like components, and the pollinators, primarily Nitidulidae (Colopterus spp.) are attracted by deceit. Strong scenting pollination chambers occur also in most other cantharophilous Annonaceae. Novel floral developments are apparent mainly in fly-, cockroach- and bee-pollinated Annonaceae, which have patterns different from cantharophilous species and exhibit open flowers with reflexed petals, which allow their pollinators to reach and touch the reproductive organs.

Phylogenetic Reconstruction, Morphological Diversification and Generic Delimitation of Disepalum (Annonaceae)

Taxonomic delimitation of Disepalum (Annonaceae) is contentious, with some researchers favoring a narrow circumscription following segregation of the genus Enicosanthellum. We reconstruct the phylogeny of Disepalum and related taxa based on four chloroplast and two nuclear DNA regions as a framework for clarifying taxonomic delimitation and assessing evolutionary transitions in key morphological characters. Maximum parsimony, maximum likelihood and Bayesian methods resulted in a consistent, well-resolved and strongly supported topology. Disepalum s.l. is monophyletic and strongly supported, with Disepalum s.str. and Enicosanthellum retrieved as sister groups. Although this topology is consistent with both taxonomic delimitations, the distribution of morphological synapomorphies provides greater support for the inclusion of Enicosanthellum within Disepalum s.l. We propose a novel infrageneric classification with two subgenera. Subgen. Disepalum (= Disepalum s.str.) is supported by numerous synapomorphies, including the reduction of the calyx to two sepals and connation of petals. Subgen. Enicosanthellum lacks obvious morphological synapomorphies, but possesses several diagnostic characters (symplesiomorphies), including a trimerous calyx and free petals in two whorls. We evaluate changes in petal morphology in relation to hypotheses of the genetic control of floral development and suggest that the compression of two petal whorls into one and the associated fusion of contiguous petals may be associated with the loss of the pollination chamber, which in turn may be associated with a shift in primary pollinator. We also suggest that the formation of pollen octads may be selectively advantageous when pollinator visits are infrequent, although this would only be applicable if multiple ovules could be fertilized by each octad; since the flowers are apocarpous, this would require an extragynoecial compitum to enable intercarpellary growth of pollen tubes. We furthermore infer that the monocarp fruit stalks are likely to have evolved independently from those in other Annonaceae genera and may facilitate effective dispersal by providing a color contrast within the fruit.

Evolutionary steps in the reproductive biology of Annonaceae

Flowers of Annonaceae are characterized by fleshy petals, many stamens with hard connective shields and numerous carpels with sessile stigmas often covered by sticky secretions. The petals of many representatives during anthesis form a closed pollination chamber. Protogynous dichogamy with strong scent emissions especially during the pistillate stage is a character of nearly all species. Scent emissions can be enhanced by thermogenesis. The prevailing reproductive system in the family seems to be self-compatibility. The basal genus Anaxagorea besides exhibiting several ancestral morphological characters has also many characters which reappear in other genera. Strong fruit-like scents consisting of fruit-esters and alcohols mainly attract small fruit-beetles (genus Colopterus, Nitidulidae) as pollinators, as well as several other beetles (Curculionidae, Chrysomelidae) and fruit-flies (Drosophilidae), which themselves gnaw on the thick petals or their larvae are petal or ovule predators. The flowers and the thick petals are thus a floral brood substrate for the visitors and the thick petals of Anaxagorea have to be interpreted as an antipredator structure. Another function of the closed thick petals is the production of heat by accumulated starch, which enhances scent emission and provides a warm shelter for the attracted beetles. Insight into floral characters and floral ecology of Anaxagorea, the sister group of the rest of the Annonaceae, is particularly important for understanding functional evolution and diversification of the family as a whole. As beetle pollination (cantharophily) is plesiomorphic in Anaxagorea and in Annonaceae, characters associated with beetle pollination appear imprinted in members of the whole family. Pollination by beetles (cantharophily) is the predominant mode of the majority of species worldwide. Examples are given of diurnal representatives (e.g., Guatteria, Duguetia, Annona) which function on the basis of fruit-imitating flowers attracting mainly fruit-inhabiting nitidulid beetles, as well as nocturnal species (e.g., large-flowered Annona and Duguetia species), which additionally to most of the diurnal species exhibit strong flower warming and provide very thick petal tissues for the voracious dynastid scarab beetles (Dynastinae, Scarabaeidae). Further examples will show that a few Annonaceae have adapted in their pollination also to thrips, flies, cockroaches and even bees. Although this non-beetle pollinated species have adapted in flower structure and scent compounds to their respective insects, they still retain some of the specialized cantharophilous characters of their ancestors.

A novel pollination mode, saprocantharophily, in Duguetia cadaverica (Annonaceae): A stinkhorn (Phallales) flower mimic

Duguetia cadaverica (Annonaceae), a small understory tree of humid primary forest from the Guianas to Pará state, Brazil, unites several unusual blossom and floral characters such as flagelliflory and putrid-smelling flowers, respectively. The few pollination studies conducted in the large genus Duguetia have shown that species are usually cantharophilous, pollinated by either small (mostly Nitidulidae) or large specialized dynastid (Scarabaeidae) beetles. Foul-smelling flowers are a novelty within the genus, and to better understand their significance, we undertook a study of the reproductive biology and flower scent chemistry of D. cadaverica. In a primary forest of French Guiana, we observed and measured morphology and phenology of trees and flowers; additionally, flower pollination chamber temperature was measured and insect visitors to flowers observed. Flower scent was collected in situ and later analyzed in the laboratory by GC–MS. Flowers are visited by small beetles of a single Pycnocnemus species (Nitidulidae), which are the only insects observed to enter the pollination chamber. Moreover, flowers evince a rhythm in sexual stage, scent emission and temperature, which finds correspondence in behavioral characters of the putative nitidulid pollinator, such as timing of entry and exit from the pollination chamber. Floral scent analysis revealed an unusual, previously undescribed combination of chemical odor classes. The earthy, rank flower scent contained 18 compounds, among them fatty acid derivatives, terpenoids and N- and S-bearing compounds. The most abundant volatiles were 1-octen-3-ol, 3-octanone, and (E)-2-octenol, which are characteristic earthy odors of fungi; additionally, there were sulfides and 4-methylpentanoic acid, which are molecules associated with carcass and cheese odors, respectively.Saprocantharophily, discovered in Duguetia cadaverica, is a novel pollination mode for Annonaceae. The beetle pollinator Pycnocnemus sp., which belongs to the Oxycnemus genus complex having fungal hosts of the order Phallales, appears to visit the flowers through deception. This extraordinary pollination system, whereby flowers mimic olfactory and visual cues of fungi, is rare and previously only known from three angiosperm families (Araceae, Aristolochiaceae and Orchidaceae) wherein the pollinators were flies.

A plastid DNA phylogeny ofDasymaschalon(Annonaceae) and allied genera: Evidence for generic non–monophyly and the parallel evolutionary loss of inner petals

AbstractDasymaschalonand the closely related generaDesmos, FriesodielsiaandMonanthotaxistogether comprise ca. 170 species of trees, shrubs and woody climbers distributed in tropical Africa and tropical Asia. These genera form the desmoid clade, which, because of the presence of diverse flower and fruit syndromes including different types of pollination chambers and moniliform monocarps, offers an opportunity to investigate potentially ecologically significant shifts in flower and fruit characters. Despite its morphological diversity, however, generic delimitation within the desmoid clade is problematic and the intergeneric relationships of the constituent genera are only poorly understood. Bayesian, maximum likelihood and maximum parsimony analyses of plastid DNA sequence data (matK, psbA–trnH, ndhF, rbcL, trnL–F; ca. 5.4 kb; 52 taxa) were used to clarify phylogenetic relationships within the desmoid clade. The evolution and taxonomic utility of selected fruit and flower characters was investigated with likelihood and parsimony ancestral character reconstructions. The results indicate problems in the current delimitations ofDasymaschalonandFriesodielsia. Friesodielsiaas currently circumscribed is polyphyletic, with AfricanFriesodielsiaspecies allied to the African genusMonanthotaxis, and only distantly related to Asian representatives. The majority ofDasymaschalonspecies form a strongly supported clade, but three species are more closely related to Asian species ofFriesodielsia. Ancestral character reconstructions indicate that seed number and monocarp shape are of limited value in generic circumscriptions, and that the three–petalled corolla characteristic ofDasymaschalonevolved independently twice within the desmoid clade. Disruptions to homeotic gene expression or strong selective pressure for a partial enclosure of the mature stamens and carpels by the corolla are hypothesised to underlie the parallel evolution of pollination chambers formed by outer petal homologues subsequent to inner petal loss.

How diverse are Annonaceae with regard to pollination?

Studies during the last decades on representatives of Annonaceae have revealed their diversification with regard to pollination. Examples are given of species pollinated by beetles (cantharophily), which is the predominant mode of the majority of species worldwide, by small or large beetles (both groups having either diurnal or nocturnal flowers with or without thermogenesis), species pollinated by thrips (Thysanoptera), flies (myiophily and sapromyiophily), cockroaches and even bees (melittophily). Adaptational features of floral structures are compared with the behaviour of flower visitors, emphasizing floral rhythm, flower size, petal thickness, stamen structure and odour production. Anaxagorea, the earliest divergent surviving genus in Annonaceae, exhibits floral characters thought to be basal for the family: tissue-rich thick petals that form a pollination chamber; several Anaxagorea spp. exhibit thermogenesis, emit a fruit-like odour and attract small beetles as pollinators. As cantharophily is plesiomorphic in Anaxagorea and in Annonaceae, characters associated with beetle pollination appear imprinted in members of the whole family. Even non-cantharophilous species retain one or more characteristic features of beetle-pollinated species, such as thick petals, flattened and sclerified connective shields or protogynous dichogamy. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169, 245–261.

First records of flower biology and pollination in African Annonaceae: Isolona, Piptostigma, Uvariodendron, Monodora and Uvariopsis

Seven species from five genera of Annonaceae were studied with regard to their flower biology and pollination in the Southwest Province of Cameroon, West Africa. They have protogynous hermaphroditic flowers, with exception of Uvariopsis species, which are monoecious. Fused petals of Isolona campanulata remain apically spreading and open during anthesis but form a deep basal urceolate tube around the reproductive organs. At anthesis the yellow pendent flowers emit a fruit-like scent and attracted small beetles, the likely pollinators. Piptostigma sp. flowers also emit a fruit-like scent but provide a closed pollination chamber formed by the three inner petals. Small staphylinid beetles attracted during the female stage of anthesis are released from the flowers at the end of the male stage 2–3 days later. Both species have diurnal anthesis, attracting and releasing the flower visitors during daytime. In contrast, Uvariodendron connivens and U. calophyllum have nocturnal anthesis with floral thermogenesis, produce spicy, aromatic and fruity scents and attract large Scarabaeidae beetles, the pollinators, along with many curculionid beetles, which were principally predators of the thick petals. The very large flowers of Monodora tenuifolia have yellowish petals which are spotted with dark red markings. Together with the sweetish, slightly disagreeable scent the flowers attract flies, principally dung flies. The two investigated Uvariopsis species are monoecious with pistillate and staminate flowers being functional at the same time. The violet red flowers of U. bakeriana visually seem to mimic the fruiting body of certain stinkhorn fungi (Phallaceae) although without producing their strong unpleasant carcass stench. Flower-visiting dung flies were rare. Conversely, U. congolana has a strong fungus-like scent, its flowers are presented at litter height and dung flies living in the litter were the flower visitors, albeit sporadic. The 4–5 days lasting anthesis of both Uvariopsis species appears to be an evolutionary consequence of their diffuse pollinator spectra. The studied African Annonaceae therefore have either cantharophilous or myiophilous/sapromyiophilous flowers with, in part, respectively, remarkably long anthesis, thermogenesis, and widely open, large flowers – all attributes unknown or rare in the hitherto better studied Neotropical Annonaceae.

Heterodichogamy and nitidulid beetle pollination in Anaxagorea prinoides, an early divergent Annonaceae

Heterodichogamy in a natural population of an Annonaceae species from the rainforests of French Guiana is described for the first time. Anaxagorea prinoides had bisexual flowers and two floral morphs within the studied population were protogynous. The population under study comprised 7 mature trees belonging to one morph and 12 to the other. Statistical analyses showed that the two morphs were in a 50:50% ratio, and therefore the temporal sexual pattern of heterodichogamy is given. When anthesis of flowers in the male stage ended in one morph, anthesis started with flowers in the female stage in the complementary morph. Approximately 1 h before the end of anthesis in one morph, flowers of the reciprocal morph started to emit a fruit-like scent. The temporal separation of the female and the male stages of the two different morphs lasted only approximately 1 h. Six of the seven identified compounds in the banana-like floral scent were esters and one was an alcohol. The main compounds examined are known to be components of fruit scents. Nitidulidae beetles of the genus Colopterus were the pollinators of A. prinoides and during flowering were maintained within the population of this species. This was not only due to the fact that the beetles remained sheltered in the pollination chamber of the flowers, but also because upon release from individuals of male-stage flowers at the end of flower anthesis they were attracted by the odoriferous female-stage flowers of other individuals of the same population. Heterodichogamy of A. prinoides appears to be a means by which reproductive success is augmented. Attraction of beetle pollinators by “fruit-imitating” floral scent is not restricted to species of Anaxagorea, but occurs in many representatives of the Annonaceae.

Floral evolution in the Annonaceae: hypotheses of homeotic mutations and functional convergence

The recent publication of hypotheses explaining the homeotic control of floral organ identity together with the availability of increasingly comprehensive and well-resolved molecular phylogenies presents an ideal opportunity for reassessing current knowledge of floral diversity and evolution in the Annonaceae. This review summarizes currently available information on selected aspects of floral structure and function, including: changes in the number of perianth whorls and the number of perianth parts per whorl; the evolution of sympetaly; the diversity and evolution of pollination chambers (with a novel classification of seven main structural forms of floral chamber based on the different arrangement, size and shape of petals); the evolution of perianth glands; floral unisexuality and hypotheses explaining the unexpectedly high frequency of occurrence of androdioecy; the origin and possible function of inner and outer staminodes; the evolution of stamen connective diversity and theca septation; and the origin of 'true' syncarpy and functionally equivalent extragynoecial compita. In each case, current ideas on the origin, evolution and function are discussed. The information presented in this review enables two main conclusions to be drawn. The first is that changes in the homeotic control of floral organ identity may have had a profound impact on floral structure in several disparate lineages in the family. This is most obvious in Fenerivia, in which a centrifugal shift of floral organ identity has occurred, and in Dasymaschalon, in which a reverse (centripetal) shift has occurred. Other genera that have gained or lost entire perianth whorls are likely to have undergone similar homeotic changes. Attention is also drawn to the extensive functional convergence in Annonaceae flowers, with widespread homoplasy in many characters that have previously been emphasized in higher-level classifications.

The Genus Dasymaschalon (Annonaceae) in Thailand

A comprehensive taxonomic revision of the genus Dasymaschalon (Annonaceae) in Thailand is presented. Twelve species are recognized, including five that are newly described and one new nomenclatural combination, viz. D. acuminatum sp. nov., D. angustifolium sp. nov., D. dasymaschalum, D. echinatum sp. nov., D. filipes, D. glaucum, D. grandiflorum sp. nov., D. lomentaceum, D. macrocalyx, D. obtusipetalum sp. nov., D. sootepense, and D. wallichii comb. nov. Previous taxonomic confusion regarding the relationship between Dasymaschalon and Desmos is discussed. The most significant diagnostic difference between the two genera is the number and arrangement of petals: Dasymaschalon species have only three petals (homologous with the outer whorl of other Annonaceae) that are apically connivent to form an enclosed pollination chamber, whereas Desmos species have two whorls of three petals which are basally constricted and apically free.

Reproductive Biology of Two Sympatric Species of Polyalthia (Annonaceae) in Sri Lanka. I. Pollination by Curculionid Beetles

The pollination biology of two sympatric species, Polyalthia coffeoides and Polyalthia korinti (Annonaceae), is described in detail. An Endaeus species (Coleoptera: Curculionidae) is shown to be the major pollinator of both species, with Carpophilus plagiatipennis (Coleoptera: Nitidulidae) as the secondary pollinator of P. coffeoides. Both Polyalthia species show intrafloral dichogamy (protogyny) with a reproductively inactive phase between the pistillate and staminate phases, although there is no evidence of interfloral dichogamy. A pollination chamber is formed by the inner petals throughout the reproductively active phases. Thermogenesis occurs in P. korinti, with internal floral temperatures up to 6°C above ambient levels. The heat is presumably an energy reward for the beetles. Although most pollination systems are regarded as diversified and opportunistic, specialized pollination systems are typical of the Annonaceae. Although P. coffeoides and P. korinti have overlapping distributions, habitats, and flowering seasons and share the same pollinators, the extent of competition for pollinators is likely to be lessened due to the abundance and nonspecificity of the beetles.

An Examination of the Reproductive Biology of Telopea speciosissima (Proteaceae) with Emphasis on the Nature of Protandry and the Role of Self‐Pollination in Fruit Set

Aspects of the reproductive biology of the waratah Telopea speciosissima R.Br. were studied under controlled conditions using large, pot‐grown plants. One to 2 d prior to perianth opening, anthers dehisced in a circle of clumps onto the pollen presenter around the oval stigmatic groove (pollination chamber). This deposition pattern may lead to a degree of autogamous pollination. Pollen viability, measured by fluorescence microscopy (fluorescein diacetate), was at a maximum of 90% at perianth opening, decreasing to less than 50% after 8 d. Some viable pollen (ca. 10%) was detected up to 19 d after perianth opening. The timing of stigma receptivity was determined by esterase activity, by examination of pollen‐tube growth using fluorescence microscopy, and by visual inspection of the stigma using SEM. The stigma was receptive at perianth opening and up to ca. 9 d after. Although peak stigma receptivity occurred at 2 d and up to 7 d postperianth opening, this species may be considered only weakly protandrous and essentially homogamous, as pollen was generally viable throughout the entire period. Two days following self‐ or cross‐pollination, pollen tubes had grown through the pollination chamber and could be seen just entering the upper style. By 8 d, some pollen tubes were observed in the ovary area in self‐ and cross‐pollen treatments. Proportionally, more cross‐pollinated pistils had pollen tubes growing through to the ovary than self‐pollinated pistils. Manual pollen removal resulted in greater growth of self‐pollen tubes when compared with self‐pollen that was left intact on the flower. This indicates that either the stigma was stimulated by pollen removal or that pollen was pushed down into the stigmatic groove into closer contact with stigmatic surfaces. Despite the presence of pollen tubes in all parts of the pistil and the early growth of a small number of fruits in self‐pollinated treatments, only cross‐pollinated treatments resulted in mature fruits containing viable seeds. This evidence confirms late‐acting gametophytically controlled self‐incompatibility as the main nonvector mechanism for outbreeding in this species.

Morphological and Functional Flower Characteristics of New and Old World Annonaceae with Respect to Their Mode of Pollination

The Annonaceae show a broader flower biological radiation than originally thought, with flowers being pollinated not only by beetles, but also by thrips, flies and even bees. The majority of species have hermaphroditic protogynous flowers. Species with white or yellowish-white, small, delicate, day-active flowers, may be pollinated either solely by thrips, or by thrips and small beetles (e.g., species of Bocageopsis, Oxandra, Xylopia). Several of these thrips-pollinated species have stamens with an elongated, tongue-like connective. Pollination by flies is not well documented for American species, notwithstanding it appears to be more common in Old World species, e.g., in the genus Pseuduvaria. The mitriform flowers exhale an unpleasant smell, produce nectar in purple-colored petal glands and have a sapromyiophilous syndrome. Flies enter the flower center through large openings between the inner petals. Beetle-pollinated Annonaceae have flowers with comparatively thick and, often, fleshy petals, which, during anthesis frequently form a pollination chamber with the petals inclining over the flower center. The stamens usually have peltate connective shields, probably a device for protection against voracious beetles. Some cantharophilous species have flowers which are day-active while others are night-active. When they are in their pistillate phase, the beetles are attracted by characteristic odor components. They enter the pollination chamber and usually remain in the interior of the flower until the flower has changed to its staminate phase, when pollen is shed and afterwards petals and stamens detach. Two lines of cantharophilous Annonaceae are recognizable on the basis of present knowledge. Species with smaller and more delicate flowers are pollinated by small beetles (Nitidulidae, Curculionidae, Chrysomelidae and Staphylinidae), whereas species with large, more robust flowers in the Neotropics are pollinated by large beetles of the family Scarabaeidae, subfamily Dynastinae. Some species of the cantharophilous Annonaceae, especially the large-flowered ones, but also some species with smaller flowers, produce heat during anthesis (thermogenesis). Food bodies, developed on the adaxial surfaces or sides of the petals, provide unique nourishment possibilities for beetles when they stay inside the flowers during the pistillate phase. In the staminate stage of the flower, after pollen is shed, beetles also feed on pollen. Apparently, no dynastid-flower relationship has evolved in Asia and Australia. Pollination by bees was discovered recently in Unonopsis guatterioides in Amazonia and Uvaria concava in North Queensland: the first by scent-collecting euglossine males and the second by pollen-collecting Meliponinae. The general trends in morphological/functional floral characteristics in the family are discussed in a presumptive phylogenetic context.

Morphological and functional flower characteristics of New and Old World Annonaceae with respect to their mode of pollination

The Annonaceae show a broader flower biological radiation than originally thought, with flowers being pollinated not only by beetles, but also by thrips, flies and even bees. The majority of species have hermaphroditic protogynous flowers. Species with white or yellowish‐white, small, delicate, day‐active flowers, may be pollinated either solely by thrips, or by thrips and small beetles (e.g., species of Bocageopsis, Oxandra, Xylopia). Several of these thrips‐pollinated species have stamens with an elongated, tongue‐like connective. Pollination by flies is not well documented for American species, notwithstanding it appears to be more common in Old World species, e.g., in the genus Pseuduvaria. The mitriform flowers exhale an unpleasant smell, produce nectar in purple‐colored petal glands and have a sapromyiophilous syndrome. Flies enter the flower center through large openings between the inner petals. Beetle‐pollinated Annonaceae have flowers with comparatively thick and, often, fleshy petals, which, during anthesis frequently form a pollination chamber with the petals inclining over the flower center. The stamens usually have peltate connective shields, probably a device for protection against voracious beetles. Some cantharophilous species have flowers which are day‐active while others are night‐active. When they are in their pistillate phase, the beetles are attracted by characteristic odor components. They enter the pollination chamber and usually remain in the interior of the flower until the flower has changed to its staminate phase, when pollen is shed and afterwards petals and stamens detach. Two lines of cantharophilous Annonaceae are recognizable on the basis of present knowledge. Species with smaller and more delicate flowers are pollinated by small beetles (Nitidulidae, Curculionidae, Chrysomelidae and Staphylinidae), whereas species with large, more robust flowers in the Neotropics are pollinated by large beetles of the family Scarabaeidae, subfamily Dynastinae. Some species of the cantharophilous Annonaceae, especially the large‐flowered ones, but also some species with smaller flowers, produce heat during anthesis (thermogenesis). Food bodies, developed on the adaxial surfaces or sides of the petals, provide unique nourishment possibilities for beetles when they stay inside the flowers during the pistillate phase. In the staminate stage of the flower, after pollen is shed, beetles also feed on pollen. Apparently, no dynastid‐flower relationship has evolved in Asia and Australia. Pollination by bees was discovered recently in Unonopsis guatterioides in Amazonia and Uvaria concava in North Queensland: the first by scent‐collecting euglossine males and the second by pollen‐collecting Meliponinae. The general trends in morphological/functional floral characteristics in the family are discussed in a presumptive phylogenetic context.

Pollination and evolution in neotropical Annonaceae

AbstractThe most prominent pollination mode in neotropical Annonaceae is pollination by beetles. Flowers are protogynous and have fruity, spicy or unpleasant odors. The floral chambers, formed by the petals closing over the flower center, emit these specific odors which entice the beetles to enter the flowers. There, the beetles are sheltered from daylight and predators and encounter food (tissues and pollen) as well as opportunities for mating. The amount of food offered, the thickness of the petal tissue and the dimension of the flowers increases with size, number and voraciousness of the attracted beetles. Three main groups of beetle‐pollinated Annonaceae can be distinguished. Two of them have relatively small floral chambers, exhibit diurnal and/or nocturnal anthesis and are visited and pollinated by relatively small beetles (Nitidulidae, Curculionidae, Chrysomelidae). Large flowers with a large pollination chamber and very thick petals are associated with nocturnally active, large and voracious dynastid scarab beetles, which are attracted by strong odors promoted principally by thermogenetic processes of the flowers during the time of the beetles’ main activity. The dynastid beetle‐pollinated species appear to have the most adapted and most specialized flower characteristics in the Annonaceae. Some small‐flowered Annonaceae are pollinated by thrips and, for a few species, pollination by flies is suspected. Some genera, such as Guatteria, are uniform with respect to flower biology and seem to have adapted principally to nitidulids as pollinators. In contrast, the genus Annona, basically a group pollinated by dynastid beetles, is diversified with respect to flower morphology and pollination. The neotropical Annonaceae as a whole may have started as a group pollinated by sucking and pollen‐eating Thysanoptera and non‐destructive beetle groups. Species pollinated by such Thysanoptera and/or rove beetles (Staphylinidae) still show the laminar, plesiomorphic stamen type of Annonaceae with a tongue‐shaped connective prolongation. The disc‐like sclerified connective shield of the majority of Annonaceae is apparently a secondary and modified structure, especially prominent in the beetle‐pollinated species. The densely aggregated stamens with their connective shield appear to be a kind of antipredator structure in Annonaceae adapted to pollination by beetles.

The Proteaceous Pistil: Morphological and Anatomical Aspects of the Pollen Presenter and Style of Eight Species Across Five Genera

The morphology and anatomy of pollen presenters, styles and pollen of species ofBanksia, Dryandra, Hakea, IsopogonandMacadamiawere studied. Serial sections of pistils and SEM images of pollen were quantified to determine whether the low fertility observed in the Proteaceae has a structural basis. Pollen access to the stigma was investigated. There were three types of stigmatic cavity. A groove in which the stigmatic papillae were enclosed was present inDryandra, BanksiaandHakea. Macadamiahad a groove with protruding papillae, andIsopogonhad a tube which enclosed the papillae. Anatomical studies showed the pollen presenter to be structurally complex but overall to have similar internal anatomy across the species studied. The species could be grouped according to presence or absence of transfer tissue and presence or absence of sclerenchyma, but these groups were not mutually exclusive. In the pistil there were three structural filters to pollen tube passage. The first was at the stigma, where pollen grain access could be limited by the diameter or length of the stigmatic groove or the capacity of the pollination chamber in relation to pollen volume. The second and third related to a narrowing of the transmitting tissue tract within the pollen presenter and in the lower style which could influence pollen tube passage to the ovule.