Morphology and morphogenesis of ensiform leaves, syndesmy of shoots and an understanding of the thalloid plant body in species of Apinagia, Mourera and Marathrum (Podostemaceae)

The flattened, irregularly shaped and lobed or dissected leaves of Apinagia riedelii , A. latifolia , A. goejei , Mourera aspera and Marathrum utile (subfamily Podostemoideae) are ensiform in structure. After the typical bifacial inception, further growth of leaves proceeds in the midrib area, i.e. in the median plane of the leaf. The lower leaf zone is characterized by a sheath that orientates 'at the side of the blade', i.e. at the adaxial edge of the sword-like leaf. The ensiform blades are lobed, incised or pinnately dissected with the tips terminated in elongated threads or thin filaments. Leaves of Apinagia riedelii resemble pinnately dissected compound leaves. The dissected structure represents a secondary superimposition of the ensiform shape and a parallel development to compound leaves. It is interpreted as an adaptation to the rapid current, established in the floating shoots of these aquatic plants. The basal portions of main shoots and successive branches are fused due to a retarded separation. Fusion of this kind has been termed a syndesmy. The fused region of shoots is superseded by the fusion of the lower leaf zones of (distichously positioned) adjacent leaves, occurring at their margins. The fused leaf bases form a cavity for the terminal flower bud of each shoot and cover it in the form of a hood. The flower buds are hidden from external view. The meristematic growing zones are thus protected and enclosed within the syndesmic plant body which, in this way, attains the 'thalloid' appearance especially developed in Apinagia goejei and A. latifolia but also present in the other species. The results of this study enable an understanding of the particular appearance of these Podostemoideae as modifications of the typical structures according to the 'principle of variable proportions'.  © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society , 2005, 147 , 47–71.     

The ramification of Apinagia riedelii: A key to the understanding of the plant architecture of Podostemaceae,subfamily Podostemoideae

The study of the ramification pattern of Apinagia riedelii results in a new concept of the architecture of this species, with general implications to members of subfamily Podostemoideae with dithecous leaves. The presence of a subtending leaf below the floriferous shoot proves axillary branching also for species with dithecous leaves. Previous opinions of an unusual ramification mode by subfoliar or non-axillary branching or stem bifurcation in combination with dithecous leaves hitherto pleaded for Podostemoideae is refuted. Moreover, the view of the so-called dithecous leaves with one sheath (theca) at the ventral and one at the dorsal side of the leaf, previously regarded as initially connected with branching, has to be changed. The dithecous leaf arises from the branch and not from the mother shoot axis – as previously believed – and represents the addorsed hypsophyll, i.e., the first leaf (prophyll) of the floriferous branch. This finding leads to the conclusion that the lower sheath of the dithecous leaf is the ventral (not dorsal) sheath pointing to the branch and surrounding its flower bud with a ligule or an ochrea and a hood upon the bud. In this way, the branch and its flower bud become seemingly sunk in the leaf base. At the fusion of leaf basis and shoot results this enigmatic common tissue. The wings of the dorsal (upper) sheath of the dithecous leaf point to the mother shoot axis of the branch. Successive floriferous branches along the main stem disclose the shoot axis of A. riedelii as a monopodium (not sympodium) that develops an anthocladial (foliated) inflorescence in the form of a botrys or a compound botrys, respectively. Since it is generally difficult to define cymose or racemose inflorescences if subtending leaves are absent – which occur in most other species of subfamily Podostemoideae with dithecous leaves – the nature of these inflorescences is discussed anew. The findings on A. riedelii have consequences on our comprehension of the shoot architecture of Podostemoideae.     

Enigmatic morphology of Djinga felicis (Podostemaceae – Podostemoideae), a badly known endemic from northwestern Cameroon

Djinga is a monotypic genus restricted to the Cameroon Ridge (‘Dorsale Camerounaise’) of NW Cameroon. Besides the type locality Mount Djinga (Adamawa Province, near Tignère), it also grows in waterfalls near Mount Oku (NW Province). This paper describes the structure and development of Djinga felicis using scanning electron microscopy and microtome sections. Cusset's protologue is enriched considerably. Roots are green, dorsiventrally flattened and adherent to submerged rocks. They are broad ribbons or crusts (up to 1 cm broad) which branch exogenously. Root‐borne shoots (up to 17 cm) have filamentous leaves with sheaths and (occasionally) attached stipules. Flowers are borne as part of reproductive short shoots which arise exogenously along the stems and endogenously along the roots. Djinga shows non‐axillary stem branching. Reproductive shoots along the main stem usually stay short. They arise from the abaxial side of double‐sheathed leaves, a key innovation of Podostemoideae. These short shoots shift into pocket‐like stem positions clearly below their associated leaves. Each flower bud inside a spathella is erect, but with an inclined ovary. The flowers are unistaminate with a broad connective. Unlike many other Podostemoideae, the tricolpate pollen grains are arranged in both dyads and monads. The ovary is globular and unilocular. The mature 8‐ribbed capsule dehisces by two slightly unequal valves, releasing 40–50 seeds. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 160 , 64–81.     

Molecular phylogenetic analysis of Podostemaceae: implications for taxonomy of major groups

The river‐weed family Podostemaceae (c. 300 species in c. 54 genera) shows a number of morphological innovations to be adapted to its unusual aquatic habitat, and its unique or rare bauplan features have been reflected in the traditional (i.e. non‐molecular) classification recognizing numerous monotypic or oligospecific genera. The infrasubfamilial relationships of many genera remained unclear. The present study used molecular phylogenetic analysis of matK sequences for 657 samples (c. 132 species/c. 43 genera). The family was traditionally divided into three subfamilies (Podostemoideae, Tristichoideae and Weddellinoideae). American Podostemoideae were shown to be polyphyletic and divided into four clades, i.e. Ceratolacis, Diamantina, Podostemum and all other genera. Among the podostemoid clades, Diamantina was the first branching clade and a clade comprising Mourera and the Apinagia subclade was then sister to the remainder of the New World and Old World Podostemoideae with low statistic supports. The Old World Podostemoideae comprised four monophyletic clades, i.e. two African clades, one Madagascan clade and one Asian clade, although the relationships among these clades and American Ceratolacis and Podostemum were poorly resolved. African Podostemoideae were polyphyletic, with Saxicolella pro parte being weakly supported as sister to the remaining Old World Podostemoideae plus Ceratolacis and Podostemum. In contrast to the American and African clades, monophyly of four Asian subclades was well supported. Plants of Tristicha (Tristichoideae) and of Weddellina (Weddellinoideae), which are currently treated as monospecific, had great matK differentiation equivalent to at least interspecific variation. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169 , 461–492.     

Development of leaves and shoot apex protection in Metrodorea and related species (Rutaceae)

Most members of Sapindales are characterized by compound leaves, but several genera also (or only) produce simple or unifoliolate leaves. A few genera may bear stipules or pseudostipules. Little is known about the morphological structure and morphogenesis of these types of leaves in Sapindales, but this information is required for comparative and evolutionary studies. Metrodorea is a Neotropical genus of Rutaceae, comprising species presenting compound and unifoliolate leaves, plus heterophylly, together with an intriguing bud‐protecting structure at the leaf base. The aims of the present study are: (1) to examine leaf morphogenesis in Metrodorea and in closely related species (four Esenbeckia spp., Helietta apiculata and Raulinoa echinata); and (2) to improve our understanding of the morphological evolution of leaves in Metrodorea and Rutaceae. Our data show that the hood‐shaped structure at the base of the leaf in Metrodorea, usually interpreted as a sheath, is, in fact, a pair of united stipules, a synapomorphy of the genus. In the species studied, it is possible to recognize two main types of unifoliolate leaf: early unifoliolate leaves and late unifoliolate leaves. We also found that the number of leaflets in the studied species is dependent on the late or early determination of the leaf primordium, and that loss of leaflets may have been favoured by the restriction of space available for development within the cavity formed by the pair of united stipules. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178 , 267–282.     

Development of the floral shoot and pre‐anthesis cleistogamy in Hydrobryopsis sessilis (Podostemaceae)

The reproductive biology of Hydrobryopsis sessilis (Podostemaceae, subfamily Podostemoideae), a reduced, threatened, aquatic angiosperm endemic to the Western Ghats of India, was examined. This is the first report on the transition from the vegetative to the reproductive phase in this plant, describing floral ontogeny, pollination and the breeding system. The cytohistological zonation of the apical meristem of the reproductive thallus is identical to that of the apical meristem of the vegetative thallus. The floral shoots do not replace vegetative shoots (i.e. the vegetative shoots never bear flowers), but form at new sites at the tip of the flattened plant body. Each floral shoot meristem is tiny, deep‐seated and concave and arises endogenously following lysigeny. The floral shoot meristem gives rise to four to six bracts in a distichous manner. The development of spathe, stamens and carpels is described. The ab initio dorsiventrality of the carpels and the occurrence of endothelium in the ovules are reported. The mature stigmas and anthers lie close to each other. The pollen germinates within undehisced anthers and the pollen tubes enter the stigmas in the unopened floral bud, leading to pre‐anthesis, complete, constitutional cleistogamy under water. The seed set is 63.2%. A significant finding is the penetration of several pollen tubes into the filaments of stamens in 16% of the flower buds, indicating a trend towards cryptic self‐fertilization. The Indian Podostemoideae appear to show a shift from xenogamy or geitonogamy or autogamy in a chasmogamous flower to complete autogamy in a cleistogamous flower. The floral modifications leading to cleistogamy in H. sessilis have been identified. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159 , 222–236.     

The architecture of Zeylanidium olivaceum (Podostemaceae) inferred from the structure of the primary shoots

Zeylanidium olivaceum (Podostemaceae-Podostemoideae) is the only crustose-rooted species of the genus that still develops prominent primary shoots from the seedling in addition to the secondary (root-borne) shoots forming the clonal plant body. The primary shoots are articulated into an up to 8.5 cm long and 4 mm thick stalk (hypocotyl) and a copiously foliated paint-brush-like shoot which is sympodially branched in the form of a helicoid cyme. The helicoid branching pattern indicates a transversal prophyll position, typical of the dicotyledons, but replaced in most other Podostemoideae by a median prophyll position. The short stems within the leafy head do not separate, but are fused to a dense aggregate (coenosome). Branches are mainly vegetative with a rosette of about 20 elongate subulate leaves. The primary shoots branch in the vegetative stage and thus differ from other Podostemoideae where ramification is confined to the floriferous shoots. The leaves adhere together at the base, forming an apical furrow-like hollow surrounding the shoot tip. The tiny shoot apex is one-layered, radially symmetrical, and develops leaf primordia in a decussate pattern. The erect primary shoots thus differ from the distichously foliated plagiotropic secondary shoots by the decussate phyllotaxis, and by the presence of more than 20 leaves on a shoot as compared to the about six leaves on the vegetative and floriferous secondary shoots. The features observed in the primary shoots are interpreted as primitive as compared to those of the secondary shoots. Z. olivaceum is thus characterised by heterobathmy, i.e., the occurrence of plesiomorphic (primary shoots) and apomorphic features (secondary shoots). The primary shoots exhibit primitive features that apparently have been lost in secondary and primary shoots of most other members of subfamily Podostemoideae.     

Multivariate analysis of morphological and anatomical characters of Calophyllum (Calophyllaceae) in South America

Calophyllum (Calophyllaceae), previously placed in Clusiaceae, is easily recognizable by its opposite entire leaves with close parallel venation alternating with resin canals. However, distinction between species has been difficult, because of infraspecific variation in tepal and stamen number and resemblance among species that share similar habitats. Here, I report the results of multivariate analyses of morphological and anatomical characters for Calophyllum in South America, and provide a taxonomic treatment for the genus in South America, the first since that of Vesque in 1893. Thirteen preliminary morphogroups were identified. Thirty‐two morphological characters of the leaf, flower and fruit from 401 specimens, and 17 anatomical leaf characters from 45 specimens were measured and analysed using principal component analyses (PCAs) and discriminant analyses (DAs). PCAs were used to find groups and DAs were used to validate those PCAs that were potential groups. Two main subgroups were identified in the general analysis. Subgroup M1 has terete stems and smaller leaves and flowers than subgroup M2, which, instead, has quadrangular stems. Only subgroup M2 showed distinctive clusters in regional and local analyses. Distinctive clusters and morphological and anatomical characters helped us to recognize four species in South America, including a new species, Calophyllum pubescens sp. nov. . In addition, a new species, Calophyllum mesoamericanum sp. nov. , is described from Central America. © 2013 The Linnean Society of London,     

Shoot anatomy and secretory structures in Hypericum species (Hypericaceae)

The anatomy and ultrastructure of internodes, leaves and petals were compared in Hypericum elegans, H. inodorum, H. olympicum, H. forrestii and two genotypes of H. perforatum. Internode anatomy was variable between species with respect to the structure of the cortical and pith parenchyma, including the presence of secretory reservoirs. Also, the secondary growth was more extensive in shrubs, i.e. H. inodorum and H. forrestii. In leaves, phloem secretory reservoirs were formed in all species, mesophyll secretory reservoirs were absent only in H. elegans and internal nodules were present only in H. elegans and H. perforatum. The petals differed between species in the mesophyll structure and the occurrence and location of secretory structures. The phloem secretory reservoirs lacked sheaths, whereas these were distinct in the mesophyll reservoirs. Other ultrastructural traits of the reservoirs were similar in all the species studied, with the exception of the leucoplast ultrastructure. In internal nodules, the inner cells vs. sheath cells differed in the number of vesicles and other membranous structures and plastid ultrastructure. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163 , 70–86.     

Leaf epidermal micromorphology of Cercis (Fabaceae: Caesalpinioideae)

The micromorphology of leaf epidermal cells and stomata of all eight species and one form (11 samples) of Cercis were observed by scanning electron microscopy and light microscopy. Both the adaxial and abaxial epidermal cells are polygonal or irregular in shape; the anticlinal walls are straight and arched or undulate. Two types of stomata, which occur only on the abaxial surface of the leaves, are found in the genus. The atypical paracytic type is present in only one species, Cercis chingii, and the anomocytic type is present in all other species. Interspecific differences are minor in the genus with regard to leaf epidermal characters, except for C. chingii, which is characterized by atypical paracytic‐type stomata, a two‐lipped outer stomatal rim, the highest stomatal density and undulate and densely pitted anticlinal walls in the adaxial epidermis. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 158 , 539–547.     

A cladistic analysis of the Stygnicranainae Roewer, 1913 (Arachnida,Opiliones, Cranaidae) – where do longipalp cranaids belong?

A character survey compiling the morphological information of the subfamily Stygnicranainae was carried out. Two new species of Stygnicranaus Roewer, 1913 are described from Colombia and the new genus Agathocranaus is described from Ecuador. All known species of the subfamily are included in a matrix of 46 morphological characters. Parsimony analysis under implied weights recovered a monophyletic Stygnicranainae including Tryferos Roewer, 1931 plus Stygnicranaus and Agathocranaus. However, the usage of the four subfamilies of Cranaidae as currently defined is abandoned because the two largest subfamilies of Cranaidae – Cranainae and Prostygninae – represent paraphyletic groups (grades), whereas Heterocranainae is a superfluous subfamily, including only the genus Heterocranaus Roewer, 1913. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 157 , 470–494.     

Microspore development in Podostemaceae-Podostemoideae, with implications on the characterization of the subfamilies

Subfamilies Podostemoideae and Tristichoideae of the aquatic flowering plant family Podostemaceae are conventionally characterized by a different mode of microsporogenesis. Simultaneous meiotic division into the four microspores is found in Tristichoideae, successive meiotic division is said to be typical of Podostemoideae. In contrast, the results of the present study reveal that in subfamily Podostemoideae both modes of microsporogenesis occur. This is exemplified by the early pollen development of two neotropical species: Apinagia latifolia and Marathrum rubrum. Successive versus simultaneous meiotic cytokinesis are thus not differential characters of the two subfamilies. It is worthy to note that successive cytokinesis occurs in a family (Podostemaceae) of the Eudicots which are characterized by simultaneous cytokinesis. The occurrence of Ubisch bodies (orbicules) in several species of Apinagia and Marathrum parallels the echinate ornamentation of the pollen grains.     

Comparative anatomy of root meristem and root cap in some species of Podostemaceae and the evolution of root dorsiventrality

In the unusual aquatic Podostemaceae, the root is the leading organ of the plant body and is variously compressed and submerged as it adheres to rock surfaces in rapid water. In an anatomical comparison of the root apical meristems and root caps of 33 species that represent the major lineages of the family, the dorsiventrality of root meristems varied and was classified into four patterns: (1) The root cap is produced outward from a nearly radially symmetrical meristem. (2) The meristem and root cap are markedly dorsiventral; the outermost cells of the hood-shaped cap are acroscopic derivatives from bifacial initials on the ventral side, while the pattern on the dorsal side is similar to pattern 1. (3) Bifacial initials are on both the dorsal and ventral sides. (4) No root cap is present. An evolutionary polarity may be evident from pattern 1 to 2 and then to 3. Pattern 2 arose in the early evolution of the subfamily Podostemoideae and subsequently, pattern 3 arose in species with crustose roots, while the least specialized pattern 1 is retained in Tristichoideae and Weddellinoideae. Pattern 4 characterized by caplessness may have appeared recurrently in Tristichoideae and Podostemoideae. These evolutionary changes in the meristem preceded the specialization of external root morphologies.     

Powdering of egg nests with brochosomes and related sexual dimorphism in leafhoppers (Hemiptera: Cicadellidae)

Leafhoppers from 16 New World genera currently placed in the tribes Proconiini (13) and Cicadellini (2) of the subfamily Cicadellinae, in the subfamily Phereurhininae (1), and one undescribed genus exhibit a suite of morphological specializations associated with a unique type of maternal care. The females produce a specific type of brochosomes (secretory particles manufactured in the Malpighian tubules of most leafhoppers and usually forming a non‐sex‐specific hydrophobic coating of the integument), which they store prior to oviposition on their forewings in the form of pellets and then apply as a powdery coating to the egg clusters placed under the epidermis of leaves or, in one genus, exposed. The function of the brochosome coating is unknown, but may include protection of eggs against parasitoids and pathogens, and facilitating gas exchange. Observations on several species from the genera Phera, Homalodisca, Oncometopia, Quichira, Cuerna, and the undescribed genus are reported, complementing scanty existing data on this behaviour. Its taxonomic occurrence is described for the first time based on study of collections, where ready‐to‐oviposit females are occasionally preserved with pellets of brochosomes on their forewings. A comprehensive survey of associated female‐specific structural modifications is presented based on examination of c. 80 predominantly Neotropical species. These modifications include (1) production of modified brochosomes (2) modified setation of the forewing area upon which pellets of such brochosomes are placed, and (3) elongation of the metathoracic tibial macrosetae, which transfer the brochosomes onto the egg nest. The traits are absent or rudimentary in males. The specialized brochosomes display remarkable interspecific diversity and can be used for taxonomic identification of eggs. Egg‐powdering apparently has evolved as a modification of the anointing and grooming behaviours involved in making coatings of integumental brochosomes in most leafhoppers. Morphological similarity, extending to characters not related to oviposition, suggests that all genera containing ‘powdering’ species may form a single lineage, but this hypothesis yet needs to be tested by phylogenetic analyses. Several such genera include species displaying powdering‐associated traits and species lacking these, suggesting multiple independent losses or origins of powdering. This peculiar kind of maternal care provides an interesting model for study of the evolution of novel functional complexes of traits. © 2004 The Linnean Society of London, Zoological Journal of the Linnean Society, 2004, 140 , 353–381.     

Leaf epidermal features of Lithocarpus (Fagaceae) from China and their systematic significance

The leaves of 52 species of Lithocarpus in China were studied. The adaxial leaf epidermis was investigated by light microscopy. Epidermal cells of the adaxial surface were classified into three types on the basis of the outline of their anticlinal walls, i.e. sinuate, straight and curved. The abaxial leaf epidermis was investigated by light microscopy and scanning electron microscopy. The following types of trichome were observed: appressed parallel tuft, stellate, fused stellate, papillae, stipitate fasciculate, solitary unicellular, appressed laterally attached unicellular, curly thin‐walled unicellular, bulbous and thin‐walled peltate. The fused stellate, appressed laterally attached unicellular and curly thin‐walled unicellular trichomes were reported in Lithocarpus for the first time. The appressed parallel tuft trichome, which is recognized as a salient characteristic of Lithocarpus, was not found in 15 species. A cladistic analysis was performed on the basis of the leaf epidermal features. According to the leaf epidermal features and several morphological characteristics, 26 of the 52 species could be divided into seven groups. Similar groups can be found in Barnett's and Camus' systems. The trichomes of four genera in Fagaceae are listed and compared. Lithocarpus had 14 types of trichome, 11 of which were identical to types found in Quercus, more than in Castanopsis and Cyclobalanopsis. The evolutionary trends of trichomes in Fagaceae are discussed and a new point of view is raised. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168 , 216–228.     

The shoot apex of Podostemaceae: De novo structure or reduction of the conventional type?

The paper reviews and discusses various interpretations of the shoot apex of Podostemaceae with special reference to subfamily Podostemoideae. Main questions concern (1) the proposed absence of a shoot apical meristem (SAM) in apical “meristemless” shoot tips of Podostemoideae and, as the consequence, the endogenous inception of leaf-borne leaves and branches and (2) the predicted stem bifurcation below a “terminal” dithecous (double-sheathed) leaf positioned instead of a shoot apex, as it is reported for subfamily Podostemoideae. Does the “meristemless” shoot apex represent a true evolutionary novelty? Does the view of stem bifurcation represent a new ramification pattern with the consequence that the “classical root–shoot model” of angiosperms is not valid for Podostemaceae? Both interpretations do not conform to previous studies that are complemented here by new data on the SAM of Zeylanidium olivaceum and Thelethylax minutiflora (Podostemoideae). Although a SAM is difficult to observe in the vegetative shoots of many Podostemoideae, it becomes well visible when the shoot passes into the flowering stage approaching the conspicuous shoot apex of floriferous shoots. The arguments of the absence of a SAM in vegetative shoots are not convincing and the endogenous origin of “leaf-borne leaves” appears questionable. Consequently, the “meristemless” shoot apex cannot be considered as a structure having evolved de novo. In the less advanced subfamilies Tristichoideae and Weddellinoideae, the leaf primordia develop only from a few apical cells of the outer shoot layer. This allows the conclusion that the surface layer of the apex in these subfamilies corresponds to the horizontally spread single-layered apical meristem of subfamily Podostemoideae. Similarly, the view of shoot bifurcation does not conform to the diachsial–sympodial branching pattern occurring in the cymose inflorescences of many Podostemoideae. This fact contradicts the presence of a terminal leaf.     

The effect of shade on leaf structure and physiology of tree seedlings from a mixed dipterocarp forest

This study builds upon past work investigating seedling leaf physiology and structure among tropical trees. We seek to explain how related and unrelated species and genera co‐occur in relation to varying amounts of shade. Seedlings of eight Sri Lankan rain forest tree species in three genera (Dipterocarpus, Mesua, Shorea section Doona) were grown for 2 years in four treatments that simulated a variety of shade environments across the understorey of a rain forest. All three genera comprise major canopy tree species of mixed dipterocarp forest, a widespread and important Asian tropical forest type. Compared with the other genera, Dipterocarpus spp. had the largest leaves, the thinnest leaf blades and relatively high rates of stomatal conductivity across all shade treatments, making them water‐loving species sensitive to droughty soils. Mesua spp. had intermediate sized leaves, with the thickest leaf blades and palisade mesophyll layers, the highest stomatal densities, the smallest aperture sizes and the lowest rates of stomatal conductance, making them the most water conservative. Shorea spp. were generally intermediate in blade and palisade mesophyll dimensions between Dipterocarpus spp. and Mesua spp., but they had the smallest leaves. Greater differences among genera than among species within genera were apparent, but species differences within genera were also apparent. Differences among genera and species conform to their known successional status and topographical affinities and provide a more comprehensive understanding of species site adaptation. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 167 , 332–343.