Flowering patterns of long-lived Heliconia inflorescences: implications for visiting and resident nectarivores

Summary Flowering patterns of four Heliconia (Heliconiaceae) species in Trinidad, West Indies were examined for their predictability and availability to the nectarivores that rely on Heliconia floral nectar. Principal flower visitors are trapling hermit hummingbirds; inflorescences are inhabited by nectarivorous hummingbird flower mites that move between inflorescences by riding in the hummingbirds' nares. Heliconia inflorescences flower for 40–200 days, providing long-term sources of copious nectar (30–60 l per flower), but each Heliconia flower lasts only a single day. As an inflorescence ages the interval increases between open flowers within a bract; wet-season inflorescences produce open flowers more slowly than dry-season conspecifics.Estimated daily energy expenditures for hermit hummingbirds demonstrate that slow production of short-lived open flowers plus low inflorescence density preclude territorial defense of Heliconia by the hermits. Heliconia flowering patterns are viewed as a means of (i) regulating reproductive investment by the plants through staggered flower production over long periods of time, and (ii) maintaining outcrossing by necessitating a traplining visitation pattern by its hummingbird pollinators. I suggest that Heliconia exhibit a two-tiered pollination system by using hermit hummingbirds primarily for outcrossing and using hummingbird flower mites primarily for self-pollination.     

Influence of a simulated hurricane on aquatic insect recolonization in the phytotelma of Heliconia caribaea (Heliconiacaea)

Disturbances like hurricanes can affect diversity and community composition, which may in turn affect ecosystem function. We examined how a simulated hurricane disturbance affected insect communities inhabiting the phytotelma (plant-held waters) of Heliconia caribaea in the Luquillo Experimental Forest of eastern Puerto Rico, a tropical island that frequently experiences hurricanes. We hypothesized that disturbance would alter diversity and that larger Heliconia would attract more species following disturbance due to the area-diversity relationship described by the Theory of Island Biogeography. Individual flower parts (bracts) of Heliconia inflorescences (racemes) were artificially disturbed via removal of existing insect communities, then after refilling with water, cohorts of Heliconia were destructively sampled biweekly for 6 weeks to assess recolonization patterns of α (bract level), β, and γ (summed across bracts; raceme level) diversity over time and across raceme sizes. Although we found no support for our hypothesis about the effect of raceme size on recolonization, our hypothesis regarding recolonization patterns over time was supported; species richness, evenness, and abundance of bracts increased directly after the disturbance and then decreased below pre-disturbance levels, and community composition at the raceme level changed significantly over time during recolonization. β Diversity was also greater in smaller racemes compared to larger racemes, suggesting high heterogeneity across bracts of Heliconia racemes exacerbated by raceme size and age. Overall, our results highlight the importance of scale and appropriate measurements of diversity (particularly α) in experiments aiming to extrapolate conclusions about the ecological impacts of disturbances across different habitats and ecosystems.     

Inflorescence bracts of fossil and extant Tilia in North America,Europe, and Asia: patterns of morphologic divergence and biogeographic history

The enlarged inflorescence bract diagnostic of extant Tilia has an extensive Tertiary fossil record in the Northern Hemisphere. Diversity of bract morphology, and the extent of adnation between peduncle and bract, is reviewed for fossil and extant species of Tilia. An extinct type of bract with an orbicular outline and palmate venation is documented by the fossil species Tilia circularis (Chaney) comb. nov. from the early Oligocene of Oregon and is designated Type A. Living species of the genus have elongate bracts with predominately pinnate venation that are borne in two basic configurations: Type B, with the peduncle fused only to the extreme base of the bract lamina, as in extant Tilia endochrysea Hand.-Mzt. of southern China; and Type C with the peduncle fused medially along the basal one-third of the bract lamina, as in most extant species. Bracts of Type B were widely distributed in the Tertiary of western North America (late Eocene to Miocene) and Europe (early Miocene to Pliocene), while those of Type C are known in the fossil condition only from the middle and late Tertiary of Asia and Pliocene of Europe. The bracts of T. circularis, like those of type B, are borne on relatively long stalks and have the peduncle fused only at the extreme base. The fossil record supports recognition of the following characters as apomorphic in Tilia bract evolution: bracts sessile, peduncle adnate to the upper surface of the bract, and pinnate bract venation.     

DFL, a FLORICAULA/LEAFY homologue gene from Dendranthema lavandulifolium is expressed both in the vegetative and reproductive tissues

FLO/LFY homologue genes were initially characterized as floral meristem identity genes and play a key role in flower development among diverse species. The inflorescence organization of chrysanthemum differs from typical dicotyledons such as Arabidopsis and Antirrhinum as clear sepals are absent, and instead, a pappus, a rudimentary sepal, is formed. To understand the mechanism of reproduction of chrysanthemum at the molecular level, DFL, a FLORICAULA/LEAFY homologous gene, was cloned from Dendranthema lavandulifolium, which is one of the original species of chrysanthemum. The DFL gene consists of a 1,236-bp open reading frame and encodes a putative protein of 412 amino acids, which is 63% identical to LFY and 70% to FLO. The expression patterns of DFL during the flower development were analyzed, and RT-PCR results showed that DFL was strongly expressed in the flower bud. In situ hybridization experiments showed that it is strongly expressed in the inflorescence bract, petal and stamen primordial tissues throughout the inflorescence development. Its expression signals were also detected in stems, leaf primordial tissues and developing inflorescence bracts.     

UFO in the Arabidopsis inflorescence apex is required for floral-meristem identity and bract suppression

The UNUSUAL FLORAL ORGANS (UFO) gene of Arabidopsis encodes an F-box protein required for the determination of floral-organ and floral-meristem identity. Mutation of UFO leads to dramatic changes in floral-organ type which are well-characterized whereas inflorescence defects are more subtle and less understood. These defects include an increase in the number of secondary inflorescences, nodes that alternate between forming flowers and secondary inflorescences, and nodes in which a single flower is subtended by a bract. Here, we show how inflorescence defects correlate with the abnormal development of floral primordia and establish a temporal requirement for UFO in this process. At the inflorescence apex of ufo mutants, newly formed primordia are initially bract-like. Expression of the floral-meristem identity genes LFY and AP1 are confined to a relatively small adaxial region of these primordia with expression of the bract-identity marker FIL observed in cells that comprise the balance of the primordia. Proliferation of cells in the adaxial region of these early primordia is delayed by several nodes such that primordia appear “chimeric” at several nodes, having visible floral and bract components. However, by late stage 2 of floral development, growth of the bract generally ceases and is overtaken by development of the floral primordium. This abnormal pattern of floral meristem development is not rescued by expression of UFO from the AP1 promoter, indicating that UFO is required prior to AP1 activation for normal development of floral primordia. We propose that UFO and LFY are jointly required in the inflorescence meristem to both promote floral meristem development and inhibit, in a non-cell autonomous manner, growth of the bract.Shelley R. Hepworth and Jennifer E. Klenz contributed equally to this work.     

INFLORESCENCE AND FLOWER DEVELOPMENT IN THE PIPERACEAE. II. INFLORESCENCE DEVELOPMENT OF PIPER

The inflorescence development of three species of Piper (P. aduncum, P. amalago, and P. marginatum), representing Sections Artanthe and Ottonia, was studied. The spicate inflorescences contain hundreds or even thousands of flowers, depending on the species. Each flower has a tricarpellate syncarpous gynoecium and 4 to 6 free stamens, in the species studied. No sepals or petals are present. In P. marginatum the apical meristem of the inflorescence is zonate in configuration and is unusually elongate: up to 1,170 μm high and up to 480 μm wide during the most active period of organogenesis. Toward the time of apical cessation both height and diameter gradually diminish, leaving an apical residuum which may become an attenuate spine or may be cut off by an abscission zone just below the meristem. The active apex produces bract primordia; when each is 40–55 μm high, a floral apex is initiated in its axil. Both bract and floral apex are initiated by periclinal divisions in cells of the subsurface layer. The bracts undergo differentiation rather early, while the floral apices are still developing. The last-produced bracts near the tip of the inflorescence tend to be sterile.     

Pseudoracemes in papilionoid legumes: their nature, development, and variation

Pseudoracemes in papilionoid legumes: their nature, development, and variation. Cymelike partial inflorescences called fascicles have been reported in the inflorescences of several papilionoid tribes. The total inflorescence is termed a ‘pseudoraceme’ because of the multiple flowers in each bract axil. Pseudoraceme development has been studied in 22 taxa in five papilionoid tribes (Abreae, Desmodieae, Millcttieae, Phaseoleae and Psoraleeae). Two to twelve flowers occur per bract axil among various taxa, with three the most common number.Pongamia pinnata and Clitoris fairchildiana have only two flowers per axil; Vigna radiata, Phaseolus vulgaris, and Apios americana have four to five commonly, and Dioclea aff.ucayalina and Abrus precalorius have up to 12. The ‘fascicle’ usually consists of a triad of three flowers; each triad resembles a dichasial cyme in that the middle flower appears terminal. The middle flower however is subtended by a bract on the abaxial side, so that the middle flower is technically lateral. When the first-order axis elongates, each triad may either remain intact or be separated by axis intervalS. Many variations on the basic triad pattern occur in the species studied: 1.one or two flowers may develop while others that are initiated remain suppressed; 2. Additional flowers may be produced that replicate the first triad; 3. Additional flowers may form medianly only, on the abaxial side. The second-order inflorescence axis which has produced the three flowers persists to produce more flowers in replication of the triad pattern in several taxa (Apios americana, Vigna radiata, Phaseolus vulgaris, and Dioclea aff.ucayalina). In Butea monosperma the second-order inflorescence apex produces subsequent flowers (after the triad) in a helix. In Erylhrina perrieri, there is no indication of a persistent second-order inflorescence apex after the central flower; such a condition could be interpreted as a cyme, except for the abaxial subtending bract. The triad in Psoralea pinnata is a true cyme; the middle flower lacks a subtending bract other than that subtending the entire fascicle. Developmentally, the difference between a cyme and an early-determinate raceme (as in the triad type of pseudoraceme) is rather slight. Comparison of the types of inflorescences described here may indicate how the transition may have occurred between racemes and cymes in the evolution of legumes.     

Distichochlamys rubrostriata (Zingiberaceae), a new species from northern Vietnam

A third species of the until recently monotypic genusDistichochlamys (Zingiberaceae) is described from living and preserved material collected in northern Vietnam.Distichochlamys rubrostriata is distinguished from the original species,D. citrea, and the recently describedD. orlowii, on the basis of leaf, inflorescence bract, lateral staminode, and labellum characters.     

Limonium cedrorum sp. nov. (Plumbaginaceae) from Lebanon

Limonium cedrorum Domina & Ramondo, a new species belonging to the L. palmare aggr., is described and illustrated from the inland near Becharre (Lebanon). Its relationships with morphologically close taxa are discussed. Limonium cedrorum differs from L. sieberi and L. postii mainly by looser inflorescences and larger flowers. It differs from L. galilaeum by longer outer bract and longer scale below the first inflorescence branch, few sterile branches, thicker base of the inflorescence and denser spikes, and from L. graecum by the shape of the inflorescence, longer basal internodes and the shape of the calyx.     

Prototheca associated with banana

Prototheca stagnora was found to be a habitant of older harvested banana (Musa sapientum) and plantain (M. paradisiaca) stumps while P. wickerhamii colonized fresh Musa sp. stumps and flower bract water of Heliconia sp. While Prototheca sp. were known to habituate woody plants, this is the first evidence that herbaceous plants also serve as habitats.     

弯齿盾果草(紫草科)花序及花的形态发生

以弯齿盾果草不同发育时期的花芽为材料,在体视显微镜解剖观察的基础上使用扫描电镜对弯齿盾果草花序、花及果实的发育过程进行了观察。结果显示:(1)弯齿盾果草的花序是由最初的一个球形花序原基经过多次分裂形成的,且花序发生式样符合蝎尾状聚伞花序结构,而非通常所描述的镰状或螺状聚伞花序;花序发生过程中无单一主轴,花序轴是由侧枝连接而成,每一朵花原基有其对应的1枚苞片,下一花原基是从相邻的上一枚苞腋里发生,相邻两花原基交错互生。(2)花器官的发生是按照花萼原基、花冠原基、雄蕊原基和雌蕊原基的顺序发育,但雄蕊原基的花药部分发育速度要比花冠原基快,所以花器官的发育是按照花萼、雄蕊、花冠和雌蕊的顺序发育。(3)子房四深裂结构是由4个原基分别发育,而后相互靠拢而成。(4)小坚果表面的附属结构发生于子房发育后期,其背面的内外层突起分别是由生长较快的外部组织的边缘通过上部内缩和下部向外环状生长形成。     

Pollinator‐mediated selection in a specialized hummingbird–Heliconia system in the Eastern Caribbean

Phenotypic matches between plants and their pollinators often are interpreted as examples of reciprocal selection and adaptation. For the two co‐occurring plant species, Heliconia bihai and H. caribaea in the Eastern Caribbean, we evaluated for five populations over 2 years the strength and direction of natural selection on corolla length and number of bracts per inflorescence. These plant traits correspond closely to the bill lengths and body masses of their primary pollinators, female or male purple‐throated carib hummingbirds (Eulampis jugularis). In H. bihai, directional selection for longer corollas was always significant with the exception of one population in 1 year, whereas selection on bract numbers was rare and found only in one population in 1 year. In contrast, significant directional selection for more bracts per inflorescence occurred in all three populations of the yellow morph and in two populations of the red morph of H. caribaea, whereas significant directional selection on corolla length occurred in only one population of the red morph and one population of the yellow morph. Selection for longer corollas in H. bihai may result from better mechanical fit, and hence pollination, by the long bills of female E. jugularis, their sole pollinator. In contrast, competition between males of E. jugularis for territories may drive selection for more bracts in H. caribaea. Competitive exclusion of female E. jugularis by territorial males also implicates pollinator competition as a possible ecological mechanism for trait diversification in these plants.     

Variability in space and time: contrasting fruit distribution patterns in the deceptive orchid Orchis militaris

• In angiosperms, a decrease in fruit production towards the apex of individual inflorescences is usually observed. Orchids are thought to be primarily pollination‐limited species, and non‐uniform pollination could cause this decrease pattern in several species. Fruit production was investigated in relation to flower position and floral display size in Orchis militaris (Orchidaceae), a deceptive species.
• Over 2 years, eight populations of O. militaris were studied and fruit position along the inflorescence was recorded. Generalised linear models were performed to examine the effect of population, year, flower position and floral display size on fruit production.
• The dominant pattern was characterised by a higher fruit set in the middle part of the inflorescence (parabolic pattern). A non‐directional pattern of fruit production was also detected in some populations. Within a given population, patterns were generally consistent among years. In one of the two study years and in one of the eight populations specifically, the proximal‐to‐distal decrease in fruit production was dramatic in plants with a large floral display but weak or absent in small displays.
• Our study demonstrates the intraspecific diversity of fruit distribution patterns in O. militaris. Non‐uniform pollination along the inflorescence is likely to be responsible for the parabolic pattern, while irregular visitation could explain the non‐directional pattern of fruit production. Pattern variation among years and between populations could arise from spatiotemporal variation in pollinator assemblages. Resource competition effects could explain the interaction effect between display size and flower position.

     

Most organs of sugar-beet (<Emphasis Type="Italic">Beta vulgaris</Emphasis> L.) plants at the vegetative and reproductive stages of development are polysomatic

Polysomaty was studied using flow cytometry in different organs of diploid, triploid and tetraploid sugar-beet (Beta vulgaris L.) plants, in the first (at harvest) and the second (at the height of the blooming period) year of development. Of the organs/parts of organs of the vegetative plant that developed during the first year, only the leaf lamina did not contain endopolyploid cells; in all others, one to three endocycles had occurred. The second-year seed-crop plant was also highly polysomatic; even in reproductive organs such as the flower and pericarp the endopolyploid cells were present (up to 8C and 32C, respectively). At this stage of development no endocycles occurred in the leaf lamina, flower bract, and inflorescence bract. The parts of the plant with no endopolyploid cells are recommended for ploidy estimation, and as a material suitable for micropropagation and genetic manipulations. Endoreduplication, up to 32C (64Cx), was organ-specific and correlated negatively with plant ploidy. The highest mean C-value, over 7, was in the diploid, in the basal part of the oldest leaf petiole in the first-year plant, and in the storage parenchyma of the root in the second-year seed-crop plant. The results confirm that higher endopolyploidy occurs in plants with a smaller 2C DNA amount than in those with a larger one. The significance of endopolyploidization in development of sugar-beet plant organs is discussed.     

Oberonia manipurensis sp. nov. (Orchidaceae) from Manipur,India

A new species Oberonia manipurensis Chowlu, Nanda, A. N. Rao, Angela, Bishwajit & Akimpou sp. nov. (Orchidaceae) is described from Manipur, India. It is closely allied to O. pachyphylla King & Pantl. but differs in longer inflorescence, bilaterally flattened to terete leaves, entire bract, subserrate petals and anther cap with obtuse front margin. The species is described in detail and illustrated with a colour plate. The chromosome number for the species is also reported: 2n = 36.     

FLORAL DEVELOPMENT IN OTTAWA AND FLOREX RED CLOVER TRIFOLIUM PRATENSE (PAPILIONOIDEAE: LEGUMINOSAE)

Floral development in Florex and Ottawa cultivars of red clover (Trifolium pratense L.: Leguminosae) was examined by scanning electron microscopy. No differences between the two cultivars were found. The terminal inflorescence is initiated in the axil of the penultimate bract before the final bract is initiated. After initiation of the final bract, the remnant apical dome is transformed to become the least mature part of the inflorescence dome. Subsequent inflorescences are initiated laterally in basipetal sequence. Inflorescence development is zygomorphic. This leads to an unusual pattern of floret initiation, the oldest florets resting basally and proximal to the penultimate bract. Florets develop with zygomorphic symmetry, each whorl of floral organs developing unidirectionally from the abaxial side. Initiation of the adaxial organ of each whorl is delayed until the abaxial organ of the succeeding whorl has been initiated. Thus there is overlapping development of the whorls of organs. The antepetalous stamens arise in close association with their respective petal primordia. As development proceeds, the corolla tube and the staminal tube exhibit basal zonal growth. In the mature flower, above the distal zone of fusion of the keel petals, marginal cells project and interlock, producing a pollination mechanism that can be sprung by the pollinator.     

Ecological fitting is a sufficient driver of tight interactions between sunbirds and ornithophilous plants

1. Plant–bird pollination interactions evolved independently on different continents. Specific adaptations can lead to their restriction when potential partners from distant evolutionary trajectories come into contact. Alternatively, these interactions can be enabled by convergent evolution and subsequent ecological fitting.
2. We studied the interactions between New World plants from the genus Heliconia, Asian plants of genus Etlingera and African sunbirds on a local farm in Cameroon. Heliconia spp. evolved together with hummingbirds and Etlingera spp. with spiderhunters —an oriental subgroup of the sunbird family.
3. Sunbirds fed on all studied plants and individual plant species were visited by a different sunbird spectrum. We experimentally documented a higher number of germinated pollen grains in sunbird‐visited flowers of Etlingera spp. For Heliconia spp., this experiment was not successful and pollen tubes were rarely observed, even in hand‐pollinated flowers, where enough pollen was deposited. The analyses of contacts with plant reproductive organs nevertheless confirmed that sunbirds are good pollen vectors for both Heliconia and Etlingera species.
4. Our study demonstrated a high ecological fit between actors of distinct evolutionary history and the general validity of bird‐pollination syndrome. We moreover show that trait matching and niche differentiation are important ecological processes also in semi‐artificial plant‐pollinator systems.

     

INFLORESCENCE AND FLORAL DEVELOPMENT IN HOUTTUYNIA CORDATA (SAURURACEAE)

The inflorescence of Houttuynia cordata produces 45–70 sessile bracteate flowers in acropetal succession. The inflorescence apical meristem has a mantle-core configuration and produces “common” or uncommitted primordia, each of which bifurcates to form a floral apex above, a bract primordium below. This pattern of organogenesis is similar to that in another saururaceous plant, Saururus cernuus. Exceptions to this unusual development, however, occur in H. cordata at the beginning of inflorescence activity when four to eight petaloid bract primordia are initiated before the initiation of floral apices in their axils. “Common” primordia also are lacking toward the cessation of inflorescence apical activity in H. cordata when primordia become bracts which may precede the initiation of an axillary floral apex. Many of these last-formed bracts are sterile. The inflorescence terminates with maturation of the meristem as an apical residuum. No terminal flowers or terminal gynoecia were found, although subterminal gynoecia or flowers in subterminal position may overtop the actual apex and obscure it. Individual flowers have a tricarpellate syncarpous gynoecium and three stamens adnate to the carpels; petals and sepals are lacking. The order of succession of organs is: two lateral stamens, median stamen, two lateral carpels, median carpel. The three carpel primordia almost immediately are elevated as part of a gynoecial ring by zonal growth of the receptacle below the attachment of the carpels. The same growth elevates the stamen bases so that they appear adnate to the carpels. The trimerous condition in Houttuynia is the result of paired or solitary initiations rather than trimerous whorls. Symmetry is bilateral and zygomorphic rather than radial. No evidence of spiral arrangement in the flower was found.     

Anther development, microsporogenesis and microgametogenesis in Heliconia (Heliconiaceae, Zingiberales)

Anther development, microsporogenesis and microgametogenesis in several species of Heliconia were investigated as part of a complementary embryological study of the Heliconiaceae. All studied Heliconia species present bithecate and tetrasporangiate anthers with fertile pollen grains; only H. rivularis, a natural hybrid, presented sterile pollen grains of variable size and no content. The anther wall has an uniseriate epidermis and endothecium, the latter with helicoidal thickenings, although some cells of the middle layers also showed thickenings; the biseriate tapetum is of amoeboid non-syncytial type, since the tapetum cells did not fuse together forming a true plasmodium. The microsporogenesis is successive leading to isobilateral tetrads. The inaperturate pollen grains had a very reduced exine consisting of a thin, more or less continuous layer with small spines upon; the pollen grain shape is variable among the species, all of them presenting heteropolar pollen, except H. angusta with isopolar ones. Most of these characteristics were shared with other studied Zingiberales, although more studies need to be done.