Nectar-carbohydrate production and composition vary in relation to nectary anatomy and location within individual flowers of several species of Brassicaceae

Nectar-carbohydrate production and composition were investigated by high-performance liquid chromatography and enzymology in nine species from five tribes of the Brassicaceae. In six species (Arabidopsis thaliana (L.) Heynh., Brassica napus L., B. rapa L., Lobularia maritima (L.) Desv., Raphanus sativus L., Sinapis arvensis L.) that produced nectar from both lateral nectaries (associated with the short stamens) and median nectaries (outside the long stamens), on average 95% of the total nectar carbohydrate was collected from the lateral ones. Nectar from these glands possessed a higher glucose/fructose ratio (usually 1.0–1.2) than that from the median nectaries (0.2–0.9) within the same flower. Comparatively little sucrose was detected in any nectar samples except from Matthiola bicornus (Sibth. et Sm.) DC., which possessed lateral nectaries only and produced a sucrose-dominant exudate. The anatomy of the nectarial tissue in nectar-secreting flowers of six species, Hesperis matronalis L., L. maritima, M. bicornus, R. sativus, S. arvensis, and Sisymbrium loeselii L., was studied by light and scanning-electron microscopy. Phloem alone supplied the nectaries. However, in accordance with their overall nectar-carbohydrate production, the lateral glands received relatively rich quantities of phloem that penetrated far into the glandular tissue, whereas median glands were supplied with phloem that often barely innervated them. All nectarial tissue possessed modified stomata (with the exception of the median glands of S. loeselii, which did not produce nectar); further evidence was gathered to indicate that these structures do not regulate nectar flow by guard-cell movements. The numbers of modified stomata per gland showed no relation to nectar-carbohydrate production. Taken together, the data on nectar biochemistry and nectary anatomy indicate the existence of two distinct nectary types in those Brassicacean species that possess both lateral and median nectaries, regardless of whether nectarial tissue is united around the entire receptacle or not. It is proposed that the term “nectarium” be used to represent collectively the multiple nectaries that can be found in individual flowers. Received: 21 July 1997 / Accepted: 19 September 1997     

EXTRAFLORAL NECTAR OF FEROCACTUS ACANTHODES (CACTACEAE): COMPOSITION AND ITS IMPORTANCE TO ANTS

Ants are attracted to extrafloral nectaries subtending reproductive organs of Ferocactus acanthodes var. lecontei (Cactaceae) in central Arizona. Extrafloral nectar produced by these glands contained amino acids, sugars, and water. Nectar quality and composition varied temporally in relation to plant reproductive phenology. The number of nectar glands on a barrel cactus did not change significantly, however; the mass of nectar produced per gland increased significantly with immature fruit production. Of the three sugars present in extrafloral nectar (fructose, glucose, and sucrose), only glucose occurred at a higher concentration in June, when immature fruits first appeared on barrel cactus. Amino acid concentration and composition in extrafloral nectar of barrel cactus did not change significantly over time. Ant density on barrel cactus increased significantly from mid-May to mid-June at two field sites. Water availability per nectar gland increased 158% from May to June. Water plays an important role in attracting ants to barrel cacti.     

Evolution of a unique seed maturity pattern in Croton bonplandianum Baill strengthens ant-plant mutualism for seed dispersal

Summary The female flowers of Croton bonplandianum bear nectar glands which become active during fruit maturation and attain peak activity just prior to the splitting of fruits. This temporal specificity of nectar gland activity is shown to facilitate seed dispersal by ants, which are attracted to the plant only during the fruit maturation period. The nectar glands establish a nectar influence zone with a radius of 60 cm around the plant within which seed dispersal by ants is effective. Seed dispersal by ants is facilitated only if the seeds are placed within this nectar influence zone. This is accomplished by an intriguing evolutionary shift in the maturation pattern of the fruits. Unlike the usual acropetal development, fruit maturation in Croton is temporally asymmetrical, with the fruits nearer the parental axis maturing early. This unique pattern of fruit development together with the polychasial branching system leads to a concentration of seeds within the nectar influence zone and enhances seed dispersal by ants. The proximate factors responsible for this asynchronous fruit maturity were investigated.     

MORPHOLOGICAL STUDIES OF THE NYMPHAEACEAE. XII. THE FLORAL BIOLOGY OF CABOMBA CAROLINIANA

Observations have been made on the pollination ecology of Cabomba caroliniana Gray in Texas. Flowers are trimerous with morphologically similar perianth parts. The adaxial corolla spurs are nectariferous and attract small Diptera (e.g. Notiphila cressoni and Hydrellia bilobifera). Anthesis occurs for 2 consecutive days with flowers opening about 10:00 a.m. and closing around 4 p.m. on each day. First-day flowers have short, indehiscent stamens and longer pollen-receptive stigmata which arch outward over the nectaries. In 2nd-day flowers the stamens have elongated to the level of the stigmata and extrorse dehiscense occurs above the nectaries. Stigmata of 2nd-day flowers are pressed together at the center of the flower and are nonreceptive to pollen. Insects attracted to 2nd-day flowers in search of nectar become dusted with pollen (due to the position and extrorse dehiscence of the anthers) and as insects fly to 1st-day flowers, achieve cross-pollination by virtue of the stigmata position over the nectaries. Seed anatomy is similar to that of other nymphaeaceous genera (i.e., abundant perisperm, little cellular endosperm, a haustorial nucellar “tube,” and a small dicotyledonous embryo). Pollination morphology and comparative xylem anatomy support the segregation of Cabomba from the Nymphaeaceae, sensu stricto. The anatomical correlations between seeds and the myophilous pollination syndrome (found elsewhere in Nymphaeaceae, sensu lato), however, suggest a phyletic relationship.     

DEVELOPMENT AND VASCULATURE OF THE FLOWERS OF LOPHOTOCARPUS CALYCINUS AND SAGITTARIA LATIFOLIA (ALISMACEAE)

The development of the bisexual flower of Lophotocarpus calycinus and of the unisexual flowers of Sagittaria latifolia has been observed. In all eases floral organs arise in acropetal succession. In L. calycinus, after initiation of the perianth, the first whorl of stamens to form consists of six stamens and is ordinarily followed by two alternating whorls of six stamens each. The very numerous carpels arc initiated spirally. In the male flower of S. latifolia the androecium develops in spiral order. A few rudimentary carpels appear near the floral apex after initiation of the stamens. There are no staminodia. The female flower has a similar developmental pattern to that of Lophotocarpus except that a prominent residual floral apex is left bare of carpels. The vascular system in all flowers is semiopen, with vascular bundles passing to the floral organs in a pattern unrelated to the relative positions of those organs. The androecia of these two taxa are similar to those of some Butomaceae and relationships based on ontogeny and morphology are suggested. The gynoecia are meristically less specialized but morphologically more specialized than the gynoecia of Butomaceae.     

COMPARATIVE REPRODUCTIVE BIOLOGY OF HERMAPHRODITIC AND MALE-STERILE IRIS DOUGLASIANA HERB. (IRIDACEAE)

A comparative study of the reproductive biology of male-sterile and hermaphroditic plants in a gynodioecious population of Iris douglasiana Herb. (Iridaceae) was conducted at the University of California's Marine Laboratory at Bodega Bay, California, between 1976–1979. Each year of the study, there were 11.1% male-sterile plants in the population, some of which began blooming at the same time as the earliest blooming hermaphrodites. Male-sterile flowers made up between 7–21% of the flowers produced during the male-sterile flowering period. Male-sterile flowers had smaller sepals and petals than hermaphrodites, there were fewer of them per square meter, and they had fewer pollinated stigmas than did hermaphroditic flowers. In a test to determine pollinator preference, intact hermaphroditic flowers tended to have more pollinated stigmas than did hermaphrodites with their stamens removed or those flowers with shortened sepals made to resemble the smaller male-sterile flowers. Floral phenology and nectar-flow patterns were similar in both types of flowers as were the kinds of amino acids and sugar rewards in the nectar. Male-sterile flowers, however, produced much less nectar per flower. There were no significant differences in the number of ovules per flower or the number of seeds produced per capsule between the two flower types, but the loss of seeds through larval predation was much greater in capsules from hermaphroditic flowers. Early flowering and setting of seed by plants with male-sterile flowers could give them a reproductive advantage over plants with hermaphroditic flowers which experience higher levels of larval predation later in the growing season.     

STUDIES ON THE POLLINATION ECOLOGY OF TIPULARIA DISCOLOR (ORCHIDACEAE)

Tipularia discolor, a woodland orchid, flowers in mid-summer when reproductive activity is minimal within the herb synusia. Tipularia is insect-pollinated, and artificial crosses showed that seeds are produced after self-pollination, intra-inflorescence pollination, and outcrossing. The single nocturnal pollinator, Pseudaletia unipuncta (Noctuidae), located Tipularia populations within a day or two of anthesis. Pollinators were shown to be capable of utilizing portions of the inflorescences that contained the most nectar. After total nectar resources declined, pollinators were no longer active on the inflorescences, even though flowers and nectar were still available. The mode of pollinator activity seems to be closely related to floral morphology, although the moths are able, early in the flowering phenophase, to successfully obtain nectar without effecting any change in the reproductive status of flowers.     

INITIATION AND DEVELOPMENT OF INFLORESCENCE AND FLOWER IN ANEMOPSIS CALIFORNICA (SAURURACEAE)

All flowers of Anemopsis californica, the most specialized taxon of the family Saururaceae, are initiated as individual primordia subtended by previously initiated bracts, in contrast to the common-primordium initiation of all flowers of Saururus cernuus and of most flowers of Houttuynia cordata. Floral symmetry is bilateral and zygomorphic, and the sequence of initiation among floral parts is paired or whorled. In A. californica, the six stamens arise as three common primordia, each of which later bifurcates to form a pair. The three common primordia occupy sites corresponding to the positions of the three stamens in H. cordata flowers. In Anemopsis, the filaments of each pair are connate. Each stamen pair is vascularized by a single bifurcating vascular bundle. The three carpels per flower are usually initiated simultaneously although there may be some variation. Adnation between stamens and carpels results from zonal growth. Downward extension of the locule, and proliferation and expansion of receptacular tissue and inflorescence cortical tissue around the locule below the bases of the carpels produce the inferior ovary. The inflorescence terminates its activity as a flattened apical residuum, surrounded by bracts subtending reduced flowers most of which have stamens only.     

THE REPRODUCTIVE BIOLOGY OF RASPBERRIES AND PLANT-POLLINATOR COMMUNITY STRUCTURE

Rubus idaeus and Rubus pubescens are congeners which differ with respect to their life history patterns. Rubus idaeus is locally important in the Northeast in areas subject to windthrow, fire, and man-made disturbances, while R. pubescens often forms a significant portion of the ground cover of shaded, damp, woodland areas. The life history pattern of R. idaeus is based upon the short term build up and slow decay of a large seed bank. Vegetative reproduction is more important in the eventual spread of R. pubescens. The reproductive traits of the two species reflect many of the above mentioned constraints and differences. Rubus pubescens produces relatively small quantities of nectar and flowers during a brief 1–2-wk period late in May. Synchronous flowering probably minimizes the incidence of floral predation and makes the low nectar flowers more attractive by reducing the pollinators' flight time. Rubus idaeus is an abundant species, which offers almost unlimited supplies of nectar during at least part of its extended 3–4-month flowering season. It is attractive to a wide range of pollinators and has figured prominently in the design, phenology, and reward structure of the early successional northern hardwoods plant-pollinator community.     

The exploitation of floral nectar in Eucalyptus incrassata by honeyeaters and honeybees

Summary During October and November, 1977, a study of nectar production and nectarivore foraging in Eucalyptus incrassata was conducted at Wyperfeld National Park in south-eastern Australia in order to evaluate the extent to which introduced honeybees (Apis mellifera) compete with native honeyeaters for floral nectar. Data on nectar production, nectar availability, ambient air temperature and the numbers of visiting honeyeaters and honeybees were collected. Most of the daily nectar production in E. incrassata occurs early in the morning when temperatures are too low for insects to forage. In addition, insects, particularly honeybees, are unable to exploit nectar in the youngest flowers because the stamens are clustered tightly around the style. As a result of these temporal and structural characteristics of the flowers, honeyeaters are able to harvest most of the nectar. Honeybees potentially have access to 35–47% of the average daily production of floral nectar in E. incrassata and actually harvest considerably less. These data show that E. incrassata flowers are adapted to restrict insect foragers despite their superficially unspecialized appearance. Eight forest and woodland eucalypts do not have a flower stage which excludes insects and the significance of this difference is discussed.     

Micro-Foraging Routes of Bicolletes pampeana (Colletidae) and Bee-Induced Pollen Presentation in Cajophora arechavaletae (Loasaceae)

In flowers of Cajophora arechavaletae Urb. the stamens are hidden from flower visitors in naviculate petals. In the male phase the stamens successively migrate at irregular intervals to the centre of the flower where they present pollen. Therefore, non-specialised pollinators cannot predict the time of pollen presentation. The oligolectic females of Bicolletes pampeana are effective pollinators of Cajophora arechavaletae. Females and males can elicit stamen movements by pressing the scales of the nectaries outwards with their head while taking up nectar. If this stimulus is responded to, up to 3 stamens move and reach the centre of the flower on average after 2.4 min. Experiments showed that the stimulus of nectar scale pressing was responded to maximally when the inter-stimulus interval was at least 14 min. B. pampeana females have evolved a foraging strategy which is adapted to the unique pollen presentation of C. arechavalete flowers. On microforaging routes they trapline 30–60 flowers and, therefore, most frequently come back to the same flower after intervals of about 3 min. This is exactly the period after which a female can expect pollen in the centre of the flower if her previous stimulus was responded to. Competition between the females causes them to return to the flowers at such short intervals.     

CHLORANTHUS-LIKE STAMENS FROM THE UPPER CRETACEOUS OF NEW JERSEY

Fossil angiospermous stamens with in situ pollen from the Turonian (ca. 90 million years before present, Late Cretaceous) of New Jersey are described and assigned to the Chloranthaceae. The fossil stamens, which are three-parted and bear two bisporangiate thecae on the central lobe and one bisporangiate theca on each lateral lobe, are indistinguishable from stamens of several extant species of Chloranthus. The pollen is spheroidal, 13–18 μm in diameter, with a reticulate exine and apparently elongate/elliptical apertures. The pollen is similar to that in extant Chloranthus in grain size, shape, exine sculpture, and aperture structure. Like pollen of some extant species of Chloranthus, aperture number in the fossil pollen appears to be variable. Because fossil pistillate chloranthoid reproductive structures have not been found at this locality it is unknown whether the fossil stamens described here were borne on the side of the ovary, as in extant Chloranthus, or in another arrangement. The three-parted stamen of Chloranthus is unique in angiosperms and there has been considerable debate concerning the origin and evolutionary significance of the structure. Uncertainty as to whether the three-parted stamen represents a synapomorphy for the genus or a retained plesiomorphy in angiosperms is the primary reason why these fossil stamens are not assigned to the extant genus Chloranthus.     

FLOWERING BEHAVIOR OF THE NEOTROPICAL GENUS ANTHURIUM (ARACEAE)

The genus Anthurium (Araceae) is one of the most taxonomically complex genera in the neotropics. Studies of living material have shown modes of behavior which probably have a direct influence on pollination biology and evolution. Separation of the sexes is generally accomplished by marked protogyny. Considerable differences also exist in the rate of development of flowers, the presence, source and amount of stigmatic nectar, as well as the method of pollen presentation. The genus exhibits an unusual pattern of staminal emergence. In all species studied, the lateral pair of stamens are first to emerge, usually one at a time, followed by the anterior, then the posterior stamens of the alternate pair. There are also differences in the degree of exsertion, the disposition with respect to the stigma, degree of retraction and changes in pollen color. Some species have stamens which are retracted completely after opening: others have stamens which scarcely emerge but instead force the pollen out in long ribbons. Important differences also exist in flower aromas with both fly and bee pollination syndromes exhibited. All of these aspects of flowering behavior are natural phenomena believed to be important in pollination biology.     

Structure and development of bracteal nectary glands in Aphelandra (Acanthaceae)

A survey of bracteal (extrafloral) nectaries in species of Aphelandra (Acanthaceae) reveals substantial diversity. Each bracteal nectary is an aggregate of individual glands that vary in number, size, and structure among species. Glands contain three cell layers: a palisade-like secretory cell layer, a one-to-many-celled intermediate layer with thickened cell walls, and a foot layer. Members of the A. pulcherrima complex have one of two distinct gland types: relatively small glands with a single-celled intermediate layer or larger glands that have a multicellular intermediate layer. Nectaries composed of small glands are patches of many (>50) glands, whereas those composed of large glands are patches of < 10 glands. Four outgroup species have bracteal nectaries of numerous small glands with pluricellular intermediate layers. Glands of all three types are initiated as single enlarged protodermal cells, and all undergo similar early periclinal divisions; the large-gland type shows greater subsequent enlargement with many more anticlinal divisions. The bracteal nectar glands are interpreted to be homologous with simpler glandular trichomes, and mark a monophyletic lineage within Aphelandra. Comparisons with outgroup species show that both nectary types in the A. pulcherrima complex have diverged from an ancestral condition of numerous small glands with pluricellular intermediate layers. Use of the ontogenetic criterion to polarize gland type within the A. pulcherrima complex would yield erroneous results because evolution has apparently involved a developmental truncation with loss of cell divisions in the intermediate layer of small glands. Comparable nectar glands in more distant taxa are interpreted as remarkable cases of convergent evolution, perhaps from similar trichome precursors.     

The secretory glands of <Emphasis Type="Italic">Asphodelus aestivus</Emphasis> flower

Various secretory glands are observed on Asphodelus aestivus flower, a common geophyte of Mediterranean type ecosystem. The floral nectary has the form of individual slits between the gynecium carpels (septal nectary). The septal slits extend downwards to the ascidiate zone of the carpels. The nectar is secreted by the epidermal cells of the slits, which differentiate into epithelial cells. The latter contain numerous organelles, among which endoplasmic reticulum elements and golgi bodies predominate. Nectar secretion results in an expansion of the space between the septa. The nectar becomes discharged through small holes on the ovary wall. Six closely packed stamens surround the ovary and bear numerous papillae at their basis. These papillae are actually osmophores, i.e. secretory structures responsible for the manufacture, secretion and dispersion of terpenic scent. A mucilage gland (obturator) exists between the lateral ovule and the ovary septa, giving a positive reaction with Schiff’s reagent. This gland secretes a mucoproteinaceous product to nourish the pollen tube and to facilitate its penetration into the ovary.     

FLORAL ONTOGENY IN SOPHOREAE (LEGUMINOSAE: PAPILIONOIDEAE). I. MYROXYLON (MYROXYLON GROUP) AND CASTANOSPERMUM (ANGYLOCALYX GROUP)

Floral ontogeny is described and documented using scanning electron microscopy in Myroxylon balsamum and Castanospermum australe, representatives respectively of Polhill's Myroxylon and Angylocalyx groups (Leguminosae: Papilionoideae), groups exhibiting relatively unspecialized flower structure for the tribe Sophoreae. Both are woody tropical trees with axillary or terminal racemes or panicles. Bracteoles are present in both Myroxylon and Castanospermum. Flowers are initiated singly in bract axils, which are produced in acropetal order by the inflorescence apical meristem. The flower structure of both includes a broad calyx tube, five petals lacking any fusion (only the vexillary distinctive), ten free homogeneous stamens in two whorls, and a long-stipitate carpel. The two taxa are alike in early organogenetic stages with essentially acropetal order of initiation: sepals, petals, outer stamens plus carpel, inner stamens. Within each whorl the order is unidirectional from the abaxial side. They are alike through middevelopment with one exception. There is accelerated vexillar enlargement in Castanospermum by middevelopment, not found in Myroxylon. Both have a hypanthium, which forms late in development. In both, large flower size, exserted stamens, and hypanthium are adaptations to bird-pollination. Differences between the two that are manifested in late development include strongly zygomorphic calyx and petal color change over time (Castanospermum), stamens sagittate and apiculate with some basal filament fusion (Myroxylon), stigma form differences, and fruit form.     

ADAPTIVE SIGNIFICANCE OF FLOWER COLOR AND INTER-TRAIT CORRELATIONS IN AN IPOMOPSIS HYBRID ZONE

Flower color is often viewed as a trait that signals rewards to pollinators, such that the relationship between flower color and plant fitness might result from its association with another trait. We used experimental manipulations of flower color and nectar reward to dissociate the natural character correlations present in a hybrid zone between Ipomopsis aggregata and Ipomopsis tenuituba. Isozyme markers were used to follow the male and female reproductive success of these engineered phenotypes. One field experiment compared fitnesses of I. aggregata plants that varied only in flower color. Plants with flowers painted red received more hummingbird visits and sired more seeds than did plants with flowers painted pink or white to match those of hybrids and I. tenuituba. Our second field experiment compared fitnesses of I. aggregata, I. tenuituba, and hybrid plants in an unmanipulated array and in a second array where all flowers were painted red. In the unmanipulated array, I. aggregata received more hummingbird visits, set more seeds per flower, and sired more seeds per flower. These fitness differences largely disappeared when the color differences were eliminated. The higher male fitness of I. aggregata was due to its very high success at siring seeds on conspecific recipients. On both I. tenuituba and hybrid recipients, hybrid plants sired the most seeds, despite showing lower pollen fertility than I. aggregata in mixed donor pollinations in the greenhouse. Ipomopsis tenuituba had a fitness of only 13% relative to I. aggregata when traits varied naturally, compared to a fitness of 36% for white relative to red flowers when other traits were held constant.     

INITIATION OF STAMENS,CARPELS, AND RECEPTACLE IN THE CACTACEAE

Five taxa representing the three tribes of the Cactaceae have similar patterns of stamen and carpel initiation but display differences in early receptacle development. The first ring of stamens and the carpels arise simultaneously from subsurface layers. The bases of carpels are congenitally connate. Additional stamens are initiated centrifugally. The shape of the floral meristem within the ring created by the first stamens varies. In Pereskia corrugata it remains broadly convex; in Opuntia engelmannii it forms a depression with a small convex central region; in Epiphyllum strictum it forms a broad shallow depression; in Echinocereus reichenbachii var. albispinus it develops a deep depression; and in Mammillaria compressa it develops a depression prior to stamen and carpel initiation. Changes in receptacle shape result from cessation of apical growth and activation of an intercalary ring meristem. These two processes occur earlier in ontogeny in the more advanced of these five taxa.     

Postpollination Nectar Reabsorption and Its Implications for Fruit Quality in an Epiphytic Orchid1

We present evidence that pollination triggers nectar reabsorption in flowers of the epiphytic orchid Mystacidium venosum. The amount of sugar in nectar of M. venosum decreased significantly by more than 50 percent within 72 hours of pollination. Hand–pollinated flowers from which nectar was previously removed set significantly smaller fruits with a lower percentage of viable seeds than hand–pollinated flowers containing nectar, suggesting that resources reclaimed by nectar resorption are allocated to fruit production.     

Stamen movements in flowers ofOpuntia (Cactaceae) favour oligolectic pollinators

Opuntia brunneogemmia andO. viridirubra occur sympatrically in the Serra do Sudeste, Rio Grande do Sul, Brazil. Their flowers have 450–600 thigmonastic stamens and provide large amounts of pollen and nectar for bees. Bees of 41 species were registered at the flowers ofO. brunneogemmia and 30 at the flowers ofO. viridirubra. Females of three oligolectic species are the only effective pollinators:Ptilothrix fructifera (Anthophoridae),Lithurgus rufiventris (Megachilidae), andCephalocolletes rugata (Colletidae). During their visits inOpuntia-flowers, bees touch the filaments and stimulate the movement of the stamens to the centre of the flower. At the end of this movement, the anthers are densely packed around the style. As a consequence the pollen is presented in an easily accessible upper layer of anthers and various, nearly inaccessible lower layers. The lower layers contain about 80% of the pollen reward. Only females of the three oligolectic pollinators exploit the pollen from the lower layers and reach the nectar furrow. Therefore, through their stamen movements,Opuntia flowers hide most of their pollen from flower visitors but favour effectively pollinating, oligolectic bees.