Nectar replenishment and pollen receipt interact in their effects on seed production of Penstemon roseus

Resource supply and pollen delivery are often thought to equally limit seed production in animal-pollinated plants. At equilibrium, plants should show no response to experimental pollen supplementation because resources limit seed set above the current level of pollen attraction, while experimental reduction in pollen deposition below the equilibrium level would reduce seed set. The predicted equilibrium may be disrupted, however, if plants expend additional energy to replenish removed nectar. We investigated the combined effects of nectar removal and pollen delivery on female reproductive success of Penstemon roseus (Plantaginaceae), a hummingbird-pollinated plant that replenishes removed nectar. We first documented that the frequency of experimental nectar removal was correlated with total nectar secretion; and increased frequency of nectar removal resulted in increased female reproductive costs to the plant. Trade-offs between investing resources in nectar and investing resources in seeds were then investigated in two contrasting natural populations by removing nectar from flowers at increasing frequencies while simultaneously hand-pollinating flowers with increasing amounts of pollen. Seed set was lowest at low levels of pollen deposition, highest at medium-sized pollen loads, and intermediate when pollen loads were highest. At both sites, the frequency of nectar removal and pollen deposition had an interactive effect on seed production, in that intermediate levels of nectar removal result in the absolute highest seed set, but only at intermediate pollen loads. At high pollen loads, seed set was higher following little to no nectar removal, and at low pollen loads, all rates of nectar removal affected fecundity equally. Seed mass responded to nectar removal and pollination differently than did seed set. High levels of nectar removal and pollen delivery both lowered seed mass, with little interaction between main effects. Our findings are among the first to demonstrate that nectar replenishment costs and pollination intensity jointly affect seed production. This conflict between nectar replenishment costs and pollen-limiting factors results in trade-offs between pollinator attraction and seed provisioning. Thus, resource allocation towards nectar production should more often be considered in future studies of pollen limitation.     

Effect of nectar supplementation on male and female components of pollination success in the deceptive orchid Dactylorhiza sambucina

Many orchids lack floral nectar rewards and therefore rely on deception to attract pollinators. To determine the effect that a mutation for nectar production would have on overall pollination success of the deceptive orchid Dactylorhiza sambucina, we recorded pollen deposition and removal in flowers of plants that had either been supplemented with an artificial nectar solution or left unmanipulated as controls. Nectar supplementation resulted in significant increases in the proportion of flowers pollinated, regardless of morph colour and the density of plants supplemented in the population. However, nectar supplementation had a significant positive effect on pollinaria removal only for the yellow morph in one experiment in which a low proportion of plants were supplemented. Thus a mutation for nectar production would have a positive effect on overall pollination success in D. sambucina, particularly the female component. The observed patterns are discussed in relation to other factors, such as cross-pollination and the reallocation of nectar resources for other plant functions, which are traditionally considered to shape the rewardless strategies of orchids.     

Pollination Ecology and Effect of Nectar Removal in Macleania bullata (Ericaceae)1

The floral syndrome of Macleania bullataYeo (Ericaceae) reflects its adaptation to hummingbird pollination. Its flowers, however, are subject to high levels of nectar robbing. I examined the floral visitor assemblage of M. bullata in a tropical montane wet forest in southwestern Colombia, focusing on the behavior of the visitors. I also tested for the presence of nocturnal pollination and the effects of nectar removal on new nectar production. The principal floral visitors were the nectar robbing hummingbirds Ocreatus underwoodii (19.1% of visits) and Chlorostilbon mellisugus (18.9%). Only two species of long–billed hummingbirds visited the flowers of M. bullata as “legitimate” pollinators: Coeligena torquata (14.7% of visits) and Doryfera ludoviciae (14.3%). The remaining visits constituted nectar robbing by bees, butterflies, and other species of hummingbirds. Nocturnal pollination took place, although fruit set levels were 2.4 times higher when only diurnal pollination was allowed as opposed to exclusively nocturnal pollination. Nectar robbers removed floral nectar without pollinating the flower. Treatments of experimental nectar removal were carried out to examine if flowers synthesize more nectar after nectar removal. Nectar removal increased the total volume of nectar produced by each flower without affecting sugar concentration. Thus, nectar robbing can impose a high cost to the plants by forcing them to replace lost nectar.     

Pollination by passerine birds: why are the nectars so dilute?

Bird-pollinated flowers are known to secrete relatively dilute nectars (with concentrations averaging 20–25% w/w). Many southern African plants that are pollinated by passerine birds produce nectars with little or no sucrose. Moreover, these hexose nectars are extremely dilute (10–15%). This suggests a link between sugar composition and nectar concentration. Nectar originates from sucrose-rich phloem sap, and the proportion of monosaccharides depends on the presence and activity of invertase in the nectary. Hydrolysis of sucrose increases nectar osmolality and the resulting water influx can potentially convert a 30% sucrose nectar into a 20% hexose nectar, with a 1.56 times increase in volume. Hydrolysis may also increase the gradient for sucrose transport and thus the rate of sugar secretion. When sucrose content and refractometer data were compared, some significant correlations were seen, but the occurrence of sucrose-rich or hexose-rich nectars can also be explained on phylogenetic grounds (e.g. Erythrina and Protea). Hexose nectars may be abundant enough to drip from open flowers, but evaporation leads to much variability in nectar concentration and increases the choices available to pollinators.     

Nectar Secretion Pattern and Removal Effects in Six Argentinean Pitcairnioideae (Bromeliaceae)

Nectar secretion pattern and effects of nectar removal were analyzed in six hummingbird-pollinated Argentinean Pitcairnioideae: Abromeitiella brevifolia. A. lorentziana, Deuterocohnia longipetala. Dyckia floribunda, D. ragonesei and Puya spathacea. Flower lifetime was determined in each case. Nectar volume, concentration and sugar production were measured from bud opening till fading of flowers at different time intervals according to the species' flower life-span. Nectar volume varies while nectar concentration and cumulative sugar production increase as a function of flower age in all the studied species. In general, total nectar volume and concentration values can be affected by periodic removal, but total sugar production is unaffected. Only in Puya spathacea did periodic nectar harvesting reduce the total amount of sugar produced.     

Nectar sugar composition and volumes of 47 species of Gentianales from a southern Ecuadorian montane forest

BACKGROUND AND AIMS: This study investigates 47 taxonomically related species (Gentianales), all native to a tropical montane forest in southern Ecuador, in terms of nectar chemistry and nectar volumes in relation to pollination biology. METHODS: Nectar volumes of covered (24-h production) and uncovered (standing crop) flowers were measured in the natural habitat. Sucrose, fructose and glucose were quantified in the nectar using high performance liquid chromatography. Flower visitors were observed. KEY RESULTS: Nectar sugar concentration did not differ significantly among the pollination syndromes. Regarding sugar composition, the only significant differences were found in chiropterophilous and myiophilous flowers, which had a significantly lower sugar ratio than sphingophilous flowers. A separation of chiropterophilous and myiophilous flowers from the other pollination syndromes is further substantiated by non-linear multidimensional scaling using the chord-normalized expected species shared index of dissimilarity based on nectar sugar compositions. The matrix test revealed no correlation of observed floral visitors to nectar concentrations; however, a weak significant correlation was found between floral visitors and nectar sugar compositions. The nectar volumes of covered and uncovered flowers are related to, and differ significantly among, pollination syndromes. Matrix tests revealed correlation between floral visitors and nectar volume of covered flowers and, to a lesser extent, of uncovered flowers. CONCLUSIONS: Sucrose is the predominant floral nectar sugar in the order Gentianales, suggesting that nectar sugar composition is a conservative characteristic. However, some degree of an adaptive convergence of floral nectar compositions to principal pollinator type within the constraints set by phylogenetic history is likely. The driving force to visitation appears to be the volume of nectar the visitor can expect to consume.     

Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae)

Inga species present brush‐type flower morphology allowing them to be visited by distinct groups of pollinators. Nectar features in relation to the main pollinators have seldom been studied in this genus. To test the hypothesis of floral adaptation to both diurnal and nocturnal pollinators, we studied the pollination ecology of Inga sessilis, with emphasis on the nectar secretion patterns, effects of sequential removals on nectar production, sugar composition and the role of diurnal and nocturnal pollinators in its reproductive success. Inga sessilis is self‐incompatible and pollinated by hummingbirds, hawkmoths and bats. Fruit set under natural conditions is very low despite the fact that most stigmas receive polyads with sufficient pollen to fertilise all ovules in a flower. Nectar secretion starts in the bud stage and flowers continually secreting nectar for a period of 8 h. Flowers actively reabsorbed the nectar a few hours before senescence. Sugar production increased after nectar removal, especially when flowers were drained during the night. Nectar sugar composition changed over flower life span, from sucrose‐dominant (just after flower opening, when hummingbirds were the main visitors) to hexose‐rich (throughout the night, when bats and hawkmoths were the main visitors). Diurnal pollinators contributed less than nocturnal ones to fruit production, but the former were more constant and reliable visitors through time. Our results indicate I. sessilis has floral adaptations, beyond the morphology, that encompass both diurnal and nocturnal pollinator requirements, suggesting a complementary and mixed pollination system.     

Nectar, nectaries, flower visitors, and breeding system in five terrestrial Orchidaceae from central Argentina

Floral nectar sugar composition, nectary anatomy, and visitors are studied in five Argentine Orchidaceae, from 18 populations. Hand-pollinations were performed to evaluate their breeding system. We found two different types of perigonal nectaries located either in the spur (Habenaria gouriieana, H. hieronymi, Habenariinae), or in the basal lateral parts of the labellum (Beadlea dutraei, Pelexia bonariensis, Stenorrhynchos orchioides, Spiranthinae). The spur ofHabenaria is a nonvascularised and nonstructural nectary. The inner epidermis bears one-celled long papillae. In bud stage, the papillae are filled with starch grains, but when the flower opens and nectar secretion starts, they show no starch grains. This fact may indicate that starch is a source for some of the secreted nectar. In the remainder genera, the lateral basal parts of the labellum are secretory. The two glands are located in the adaxial basal lateral faces of the labellum. These nectaries are structural and nonvascularised.Stenorrhynchos produces abundant, concentrated nectar (40–50%).Habenaria gourlieana accumulates copious nectar in a lower concentration (<20%), whereas the other species produce small quantities of concentrated nectar (ca. 50%). Three of the studied species have sucrose predominant nectar (Beadlea dutrael, Habenaria gourlieana, andPelexia bonariensis) whileH. hieronymi, Stenorrhynchos orchioides have hexose predominant ones. Nectar removal and/or pollination induce flower senescence.H. gouriieana is visited by sphingids,S. orchioides by hummingbirds, andB. dutrael by bees. For the two other species we did not record flower visitors.Pelexia bonariensis, B. dutrael, andS. orchiodes are self-compatible species but a pollinator is needed.     

盗蜜行为在植物繁殖生态学中的意义

在动植物的相互关系中,盗蜜行为被认为是一种不同于普通传粉者的非正常访花行为。动物之所以要采取这种特殊的觅食策略,有假说认为是由访花者的口器和植物的花部形态不匹配造成的,也有认为是盗蜜行为提高了觅食效率从而使盗蜜者受益。在盗蜜现象中,盗蜜者和宿主植物之间的关系是复杂的。盗蜜对宿主植物的影响尤其是对其繁殖适合度的影响归纳起来有正面、负面以及中性3类。与此同时,盗蜜者的种类, 性别及其掠食行为差异不仅与生境因素密切相关,而且会对宿主植物的繁殖成功产生直接或间接的影响。另外,盗蜜者的存在无疑对其它正常传粉者的访花行为也产生一定的影响,从而间接地影响宿主植物的繁殖成功, 而植物在花部形态上也出现了对盗蜜现象的适应性进化。作者认为, 盗蜜是短嘴蜂对长管型花最有效的一种掠食策略, 它不仅增加了盗蜜者对资源的利用能力, 而且由于盗蜜对宿主植物繁殖成功的不同的影响使其具有调节盗蜜者和宿主之间种群动态的作用, 两者的彼此适应是一种协同进化的结果。     

3种雌雄异熟樟科植物开花动态的比较研究

为了解樟科植物雌雄异熟的繁育系统特点,对3种樟科植物阴香(Cinnamomum burmannii)、紫楠(Phoebe sheareri)和浙江楠(Phoebe chekiangensis)雌雄异熟花的开花动态进行了比较研究.结果表明,3种植物雌性功能期的开始时间、雌性功能期和雄性功能期的时间分配有差异.3种植物的主...     

Spatial distribution of nectar production in a natural Echium vulgare population: Implications for pollinator behaviour

The distribution of trait values in many populations is not homogenous but creates a mosaic of patches. This may lead to differences in selection on the patch level compared to selection on the population level. As an example we investigated the spatial distribution of nectar production and its effects on pollinator behaviour in a natural population of Echium vulgare. Nectar production per flower, number of flowers and total nectar production showed a hierarchy and spatial aggregation as expressed by Gini coefficients and significant Moran's I values. Plants in patches of high nectar production received significantly more pollinator visits and had a significant emanating effect on pollinator visits of neighbouring plants. The same was true for plants in patches with high number of flowers. To disentangle these effects a path analysis was applied, which suggested that the direct effect of nectar production per flower although present, seems to be small compared to the effect of the number of flowers. Nectar production per flower affected pollinator visits mainly indirectly by way of total nectar production, which includes the effect of number of flowers. Assuming a minor pollinator-mediated selection for number of flowers, pollinator-mediated selection for total nectar production equals that for nectar production per flower. If so, the observed spatial structure of nectar production and its emanating effect on pollinator behaviour is of importance for natural selection. Plants of low nectar production occurring close to patches of plants with high nectar production benefited from the enhanced pollinator service of their neighbours while saving costs of increased nectar production. Consequently, plants with low nectar production may have a selective advantage at patch level while plants with high nectar production may have a selective advantage at population level. Results presented stress the importance of small-scale patterns for ecological relationships and evolutionary change.     

Variation in nectar volume and composition of Impatiens capensis at the individual,plant, and population levels

Although the volume and chemical composition of nectars are known to vary among plant species and to affect pollinator response to plants, relatively little is known of the variation in volume, and sugar and amino acid composition within species. We collected nectar from Impatiens capensis in a nested design: three flowers from each of three plants from each of three populations. This design enabled us to quantify variation within individual plants, among plants within populations, and among populations. Using high performance liquid chromatography, we analyzed the sugar and amino composition of the 27 flowers. Analysis of variance showed that none of the parameters (volume, concentrations of three sugars and 24 amino compounds) varied within individuals. Variation in nectar volume was not significant among plants but was nearly significant among populations. Of the three sugars detected (sucrose, glucose, and fructose), the only significant variation was that of sucrose among populations. Concentrations of 12 amino compounds varied significantly at the plant level while 7 amino compounds varied among populations. The results indicate that: (1) pooling of nectar samples from flowers of individual plants can be an acceptable methodology for those seeking to understand within species variation; (2) amino compounds appear to vary more than either volumes or sugar concentrations; (3) future studies should assess how much of the observed variation is due to genetic versus environmental differences; (4) additional studies should examine the geographic variation in nectar parameters and pollinators of I. capensis in order to assess the role different pollinators play in shaping nectar composition.     

Interpopulation variation in nectar production in Aconitum columbianum (Ranunculaceae)

Summary In Aconitum columbianum there are extreme interpopulation differences in rates of nectar secretion per flower. Since nectar sugar concentration varies little among populations, increased nectar secretion results in a greater mass of sugar per flower for pollinator attraction. These differences in the amount of reward offered per flower account at least in part for observed higher levels of pollinator activity in populations with high nectar production. Nectar production is correlated also with nectary depth, i.e., flowers in populations with deep nectaries have higher rates of nectar secretion than those with shallow nectaries. Nectary depth differences adapt populations to different pollinator-types. Populations with deeper nectaries are adapted to pollination by bumblebees with longer tongues and more specialized foraging behaviors. In conclusion, there are basic differences in pollination ecology among geographical races of a. columbianum, which are indicated by correlated interpopulution differences in (1) nectar production, (2) level of pollinator activity, (3) nectar depth, and (4) pollinator-type.     

Nectar, floral morphology and pollination syndrome in Loasaceae subfam. Loasoideae (Cornales)

BACKGROUND AND AIMS: Loasaceae subfam. Loasoideae are mostly distributed in South America (sea level to over 4500 m) with a wide range of animals documented as pollinators. The aim was to investigate correlations between nectar parameters, flower morphology, pollination syndrome and phylogeny. METHODS: Nectar was collected from 29 species from seven genera in the subfamily. Concentration and volumes were measured and the amount of sugar calculated. Correlations of nectar data were plotted on a ternary graph and nectar characteristics compared with flower visitors, floral morphology and phylogenetic data. KEY RESULTS: Sugar concentrations are generally higher than reported for most plant families in the literature. The species investigated can be roughly grouped as follows. Group I: plants with approx. 1.5(-3.5) microL nectar with (40-)60-80% sugar and 0.19-2 mg sugar flower-1; with small, white, star-shaped corollas, pollinated by short-tongued bees. Groups II, III and IV: plants with mostly orange, balloon-, saucer-, bowl- or bell-shaped corollas. Group II: plants with approx. 9-14 microL nectar with 40-60% sugar and 4-10 mg sugar flower-1; mostly visited by long-tongued bees and/or hummingbirds. Group III: plants with 40-100 microL nectar with 30-40% sugar and 14-36 mg sugar flower-1, mostly visited by hummingbirds. Group IV: geoflorous plants with 80-90 microL with 10-15% sugar and 8.5-12 mg sugar flower-1, presumably visited by small mammals. Groups II and III include species visited by bees and/or hummingbirds. CONCLUSIONS: Pollinator switches from short-tongued bees via long-tongued bees to hummingbirds appear to have taken place repeatedly in the genera Nasa, Loasa and Caiophora. Changes in nectar amount and concentration appear to evolve rapidly with little phylogenetic constraint.     

The reproductive biology ofJaborosa integrifolia (Solanaceae): Why its fruits are so rare?

Jaborosa integrifolia exhibits stigma-height polymorphism. There are individuals with flowers where anthers and stigma are at the same height but the rule is variable herkogamy, the most common type (75%) being that with an exerted stigma. Self- and cross-tubes did not differ in their capability to reach the ovary (t = –0.67,P < 0.53); they had a high growth rate (6.95 ± 2.28 mm h^–1). There is not autogamy but mostly self-incompatibility. Fruits from controlled cross-pollination showed the highest seed set and seed viability. The nectar sugar is characterized by a similar amount of glucose and fructose, and by the absence of sucrose. Although nectar secretion was continuous throughout the life of the flower, most nectar was secreted during the first 24 h after flower opening. Nectar production costs appear to be lower than in other species since nectar secretion is neither inhibited after a removal (i.e. a pollinator visit) nor reabsorbed as the flower ages. Sphingids visit the flowers mainly after midnight. They insert their proboscis down to the base of the corolla tube to reach the nectar. The upper limit to fruit production is set by pollinator visits. Fruits produced from open-pollinated flowers are often predated by numerous larvae (mainly lepidopteran ones). Considering that this species is mostly self-incompatible and pollination is limited, that each plant displays only a low number of flowers throughout the flowering season, and that there is a high rate of fruit predation, it is not surprising that fruits ofJ. integrifolia are so rare.     

Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant mating system

The outcome of species interactions is often difficult to predict, depending on the organisms involved and the ecological context. Nectar robbers remove nectar from flowers, often without providing pollination service, and their effects on plant reproduction vary in strength and direction. In two case studies and a meta-analysis, we tested the importance of pollen limitation and plant mating system in predicting the impacts of nectar robbing on female plant reproduction. We predicted that nectar robbing would have the strongest effects on species requiring pollinators to set seed and pollen limited for seed production. Our predictions were partially supported. In the first study, natural nectar robbing was associated with lower seed production in Delphinium nuttallianum, a self-compatible but non-autogamously selfing, pollen-limited perennial, and experimental nectar robbing reduced seed set relative to unrobbed plants. The second study involved Linaria vulgaris, a self-incompatible perennial that is generally not pollen limited. Natural levels of nectar robbing generally had little effect on estimates of female reproduction in L. vulgaris, while experimental nectar robbing reduced seed set per fruit but not percentage of fruit set. A meta-analysis revealed that nectar robbing had strong negative effects on pollen-limited and self-incompatible plants, as predicted. Our results suggest that pollination biology and plant mating system must be considered to understand and predict the ecological outcome of both mutualistic and antagonistic plant-animal interactions.     

Xylose as a nectar sugar: from biochemistry to ecology

Studies of nectar sugar composition in the Proteaceae, an ancient southern hemisphere plant family, have demonstrated that xylose comprises up to 39% of nectar sugar in two genera, Protea and Faurea, and may therefore represent a substantial fraction of the energy available to pollinators of these plants. Although insect and bird pollinators of Protea species are averse to xylose, mice (Aethomys namaquensis) will drink pure xylose, which is metabolized either by gut bacteria or by the mouse tissues. In the form of xylan polymers, the pentose sugar -xylose is a structural component of plant cell walls, and there is considerable biotechnological interest in xylose fermentation. Bacteria and yeasts convert -xylose to -xylulose and thence via the pentose phosphate pathway to fructose-6-phosphate, which is either oxidized or fermented to ethanol. Gut symbionts of rodent pollinators may be analogous to ruminal xylose-metabolizing bacteria. The presence of xylose in Protea and Faurea nectar remains puzzling in view of pollinator aversions: even for rodent pollinators, it is the least preferred nectar sugar. In the generalized pollination systems of the Proteaceae, a coevolutionary explanation for nectar xylose as an attractant for mammalian pollinators is probably less likely than one involving plant physiology, with xylose in phloem sap being secreted passively into the nectar.     

Reproductive biology, variability of nectar features and pollination of Combretum fruticosum (Combretaceae) in Argentina

Flower morphology, nectary structure, nectar features (chemical composition, secretion pattern, standing crop, removal effects) and flower visitors are analysed in an Argentinian population of Combretum fruticosum. The variability of these data was examined throughout the flower lifetime. Nectar is hexose dominant. Its chemical composition and concentration are constant for all flowering stageS. Nectar volume varies as a function of flower age due to a combination of nectar secretion, cessation and resorption periods. The overall sugar production is decreased by nectar removal. The plant is self-incompatible and xenogamouS. Only 16.2% of the flowers set seedS. Inflorescences with green flowers were exclusively visited by two hummingbird and three perching bird species which transfer the pollen. A clear link was observed among nectar production pattern, standing crop of nectar, and visitors' behaviour.     

Nectar and pollination drops: how different are they?

Background

Pollination drops and nectars (floral nectars) are secretions related to plant reproduction. The pollination drop is the landing site for the majority of gymnosperm pollen, whereas nectar of angiosperm flowers represents a common nutritional resource for a large variety of pollinators. Extrafloral nectars also are known from all vascular plants, although among the gymnosperms they are restricted to the Gnetales. Extrafloral nectars are not generally involved in reproduction but serve as ‘reward’ for ants defending plants against herbivores (indirect defence).

Scope

Although very different in their task, nectars and pollination drops share some features, e.g. basic chemical composition and eventual consumption by animals. This has led some authors to call these secretions collectively nectar. Modern techniques that permit chemical analysis and protein characterization have very recently added important information about these sugary secretions that appear to be much more than a ‘reward’ for pollinating (floral nectar) and defending animals (extrafloral nectar) or a landing site for pollen (pollination drop).

Conclusions

Nectar and pollination drops contain sugars as the main components, but the total concentration and the relative proportions are different. They also contain amino acids, of which proline is frequently the most abundant. Proteomic studies have revealed the presence of common functional classes of proteins such as invertases and defence-related proteins in nectar (floral and extrafloral) and pollination drops. Invertases allow for dynamic rearrangement of sugar composition following secretion. Defence-related proteins provide protection from invasion by fungi and bacteria. Currently, only few species have been studied in any depth. The chemical composition of the pollination drop must be investigated in a larger number of species if eventual phylogenetic relationships are to be revealed. Much more information can be provided from further proteomic studies of both nectar and pollination drop that will contribute to the study of plant reproduction and evolution.Key words: Nectar, pollination drop, ovular secretion, plant reproduction, proteins, sugars, gymnosperms, angiosperms, plant–animal interaction