Hummingbird responses to gender-biased nectar production: are nectar biases maintained by natural or sexual selection?

Pollinators mediate the evolution of secondary floral traits through both natural and sexual selection. Gender-biased nectar, for example, could be maintained by one or both, depending on the interactions between plants and pollinators. Here, I investigate pollinator responses to gender-biased nectar using the dichogamous herb Chrysothemis friedrichsthaliana (Gesneriaceae) which produces more nectar during the male floral phase. Previous research showed that the hummingbird pollinator Phaethornis striigularis visited male-phase flowers more often than female-phase flowers, and multiple visits benefited male more than female fecundity. If sexual selection maintains male-biased rewards, hummingbirds should prefer more-rewarding flowers independent of floral gender. If, however, differential rewards are partially maintained through natural selection, hummingbirds should respond to asymmetry with visits that reduce geitonogamy, i.e. selfing and pollen discounting. In plants with male biases, these visit types include single-flower visits and movements from low to high rewards. To test these predictions, I manipulated nectar asymmetry between pairs of real or artificial flowers on plants and recorded foraging behaviour. I also assessed maternal costs of selfing using hand pollinations. For plants with real flowers, hummingbirds preferred more-rewarding flowers and male-phase morphology, the latter possibly owing to previous experience. At artificial arrays, hummingbirds responded to extreme reward asymmetry with increased single-flower visits; however, they moved from high to low rewards more often than low to high. Finally, selfed flowers did not produce inferior seeds. In summary, sexual selection, more so than geitonogamy avoidance, maintains nectar biases in C. friedrichsthaliana, in one of the clearest examples of sexual selection in plants, to date.     

How common is the ability of extrafloral nectaries to produce nectar droplets,to secrete nectar during the night and to store starch?

Evidence in favour of the ability of extrafloral nectaries (EFNs) to form nectar drop(let)s, secrete extrafloral nectar (EFNec) also during the night and store starch was compiled in order to refute controversial assertions. Not only were more than 150 reports of direct observations of EFNec drop(let)s found, but also 90 studies which suggest that EFNec secretion is copious enough to form drop(let)s automatically by forces of physics (surface tension strength), provided nectar accumulation is not interrupted by predatory animals. Twenty direct observations of nocturnal production of EFNec sufficiently proved that it is not always produced during the day. Additionally, numerous observations of the nocturnal activities of nectar consumers on EFNs indirectly indicated very common nocturnal secretion of EFNec. Although there is an early report of a starch‐containing EFN from 1881 (Trelease), few similar observations in other EFNs followed. Nevertheless, four studies have described the disappearance of stored starch during secretion and senescence of the EFNs. Referring back to an apparent relationship between the degradation of starch stored in a floral nectary and programmed cell death, at least in EFNs with transient storage of starch, a similar relationship cannot be excluded.     

Does spatial aggregation of total nectar production lead to genetic structure?

Spatial aggregation of plants of high nectar production, receiving an enhanced pollinator service is known to occur in Echium vulgare. Moreover, an emanating effect of nectar production on pollinator visits may occur, i.e. many pollinator visits may be observed around high nectar patches. Consequently, gene flow within patches of plants of high nectar production and their close neighbours may result in genetic structure. In this study, we investigated whether aggregation of total nectar production (nectar production per flower×number of flowers) and its emanating effect resulted in genetic structure in a natural E. vulgare population. We compared the spatial structure of total nectar production, pollinator visits and microsatellite markers using spatial autocorrelation analysis. Increased geitonogamy, caused by longer boutlengths in plants of high nectar production may generate genetic structure. We estimated selfing rates of plants of the highest and lowest total nectar production. Spatial aggregation of total nectar production occurred on a relatively small scale up to 2.83 m. A significant emanating correlation between total nectar production and pollinator visits was observed on a relatively large scale up to a 4.24 m. Thus, around patches of high nectar production numbers of pollinator visits were relatively high, while few visits were observed around patches of low nectar production. Weak genetic structure was present on a small scale up to 2.20 m. This corresponded with the scale of aggregation of total nectar production. High gene flow around the patches of high nectar production seems to weaken genetic structure. This is supported by the relatively low selfing rates. The average selfing rate of the plants of highest nectar production was 8.8% and that of the plants of lowest nectar production 5.0%. Low gene flow within and around low nectar patches sustain a weak genetic structure or, conversely, may have caused it in the first instance. Results indicate the importance of spatial structure of nectar production for pollinator movement.     

Why do ants shift their foraging from extrafloral nectar to aphid honeydew?

When aphids parasitize plants with extrafloral nectaries (EFNs) and aphid colony size is small, ants frequently use EFNs but hardly tend aphids. However, as the aphid colony size increases, ants stop using EFNs and strengthen their associations with aphids. Although the shift in ant behavior is important for determining the dynamics of the ant–plant–aphid interaction, it is not known why this shift occurs. Here, we test two hypotheses to explain the mechanism responsible for this behavioral shift: (1) Extrafloral nectar secretion changes in response to aphid herbivory, or (2) plants do not change extrafloral nectar secretion, but the total reward to ants from aphids will exceed that from EFNs above a certain aphid colony size. To judge which mechanism is plausible, we investigated secretion patterns of extrafloral nectar produced by plants with and without aphids, compared the amount of sugar supplied by EFNs and aphids, and examined whether extrafloral nectar or honeydew was more attractive to ants. Our results show that there was no inducible extrafloral secretion in response to aphid herbivory, but the sugar concentration in extrafloral nectar was higher than in honeydew, and more ant workers were attracted to an artificial extrafloral nectar solution than to an artificial aphid honeydew solution. These results indicate that extrafloral nectar is a more attractive reward than aphid honeydew per unit volume. However, even an aphid colony containing only two individuals can supply a greater reward to ants than EFNs. This suggests that the ant behavioral shift may be explained by the second hypothesis.     

Are nectar guide colour changes a reliable signal to pollinators that enhances reproductive success?

Background: Ageing and post-pollination changes in floral colour occur widely in flowering plants, but it remains an open question as to whether or not colour changes in nectar guides are associated with the quantity of floral rewards that ultimately influence pollinator visitations and reproductive success.

Aims: To examine whether nectar guide changes should be considered as a reliable signal to pollinators and to assess the effects of nectar guide changes on reproductive success.

Methods: We studied the process and adaptive value of colour changes in the nectar guides of Arnebia szechenyi whose flowers typically display conspicuous nectar guides at the onset of anthesis, after which they begin to fade, and disappear completely on the second day.

Results: Changes in nectar guide colour in A. szechenyi were intrinsic and age-dependent, although pollination somewhat accelerated the change. By the time that the nectar guides disappeared completely, floral rewards were reduced almost to zero. Artificial removal of nectar guides decreased both fruit set and pollen export. Flowers without nectar guides do not appear to increase the overall attractiveness of the plants.

Conclusions: Nectar guides and their changes represent reliable signals to pollinators and enhance both male and female reproductive success.     

Do plants dynamically regulate nectar features through sugar sensing?

Nectar properties (volume, concentration, viscosity) change dynamically in time. As stated by Pedersen some decades ago (1958), “Nectar is not a static product remaining outside the plant once produced but is in close contact with the plant system.”¹ It is now evident that secretion may occur concomitantly with resorption and that the latter process sometimes continues after secretion has ended. The rate of the two processes may be modified dynamically by the plant in response to ecological and physiological constraints, maintaining a relatively constant nectar concentration to ensure pollinator visits (nectar homeostasis) and reallocating resources, especially during development of the ovules and pericarp after fertilization. We suspect that nectar resorption is under-estimated as a phenomenon, because it requires detailed information on the dynamics of nectar production throughout the life of the flower that is seldom available or taken into consideration. The cytological and molecular mechanisms involved in nectar resorption are almost completely unknown. Sugar sensing may have a fundamental role in nectar resorption and homeostasis. Due to direct contact with sugar solutions, nectaries may offer wide scope for insights into this phenomenon which has attracted interest as part of plant signalling systems.Key words: nectaries, nectar resorption, nectar homeostasis, nectar composition     

Do extrafloral nectar resources, species abundances, and body sizes contribute to the structure of ant–plant mutualistic networks?

Recent research has shown that many mutualistic communities display non-random structures. While our understanding of the structural properties of mutualistic communities continues to improve, we know little of the biological variables resulting in them. Mutualistic communities include those formed between ants and extrafloral (EF) nectar-bearing plants. In this study, we examined the contributions of plant and ant abundance, plant and ant size, and plant EF nectar resources to the network structures of nestedness and interaction frequency of ant–plant networks across five sites within one geographic locality in the Sonoran Desert. Interactions between ant and plant species were largely symmetric. That is, ant and plant species exerted nearly equivalent quantitative interaction effects on one another, as measured by their frequency of interaction. The mutualistic ant–plant networks also showed nested patterns of structure, in which there was a central core of generalist ant and plant species interacting with one another and few specialist–specialist interactions. Abundance and plant size and ant body size were the best predictors of symmetric interactions between plants and ants, as well as nestedness. Despite interactions in these communities being ultimately mediated by EF nectar resources, the number of EF nectaries had a relatively weak ability to explain variation in symmetric interactions and nestedness. These results suggest that different mechanisms may contribute to structure of bipartite networks. Moreover, our results for ant–plant mutualistic networks support the general importance of species abundances for the structure of species interactions within biological communities.     

Nectary structure of Labiatae in relation to their nectar secretion and characteristics in a Mediterranean shrub community — Does flowering time matter?

We studied the interrelation between nectary structure (13 parameters), nectar characteristics (yield, chemical composition), and flower size of 11 Labiatae species in a Mediterranean shrub community near Athens, Greece. We also explored whether the above attributes are affected by the Mediterranean summer drought constraints. Our findings show that among all nectary parameters studied, nectary size and stomatal opening are the most important in (positively) shaping nectar secretion, nectary size being the most meaningful. Nectary structure is correlated to quantity of the nectar secreted, not its quality. Wide flowers bear wide nectaries with large stomatal openings, whereas deep flowers are not related to any nectary size. Corolla size (both length and width) and nectary stomatal opening decrease with flowering time. This applies also to nectary size, nectar volume and sugar content of the perennials (9 species). All above cases of time dependence show that there is a constraint effect of Mediterranean climate on floral and nectary structure, reflected also as a decrease in nectar secretion. Nectary structure in Labiatae is largely shaped by both phylogenetic and climate constraints. On the other hand, although nectar is largely influenced by nectary structure, it is to a large extent ecologically biased, implying that, in addition to phylogeny, there are many other ecological parameters interfering in its secretion such as time within the season, life history, and light requirements.     

Is the nectar redox cycle a floral defense against microbial attack?

Many angiosperms use a remarkable reproductive strategy that relies on attracting animals (insect, avian or mammalian pollinators) to transfer pollen between plants. Relying on other organisms for sexual reproduction seems evolutionarily untenable, but the great diversity of angiosperms illustrates how highly successful this strategy is. To attract pollinators, plants offer a variety of rewards. Perhaps the primary floral reward is floral nectar. Plant nectar has long been considered a simple sugar solution but recent work has demonstrated that nectar is a complex biological fluid containing significant and important biochemistry with the potential function of inhibiting microbial growth. These results lead the way to novel insights into the mechanisms of floral defense and the co-evolution of angiosperms and their pollinators.     

Why do some nectar foragers perch and others hover while probing flowers?

Diurnal hawkmoths, Hemaris fuciformis, and bumblebees, Bombus pasquorum, were observed foraging for nectar in flowers of Viscaria vulgaris. The hawkmoths hovered in front of the flowers, while the bees perched on them. The hawkmoths had a faster probing rate than the bees, and consequently also had higher gross and net rates of energy gain. A model is presented that shows that hovering only yields a higher net rate of energy gain (NREG) than perching when nectar volumes are high due to low competition for the resource. The difference in NREG of perchers and hoverers decreases with an increase of competition, and eventually perching yields the highest NREG. This is an effect of the higher cost of hovering. The results suggest that hovering can only evolve as a pure evolutionarily stable strategy (ESS) if competition is reduced, for example by co-evolutionary specializations with plants. The possibility that it has evolved as a mixed ESS (i.e. individuals can both hover and perch depending on the resource level) is discussed. The evolution of optimal foraging strategies is discussed, and it is pointed out that the rate of gain of an animal is independent of the strategy used when all competing foragers use the same strategy, but competitively superior strategies will nevertheless evolve because they are ESSs. Competition between strategies with different energy costs are special, because resource availability determines which strategy is competitively superior. A high-cost strategy can only evolve as a pure ESS at high resource levels, or as a mixed ESS at intermediate levels.     

Pollen amino acids—an additional diet for a nectar feeding butterfly?

The increase of the amino acid concentration over different time intervals in artificial nectar (i.e., a sucrose solution) due to pollen contamination was investigated in four Californian plant species (Aesculus californica, Amsinckia lunaris, Brodiaea pulchella, Carduus pycnocephalus), which are important nectar resources for a Californian colony of the butterflyBattus philenor as well as for other insects. The increase of the amino acid concentration in the medium is different in all four species and seems to be determined by a variety of factors including permeability of the pollen grain wall and presence or absence of pores. The results suggest a passive diffusion process of the free pollen amino acids into the medium rather than an active release. Implications from the experiments forBattus philenor and for other nectar feeding pollinators are discussed. A possible complementary effect of free pollen and nectar amino acids is proposed for plant species in which pollen is likely to be knocked into nectar by their flower visitors. A possible evolutionary pathway from nectar feeding butterflies such asBattus philenor to the complex derived pollen feeding habit in theHeliconius butterflies is proposed.     

Is nectar reabsorption restricted by the stalk cells of floral and extrafloral nectary trichomes?

Reabsorption is a phase of nectar dynamics that occurs concurrently with secretion; it has been described in floral nectaries that exude nectar through stomata or unicellular trichomes, but has not yet been recorded in extrafloral glands. Apparently, nectar reabsorption does not occur in multicellular secretory trichomes (MST) due to the presence of lipophilic impregnations – which resemble Casparian strips – in the anticlinal walls of the stalk cells. It has been assumed that these impregnations restrict solute movement within MST to occur unidirectionally and exclusively by the symplast, thereby preventing nectar reflux toward the underlying nectary tissues. We hypothesised that reabsorption is absent in nectaries possessing MST. The fluorochrome lucifer yellow (LYCH) was applied to standing nectar of two floral and extrafloral glands of distantly related species, and then emission spectra from nectary sections were systematically analysed using confocal microscopy. Passive uptake of LYCH via the stalk cells to the nectary tissues occurred in all MST examined. Moreover, we present evidence of nectar reabsorption in extrafloral nectaries, demonstrating that LYCH passed the stalk cells of MST, although it did not reach the deepest nectary tissues. Identical (control) experiments performed with neutral red (NR) demonstrated no uptake of this stain by actively secreting MST, whereas diffusion of NR did occur in plasmolysed MST of floral nectaries at the post‐secretory phase, indicating that nectar reabsorption by MST is governed by stalk cell physiology. Interestingly, non‐secretory trichomes failed to reabsorb nectar. The role of various nectary components is discussed in relation to the control of nectar reabsorption by secretory trichomes.     

Floral biology of Salvia stachydifolia,a species visited by bees and birds: connecting sexual phases,nectar dynamics and breeding system to visitors’ behaviour

一种由蜂类和鸟类传粉的鼠尾草属植物的花生物学：建立了有性阶段、花蜜动态过程和 繁育系统与访花行为的联系 在对传粉综合征的认知过程中,人们已经意识到共享某类传粉媒介的植物间的花表型中存在着适应性趋同的现象。然而,虽然许多植物都表现出了与特定综合征相关的性状,但它们的访花传粉者却不止一种。这种情况可能意味着传粉媒介的变化,或者可能形成了一种可适应不同传粉媒介的稳定情况。此前在鼠尾草属Salvia  stachydifolia 中开展的一项研究表明,该物种的花形状可以最大限度地提升蜜蜂和蜂鸟的传粉效果。在本文中,我们研究了该物种的花生物学的另外3个方面：有性阶段、花蜜动态过程和繁育系统,并探讨了它们与传粉者行为之间的联系,以了解该物种在这3个方面上对蜜蜂和/或蜂鸟传粉的适应性变化。我们以某一温室种群为研究对象,对其在5种不同传粉方式下的繁育系统进行了刻画。为了确定有性阶段,我们分别对花开、花药开裂、花冠掉落和柱头可授性的情况进行了记录。此外,我们还对花蜜体积和浓度在一整天的动态变化进行了表征。最后,为了确定传粉者的 组成和访花模式,我们开展了实地观测并记录传粉者的行为。研究结果显示,S. stachydifolia 是部分雄蕊 先成熟且可自交,但自由授粉植株的繁殖成功率最高,表明繁殖过程主要取决于传粉者的活动。熊蜂属Bombus opifex (一种大黄蜂)是最常见的访花者,但在清晨和黄昏时占主导地位的访花者则是红尾慧星蜂鸟(Sappho sparganura)。花蜜常见于大黄蜂授粉的情况。我们认为蜜蜂-蜂鸟混合访花的模式构成了一种不稳定的进化情形,使得S.  stachydifolia 成为一种理想的研究对象,用以了解传粉媒介发生变化的生态环境。     

The distribution of standing crop of nectar: what does it really tell us?

Summary Brink (1982) characterizes the distribution of standing crop of nectar for Delphinium nelsonii as bonanzablank, based on comparison with a Poisson. He then discusses possible effects of standing crop variability on pollinator foraging behavior. We disagree with the use of the Poisson and the resulting conclusions. The expected distribution should not be based on doling out random amounts of nectar to flowers, but based on random return times to flowers by pollinators (elapsed time=nectar accumulated). When this model is used, standing crop variance does not differ markedly from expectation. What differences do exist can be accounted for by variability in nectar production rates of individual plants. We also take issue with the use of the bonanza-blank terminology. As originally formulated this refers to nectar production differences within a plant rather than standing crop differences among plants.     

Why eat extrafloral nectar? Understanding food selection by Coleomegilla maculata (Coleoptera: Coccinellidae)

Methods of increasing predator abundance within a habitat include the incorporation of non-prey food items, yet the influence of this on predation intensity toward herbivores remains unknown. In order to gain an understanding of nectar feeding in the predaceous beetle, Coleomegilla maculata (DeGeer), laboratory studies were conducted evaluating prey consumption in the presence of extrafloral nectaries. The physiology of beetles with access to prey only and a mixed diet were compared. To elucidate results of beetle physiology, Y-tube olfactometer studies were conducted and preferences between food types evaluated. Coleomegilla maculata females consumed 9 % fewer aphids when nectar was available. Lipid and glycogen content, as well as oocyte volume were not increased upon consumption of a mixed diet. Evaluation of predator behavior when offered both food resources together and separately demonstrated that extrafloral nectaries are attractive.     

Do artificial nectar feeders affect bat–plant interactions in an Ecuadorian cloud forest?

Plant–pollinator interactions are critical to ecosystems. However, when artificial nectar feeders are available in an area, they could draw pollinators away from plants. We tested the effects of artificial nectar feeders in an Ecuadorian cloud forest on four aspects of bat–plant interactions: (1) bat relative abundance; (2) bat pollen loads; (3) flower visitation rates, and (4) breeding success of a bat‐pollinated species (Burmeistera glabrata). We divided the study site into areas close to (~30 m) and far from (~500 m) three different feeder sites. At each distance, we captured nectar bats (Anoura caudifer, Anoura cultrata, and Lonchophylla robusta) to estimate their relative abundance and to collect pollen from fur and fecal samples. We also videotaped flowers to estimate bat visitation rates and recorded different breeding success variables of B. glabrata. We found that areas close to feeders have higher relative bat abundance by a factor of 40. In spite of this, the presence of feeders did not affect bat pollen loads, nor the flower visitation rates and breeding success of B. glabrata. Interestingly, there were differences in pollen loads between the three bat species, in that L. robusta individuals rarely carried pollen and were only captured near feeders.     

Spatial fragrance patterns in flowers of Silene latifolia: Lilac compounds as olfactory nectar guides?

Floral odour can differ qualitatively and quantitatively between different parts of the flowers, and these spatial fragrance patterns within the flowers can be used by pollinators for orientation on flowers. Here we present results of spatial fragrance patterns within flowers of the dioecious Silene latifolia (Caryophyllaceae). Volatiles were collected and analysed using a highly sensitive dynamic headspace method, which allows dramatically reducing the sample time. From all flower parts, especially the petals and the anthophore emitted the typical flower volatiles of S. latifolia. However, compounds emitted from the petals differed from compounds emitted by the anthophore. The anthophore emitted the monoterpenoids lilac aldehydes and alcohols, whereas, all other typical scent compounds (e.g. benzoids, other monoterpenoids) were emitted by the petals. Lilac aldehydes are known to be behaviourally very attractive for noctuid moths, and they may serve as nectar guides in S. latifolia.     

Does acoustic priming ‘sweeten the pot’ of floral nectar?

A recent claim that evening primrose flowers adaptively secrete nectar in response to vibrations from hovering bees lacks supporting evidence. The authors fail to demonstrate that bees can access the concealed nectar and that their visits enhance plant fitness. Reanalysis of the authors’ data raises additional concerns about their conclusions.