Mauritian coloured nectar no longer a mystery: a visual signal for lizard pollinators

Most floral nectars are clear as water, and the enigmatic coloured nectar in three endemic plant species in Mauritius has puzzled scientists studying it. One hypothesis about the possible ecological function of coloured nectar is that it serves as a visual signal for pollinators. Recent studies have shown that at least two of the three Mauritian plant species with coloured nectar are visited and pollinated by endemic Phelsuma geckos. We here provide experimental evidence for the visual signal hypothesis by showing that Phelsuma ornata geckos prefer coloured over clear nectar in artificial flowers. In flowering plants, coloured nectar could additionally function as an honest signal that allows pollinators to assert the presence and judge the size of a reward prior to flower visitation, and to adjust their behaviour accordingly, leading to increased pollinator efficiency. Our study provides a first step in understanding this rare and intriguing floral trait.     

Risk‐averse inflorescence departure in hummingbirds and bumble bees: could plants benefit from variable nectar volumes?

Most hermaphroditic, many-flowered plants should suffer reduced fitness from within-plant selfing (geitonogamy). Large inflorescences are most attractive to pollinators, but also promote many flower visits during a single plant visit, which may increase selfing and decrease pollen export. A plant might avoid the negative consequences of attractiveness through modification of the floral display to promote fewer flower visits, while retaining attractiveness. This report shows that increasing only the variance in nectar volume per flower results in fewer flower visits per inflorescence by wild hummingbirds ( Selasphorus rufus ) and captive bumble bees ( Bombus flavifrons ) foraging on artificial inflorescences. Inflorescences were either constant (all flowers contained the same nectar volume) or variable (half the flowers were empty, the other half contained twice as much nectar as in the constant flowers). Both types of inflorescence were simultaneously available to foragers. Risk-averse foraging behaviour was expressed as a patch departure preference: birds and bees visited fewer flowers on variable inflorescences, and this preference was expressed when resource variability could be determined only by concurrent sampling. When variance treatments were clearly labelled with colour and offered to hummingbirds, the departure effect was maintained; however, when preference was measured by inflorescence choice, birds did not consistently prefer to visit constant inflorescences. The reduced visitation lengths on variable inflorescences by both birds and bees documented in this study imply that variance in nectar production rates within inflorescences may represent an adaptive trait to avoid the costs of geitonogamy.     

Coloured and Toxic Nectar: Feeding Choices of the Madagascar Giant Day Gecko,Phelsuma grandis

Coloured nectar is a rare phenomenon best known from islands and insular habitats. Islands are also known for lizard pollination, where coloured nectar potentially acts as a visual cue to attract pollinators, advertising the sweet reward. However, nectar may also contain secondary metabolites with toxic or deterrent effects. The aim of this study was to determine which factors are important as artificial nectar choice determinants to the Madagascar giant day gecko, Phelsuma grandis, an island pollinator: artificial nectar colour, artificial nectar colour saturation, artificial nectar conspicuousness and/or the presence of the alkaloid nicotine. Coloured artificial nectar and the darkest artificial nectar colour saturation were found to be important visual cues for the geckos, while the contrast between artificial nectar and petal colour was not. Geckos were deterred only by high nicotine concentrations (1000 μm in 0.63 m sucrose) and may even prefer low nicotine concentrations to sucrose‐only solutions. Given their overall fondness for sugar solutions, Madagascar giant day geckos are likely to be important pollinators of Malagasy plant species that produce enough nectar to attract them, and plants with coloured nectar and/or secondary metabolites may have evolved those traits to attract the geckos in particular.     

Gloss,Colour and Grip: Multifunctional Epidermal Cell Shapes in Bee- and Bird-Pollinated Flowers

Flowers bear the function of filters supporting the attraction of pollinators as well as the deterrence of floral antagonists. The effect of epidermal cell shape on the visual display and tactile properties of flowers has been evaluated only recently. In this study we quantitatively measured epidermal cell shape, gloss and spectral reflectance of flowers pollinated by either bees or birds testing three hypotheses: The first two hypotheses imply that bee-pollinated flowers might benefit from rough surfaces on visually-active parts produced by conical epidermal cells, as they may enhance the colour signal of flowers as well as the grip on flowers for bees. In contrast, bird-pollinated flowers might benefit from flat surfaces produced by flat epidermal cells, by avoiding frequent visitation from non-pollinating bees due to a reduced colour signal, as birds do not rely on specific colour parameters while foraging. Moreover, flat petal surfaces in bird-pollinated flowers may hamper grip for bees that do not touch anthers and stigmas while consuming nectar and thus, are considered as nectar thieves. Beside this, the third hypothesis implies that those flower parts which are vulnerable to nectar robbing of bee- as well as bird-pollinated flowers benefit from flat epidermal cells, hampering grip for nectar robbing bees. Our comparative data show in fact that conical epidermal cells are restricted to visually-active parts of bee-pollinated flowers, whereas robbing-sensitive parts of bee-pollinated as well as the entire floral surface of bird-pollinated flowers possess on average flat epidermal cells. However, direct correlations between epidermal cell shape and colour parameters have not been found. Our results together with published experimental studies show that epidermal cell shape as a largely neglected flower trait might act as an important feature in pollinator attraction and avoidance of antagonists, and thus may contribute to the partitioning of flower-visitors.     

Foraging efficiency and size matching in a plant–pollinator community: the importance of sugar content and tongue length

A long‐standing question in ecology is how species interactions are structured within communities. Although evolutionary theory predicts close size matching between floral nectar tube depth and pollinator proboscis length of interacting species, such size matching has seldom been shown and explained in multispecies assemblages. Here, we investigated the degree of size matching among Asteraceae and their pollinators and its relationship with foraging efficiency. The majority of pollinators, especially Hymenoptera, choose plant species on which they had high foraging efficiencies. When proboscides were shorter than nectar tubes, foraging efficiency rapidly decreased because of increased handling time. When proboscides were longer than nectar tubes, a decreased nectar reward rather than an increased handling time made shallow flowers more inefficient to visit. Altogether, this led to close size matching. Overall, our results show the importance of nectar reward and handling time as drivers of plant–pollinator network structure.     

Are insects flower constant because they use search images to find flowers?

Many insects which gather nectar or pollen exhibit flower constancy, a learned fidelity to a particular species of plant. Recent studies suggest that foraging insects may use a perceptual mechanism akin to a search image to detect flowers, in a manner analogous to the way that predators search for prey. This has emerged as an alternative (but not mutually exclusive) explanation for flower constancy to that proposed by Darwin, who suggested that it may result from a limited ability to learning or remember the handling skills appropriate for particular flowers. However, search images are thought to be a mechanism for locating cryptic prey. Plants which are pollinated by animals have evolved brightly coloured flowers to attract the attention of their pollinators. It thus seems implausible to argue that flowers may actually be cryptic. One possible explanation for this apparent contradiction is that flowers are effectively cryptic when viewed against a background which contains many other flowers of similar colour. I present experimental evidence which suggests that a background of flowers of similar colour does reduce foraging efficiency of bumblebees, but that a background of dissimilarly coloured flowers has no effect. This I interpret as evidence that flowers may be cryptic, suggesting that pollinators may indeed use a search image in location of flowers. However, the relative importance of constraints on foragers' abilities to locate flowers versus their abilities to handle them as causes of flower constancy remain to be elucidated.     

Bird pollinators differ in their tolerance of a nectar alkaloid

Although the function of nectar is to attract and reward pollinators, secondary metabolites produced by plants as anti‐herbivore defences are frequently present in floral nectars. Greater understanding is needed of the effects of secondary metabolites in nectar on the foraging behaviour and performance of pollinators, and on plant–pollinator interactions. We investigated how nectar‐feeding birds, both specialist (white‐bellied sunbirds Cinnyris talatala) and generalist (dark‐capped bulbuls Pycnonotus tricolor and Cape white‐eyes Zosterops virens), respond to artificial nectar containing the alkaloid nicotine, present in nectar of Nicotiana species. Preference tests were carried out with a range of nicotine concentrations (0.1–300 μM) in two sucrose concentrations (0.25 and 1 M), and for bulbuls also in two sugars (sucrose and hexose). In addition, we measured short‐term feeding patterns in white‐bellied sunbirds that were offered nicotine (0–50 μM) in 0.63 M sucrose. Both nicotine and sugar concentrations influenced the response of bird pollinators to nicotine. The birds showed dose‐dependent responses to nicotine; and their tolerance of high nicotine concentrations was reduced on the dilute 0.25 M sucrose diet, on which they increased consumption to maintain energy intake. White‐bellied sunbirds decreased both feeding frequency and feeding duration as the nicotine concentration in artificial nectar increased. Of the three species, bulbuls showed the highest tolerance for nicotine, and sugar type (sucrose or hexose) had no effect. The indifference of bulbuls to nicotine may be related to their primarily frugivorous diet. However, the response of white‐eyes to nicotine in the dilute sucrose solution was very similar to that of sunbirds, even though white‐eyes are generalist nectar‐feeders. Additional testing of other avian nectarivores and different secondary metabolites is required to further elucidate whether generalist bird pollinators, which utilise dilute nectars in which secondary metabolites have stronger deterrent effects, are more tolerant of ‘toxic’ nectar.     

Intra‐floral resource partitioning between endemic and invasive flower visitors: consequences for pollinator effectiveness

1. Sympatric flower visitor species often partition nectar and pollen and thus affect each other's foraging pattern. Consequently, their pollination service may also be influenced by the presence of other flower visiting species. Ants are solely interested in nectar and frequent flower visitors of some plant species but usually provide no pollination service. Obligate flower visitors such as bees depend on both nectar and pollen and are often more effective pollinators. 2. In Hawaii, we studied the complex interactions between flowers of the endemic tree Metrosideros polymorpha (Myrtaceae) and both, endemic and introduced flower‐visiting insects. The former main‐pollinators of M. polymorpha were birds, which, however, became rare. We evaluated the pollinator effectiveness of endemic and invasive bees and whether it is affected by the type of resource collected and the presence of ants on flowers. 3. Ants were dominant nectar‐consumers that mostly depleted the nectar of visited inflorescences. Accordingly, the visitation frequency, duration, and consequently the pollinator effectiveness of nectar‐foraging honeybees (Apis mellifera) strongly decreased on ant‐visited flowers, whereas pollen‐collecting bees remained largely unaffected by ants. Overall, endemic bees (Hylaeus spp.) were ineffective pollinators. 4. The average net effect of ants on pollination of M. polymorpha was neutral, corresponding to a similar fruit set of ant‐visited and ant‐free inflorescences. 5. Our results suggest that invasive social hymenopterans that often have negative impacts on the Hawaiian flora and fauna may occasionally provide neutral (ants) or even beneficial net effects (honeybees), especially in the absence of native birds.     

The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards

1.  The evolution of flowering plants has undoubtedly been influenced by a pollinator's ability to learn to associate floral signals with food. Here, we address the question of 'why' flowers produce scent by examining the ways in which olfactory learning by insect pollinators could influence how floral scent emission evolves in plant populations.
2.  Being provided with a floral scent signal allows pollinators to learn to be specific in their foraging habits, which could, in turn, produce a selective advantage for plants if sexual reproduction is limited by the income of compatible gametes. Learning studies with honeybees predict that pollinator-mediated selection for floral scent production should favour signals which are distinctive and exhibit low variation within species because these signals are learned faster. Social bees quickly learn to associate scent with the presence of nectar, and their ability to do this is generally faster and more reliable than their ability to learn visual cues.
3.  Pollinators rely on floral scent as a means of distinguishing honestly signalling flowers from deceptive ones. Furthermore, a pollinator's sensitivity to differences in nectar rewards can bias the way that it responds to floral scent. This mechanism may select for flowers that provide olfactory signals as an honest indicator of the presence of nectar or which select against the production of a detectable scent signal when no nectar is present.
4.  We expect that an important yet commonly overlooked function of floral scent is an improvement in short-term pollinator specificity which provides an advantage to both pollinator and plant over the use of a visual signal alone. This, in turn, impacts the evolution of plant mating systems via its influence on the species-specific patterns of floral visitation by pollinators.     

An Assemblage of Hummingbird-pollinated Flowers in a Montane Forest in Southeastern Brazil

Relationships between ornithophilous flowers and hummingbirds have been little studied in southern South America, where hummingbird species richness is low. We studied an ornithophilous flower assemblage and the hummingbird pollinators in a montane forest in southeastern Brazil. Twenty-three native hummingbird-pollinated plant species in 21 genera and 14 families were observed. Bromeliaceae, Fabaceae, Gesneriaceae, and Lobeliaceae are represented by more than one species within the assemblage. Flower shapes vary from narrow tube to bowl-shape, but tubular flowers prevail. The variety of flower shapes and sizes results in diverse pollen placement on the body parts of hummingbird visitors, although pollen is deposited mostly on the bill. Sugar concentration in nectar averages 22.1%, and nectar volume per flower averages 16.9 μl. The plant populations bloom for one month to year-round, and their flowering approaches the steady-state pattern. Four flower subsets may be defined within the assemblage, each subset related to the bill size and foraging habits of the most frequent bird visitor. Of the six species of hummingbirds recorded at the study site, four are common and largely resident. The four hummingbirds differ in bill size, body mass, and favoured foraging sites, attributes which reflect their favoured flower subsets. One hermit and one trochiline hummingbird share most of the flower species they use, these two birds being the major pollinators within the flower assemblage. This montane forest community may be viewed as medium-rich in ornithophilous flower species and poor in hummingbird species.     

Nectar robbing in Ipomopsis aggregata : effects on pollinator behavior and plant fitness

Hummingbirds foraging in alpine meadows of central Colorado, United States, face a heterogeneous distribution of nectar rewards. This study investigated how variability in nectar resources caused by nectar-robbing bumblebees affected the foraging behavior of hummingbird pollinators and, subsequently, the reproductive success of a host plant (Ipomopsis aggregata). We presented hummingbirds with experimental arrays of I. aggregata and measured hummingbird foraging behavior as a function of known levels of nectar robbing. Hummingbirds visited significantly fewer plants with heavy nectar robbing (over 80% of available flowers robbed) and visited fewer flowers on those plants. These changes in hummingbird foraging behavior resulted in decreased percent fruit set as well as decreased total seed set in heavily robbed plants. These results indicate that hummingbird avoidance of nectar-robbed plants and flowers reduces plant fitness components. In addition, our results suggest that the mutualisms between pollinators and host plants may be affected by other species, such as nectar robbers. Received: 22 April 1998 / Accepted: 12 May 1998     

Variable responses of hawkmoths to nectar-depleted plants in two native Petunia axillaris (Solanaceae) populations

Pollination success of deceptive orchids is affected by the density and distribution of nectar providing plant species and overall plant density. Here we extended the framework of how plant density can affect pollination to examine how it may promote the success of plant intraspecific cheaters. We compared hawkmoth behaviour in two native populations of Petunia axillaris, where we simultaneously offered rewarding and manually depleted P. axillaris. We asked whether pollinator foraging strategies change as a function of plant density and whether such changes may differentially affect nectarless plants. We observed the first choice and number of flowers visited by pollinators and found that in the dense population, pollinators visited more flowers on rewarding plants than on nectar-depleted plants. In the sparse population, such discrimination was absent. As we found no differences in nectar volume between plants of the two populations, the observed differences in plant density may be temporal. We reason that if differences were more permanent, an equivalent of the remote habitat hypothesis prevails: in a sparse population, cheating plants benefit from the absence of inter- and intraspecific competitors because pollinators tend to visit all potential resources. In a denser population, a pollinator’s optimal foraging strategy involves more selectivity. This would cause between-plant competition for pollinators in a pollinator-limited context, which applies to most hawkmoth-pollinated systems. We propose that nectar-provisioning of plants can be density-dependant, with cheaters able to persist in low density areas.     

Flower change in Oenothera drummondii Hooker as a response to pollinators' visits

Flower change in Oenothera drummondii Hooker as a response to pollinators' visits. The colour and shape of flowers of Oenothera drummondii change owing to senescence, pollination and/or nectar withdrawal. This phenomenon is interpreted as a signal emitted by the plant to 'inform' the potential pollinator of its new status as a rewardless flower. This method of signalling might be important for the pollinators in order to save energy in seeking the correct flowers and for the plant to ensure visits to those flowers that have not yet been visited.     

Flowers as islands: spatial distribution of nectar-inhabiting microfungi among plants of Mimulus aurantiacus, a hummingbird-pollinated shrub

Microfungi that inhabit floral nectar offer unique opportunities for the study of microbial distribution and the role that dispersal limitation may play in generating distribution patterns. Flowers are well-replicated habitat islands, among which the microbes disperse via pollinators. This metapopulation system allows for investigation of microbial distribution at multiple spatial scales. We examined the distribution of the yeast, Metschnikowia reukaufii, and other fungal species found in the floral nectar of the sticky monkey flower, Mimulus aurantiacus, a hummingbird-pollinated shrub, at a California site. We found that the frequency of nectar-inhabiting microfungi on a given host plant was not significantly correlated with light availability, nectar volume, or the percent cover of M. aurantiacus around the plant, but was significantly correlated with the location of the host plant and loosely correlated with the density of flowers on the plant. These results suggest that dispersal limitation caused by spatially nonrandom foraging by pollinators may be a primary factor driving the observed distribution pattern.     

Avoidance of an aposematically coloured butterfly by wild birds in a tropical forest

1. Birds are considered to be the primary selective agents for warning colouration in butterflies, and select for aposematic mimicry by learning to avoid brightly coloured prey after unpleasant experiences. It has long been thought that bright colouration plays an important role in promoting the avoidance of distasteful prey by birds. 2. The hypothesis that warning colouration facilitates memorability and promotes predator avoidance was tested by means of a field experiment using distasteful model butterflies. Artificial butterflies with a Heliconius colour pattern unknown to local birds were generated using bird vision models, either coloured or achromatic, and hung in tree branches in a tropical forest. Two sequential trials were conducted at each site to test avoidance by naïve and experienced predators. 3. There was a significant reduction in predation in the second trial. Also, coloured models were attacked less than achromatic models. Specifically, coloured butterflies were attacked significantly less in the second trial, but there was no significant decrease in predation on achromatic models. 4. The present results imply an important role for colour in enhancing aversion of aposematic butterflies. It has also been demonstrated that previous experience of distasteful prey can lead to enhanced avoidance in subsequent trials, supporting mimicry theory.     

Honey bees and wild pollinators differ in their preference for and use of introduced floral resources

Introduced plants may be important foraging resources for honey bees and wild pollinators, but how often and why pollinators visit introduced plants across an entire plant community is not well understood. Understanding the importance of introduced plants for pollinators could help guide management of these plants and conservation of pollinator habitat. We assessed how floral abundance and pollinator preference influence pollinator visitation rate and diversity on 30 introduced versus 24 native plants in central New York. Honey bees visited introduced and native plants at similar rates regardless of floral abundance. In contrast, as floral abundance increased, wild pollinator visitation rate decreased more strongly for introduced plants than native plants. Introduced plants as a group and native plants as a group did not differ in bee diversity or preference, but honey bees and wild pollinators preferred different plant species. As a case study, we then focused on knapweed (Centaurea spp.), an introduced plant that was the most preferred plant by honey bees, and that beekeepers value as a late‐summer foraging resource. We compared the extent to which honey bees versus wild pollinators visited knapweed relative to coflowering plants, and we quantified knapweed pollen and nectar collection by honey bees across 22 New York apiaries. Honey bees visited knapweed more frequently than coflowering plants and at a similar rate as all wild pollinators combined. All apiaries contained knapweed pollen in nectar, 86% of apiaries contained knapweed pollen in bee bread, and knapweed was sometimes a main pollen or nectar source for honey bees in late summer. Our results suggest that because of diverging responses to floral abundance and preferences for different plants, honey bees and wild pollinators differ in their use of introduced plants. Depending on the plant and its abundance, removing an introduced plant may impact honey bees more than wild pollinators.     

Colour similarity to rewarding model plants affects pollination in a food deceptive orchid, Orchis boryi

We studied the pollination of Orchis boryi at five different locations on the Greek mainland. Orchis boryi is food deceptive and obligatorily insect pollinated. Primary pollinators were Apis mellifera and Bombus spp., which foraged on rewarding plant species nearby and visited O. boryi in between. To analyse floral colour similarity among rewarding plants and O. boryi as perceived by bees, a model of bee colour vision was employed. For each food plant an index was calculated that described the probability of a bee foraging on it to subsequently choose an orchid flower. This choice probability correlated to colour distance according to the model of bee colour vision, indicating that bees chose the deceptive orchid more frequently if they foraged on more similarly coloured species. At different sites different plant species served as models. Bees foraging on food plants from which a high choice rate to the orchid was observed visited the orchid less often after approaching it than other bees, which is likely to reflect avoidance learning. In general, the pollination syndrome appears to be a generalized form of Batesian mimicry, in which similarity to rewarding plants determines reproductive success. As expected by negative density-dependent selection, individual fruit set and pollinia export rate correlated negatively with orchid density, but were unaffected by food plant density, orchid frequency, individual variation of labellum colour, labellum size, or mouth width of the flowers.     

Coloured nectar: distribution, ecology, and evolution of an enigmatic floral trait

While coloured nectar has been known to science at least since 1785, it has only recently received focused scientific attention. However, information about this rare floral trait is scattered and hard to find. Here, we document coloured nectar in 67 taxa worldwide, with a wide taxonomical and geographical distribution. We summarise what is currently known about coloured nectar in each of the lineages where it occurs. The most common nectar colours are in the spectrum from yellow to red, but also brown, black, green, and blue colours are found. Colour intensity of the nectar varies, sometimes even within one taxa, as does the level of contrast between flower petals and nectar. Coloured nectar has evolved independently throughout the angiosperms at least 15 times at the level of family, and is in many cases correlated with one or more of three parameters: (1) vertebrate pollination, known or hypothesised, (2) insularity -- many species are from islands or insular mainland habitats, and (3) altitude -- many species are found at relatively high altitudes. We discuss the evolution and speculate on possible ecological functions of coloured nectar. Apart from being a non-functional, perhaps pleiotropic, trait, we present several hypotheses on possible ecological functions of coloured nectar. Firstly, for some plant species it can be interpreted as an honest signal, leading to high pollination efficiency. Secondly, it can function as a deterrent against nectar-thieves or inefficient pollinators, thus acting as a floral filter. Thirdly, nectar colour-pigments can have anti-microbial qualities that may protect the nectar in long-lived flowers. Neither of these possibilities are mutually exclusive. Recent studies have provided experimental evidence for the first two hypotheses, and we suggest promising avenues for future research into this little-known floral trait.     

Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbirds and bees

In order to compare the effectiveness of birds and insects as pollinators, we studied the floral biology of the bromeliad Aechmea nudicaulis (L.) Grisebach in the biome of the Atlantic rain forest, southern Brazil. On Santa Catarina Island, flowering extends from mid-September to the end of December, with diurnal anthesis. The reproductive system is obligatory xenogamy, thus pollinator-dependent. Flowers secrete 31.84 μl of nectar per day, with a mean sugar concentration of 23.2%. Highest nectar volume and sugar concentration occur at the beginning of anthesis. Most floral traits are characteristic for ornithophily, and nectar production appears to be adapted to the energy demand of hummingbirds. Continued secretion of the sucrose-dominated nectar attracts and binds visitors to inflorescences, strengthening trapline foraging behaviour. Experiments assessing seed set after single flower visits were performed with the most frequent visitors, revealing the hummingbird Thalurania glaucopis as the most effective pollen vector. In addition, bees are also functional pollinators, as substantiated by their high visitation frequency. We conclude that this pollination system is bimodal. Thus, there is redundancy in the pollination service provided by birds and bees, granting a high probability of successful reproduction in Ae. nudicaulis.     

Flower colour change in Banksia ilicifolia: A signal for pollinators

Both birds and insects visit yellow flower heads of Banksia ilicifolia rather than those in the pink or red phases. Birds carry most pollen. Substantial nectar and pollen rewards are present only in the yellow phase. The timing of flower colour change also corresponds to a decline in viability of presented pollen and stigma receptivity. Colour change is age-dependent rather than pollinator-induced. Bird visits to yellow or red heads are essentially determined by the availability of nectar in each rather than differences in their visibility. Fruit set is negligible in the absence of pollinators but still < 1% in their presence. Banksia ilicifolia has the smallest heads and is the most localized of five co-occurring and partly co-flowering Banksia species. It is hypothesized that the restriction of flower colour change to B. ilicifolia increases the competitiveness of this species: bird visitors are directed to flower heads with abundant nectar, viable pollen and receptive stigmas, foraging and pollination efficiency thereby being enhanced without a marked reduction in long-distance attractiveness of the tree to potential pollinators.