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

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

Nectar secretion dynamic links pollinator behavior to consequences for plant reproductive success in the ornithophilous mistletoe Psittacanthus robustus

The mistletoe Psittacanthus robustus was studied as a model to link flower phenology and nectar secretion strategy to pollinator behaviour and the reproductive consequences for the plant. The bright‐coloured flowers presented diurnal anthesis, opened asynchronously throughout the rainy season and produced copious dilute nectar as the main reward for pollinators. Most nectar was secreted just after flower opening, with little sugar replenishment after experimental removals. During the second day of anthesis in bagged flowers, the flowers quickly reabsorbed the offered nectar. Low values of nectar standing crop recorded in open flowers can be linked with high visitation rates by bird pollinators. Eight hummingbirds and two passerines were observed as potential pollinators. The most frequent flower visitors were the hummingbirds Eupetomena macroura and Colibri serrirostris, which actively defended flowering mistletoes. The spatial separation between anthers, stigma and nectar chamber promotes pollen deposition on flapping wings of hovering hummingbirds that usually probe many flowers per visit. Seed set did not differ between hand‐, self‐ and cross‐pollinated flowers, but these treatments set significantly more seeds than flowers naturally exposed to flower visitors. We suggest that the limitation observed in the reproductive success of this plant is not related to pollinator scarcity, but probably to the extreme frequency of visitation by territorial hummingbirds. We conclude that the costs and benefits of plant reproduction depend on the interaction strength between flowers and pollinators, and the assessment of nectar secretion dynamics, pollinator behaviour and plant breeding system allows clarification of the complexity of such associations.     

Reproductive biology of a hummingbird‐pollinated Billbergia: light influence on pollinator behaviour and specificity in a Brazilian semi‐deciduous forest

• Ornithophily has evolved in parallel several times during evolution of angiosperms. Bird pollination is reported for 65 families, including Bromeliaceae. One of the most diverse bromeliad is Billbergia, which comprises species pollinated mainly by hummingbirds.
• Based on investigations on flowering phenology, morpho‐anatomy, volume and concentration of nectar, pollinators and breeding system, this paper explores the reproductive biology and pollinator specificity of B. distachia in a mesophytic semi‐deciduous forest of southeastern Brazil.
• The results have show that B. distachia is pollinated by a single species of hermit hummingbird, Phaethornis eurynome, which search for nectar produced by a septal nectary, where the secretory tissue is located above the placenta. The species is self‐incompatible. The combination of pollinator specificity, due to long corolla tubes that exclude visitation of short‐billed hummingbirds, complete self‐incompatibility and non‐territorial behaviour of pollinators, it is very important to reduce pollen loss and increase gene flow within population.
• Our results indicate that studies on pollination biology and reproduction are essential to understand the evolutionary history of pollination systems of plants since, at least in Billbergia, variation in the pollinator spectrum has been recorded for different habitats among Brazilian forests. Furthermore, according to our data, foraging of Phaethornis on flowers is independent of air temperature and humidity, while the main factor influencing hummingbird visitation is daylight. Considering current knowledge on climatic parameters influencing hummingbird foraging, pollination and reproductive biology of Neotropical flora and environment of the hermit hummingbird in tropical forests, new insights on plant–pollinator interaction are provided.

     

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.     

Can short‐billed nectar thieving sunbirds replace long‐billed sunbird pollinators in transformed landscapes?

• Pollinator specialisation through exploitation barriers (such as long floral tubes) does not necessarily mean a lack of pollination when the favoured pollinator is rare or absent. Theory predicts that suboptimal visitors will contribute to plant reproduction in the absence of the most effective pollinator. Here I address these questions with Chasmanthe floribunda a long‐tubed plant species in the Cape Floristic Region, which is reliant on one species of pollinator, the long‐billed Malachite Sunbird. In contrast to short‐billed sunbirds, the Malachite Sunbird occurs in lower abundance or is absent in transformed landscapes. Short‐billed sunbirds rob and thieve nectar from long‐tubed flowers, but their potential contribution towards pollination is unknown.
• Experiments assessing seed set after single flower visits were performed to determine whether thieving short‐billed sunbirds can act as substitute pollinators. To determine whether short‐billed sunbirds reduce pollen limitation in transformed areas, pollen supplementation was done by hand and compared to natural fruit set.
• Short billed sunbirds are unable to act as substitute pollinators, and seed set is significantly lower in the flowers that they visited, compared to flowers visited by long‐billed sunbirds. This is substantiated on a landscape scale, where fruit production in Chasmanthe floribunda could artificially be increased by 35% in transformed landscapes, but not so in natural areas.
• These findings have important consequences for the management and conservation of long‐tubed bird‐pollinated plant species that exist in recently transformed landscapes. The potential vulnerability of specialised plant species in transformed landscapes is highlighted.

     

Reloading the revolver – male fitness as a simple explanation for complex reward partitioning in Nasa macrothyrsa (Loasaceae,Cornales)

Reward partitioning and replenishment and specific mechanisms for pollen presentation are all geared towards the maximization of the number of effective pollinator visits to individual flowers. An extreme case of an apparently highly specialized plant–pollinator interaction with thigmonastic pollen presentation has been described for the morphologically complex tilt‐revolver flowers of Caiophora arechavaletae (Loasaceae) pollinated by oligolectic Bicolletes pampeana (Colletidae, Hymenoptera). We studied the floral biology of Nasa macrothyrsa (Loasaceae) in the field and in the glasshouse, which has very similar floral morphology, but is pollinated by polylectic Neoxylocopa bees (Apidae, Hymenoptera). We investigated the presence of thigmonastic anther presentation, visitor behaviour (pollinators and nectar robbers), co‐ordination of pollinator visits with flower behaviour and the presence of nectar replenishment. The aim of this study was to understand whether complex flower morphology and behaviour can be explained by a specialized pollination syndrome, or whether alternative explanations can be offered. The results showed that Nasa macrothyrsa has thigmonastic pollen presentation, i.e. new pollen is rapidly (<< 10 min) presented after a pollinator visit. Nectar secretion is independent of removal and averages 7–14 µL h^–1. The complex flowers, however, fail to exclude either native (hummingbirds) or introduced (honeybees) nectar robbers, nor does polylectic Neoxylocopa actively collect the pollen presented. The findings do not support a causal link between complex flower morphology and functionality in Loasaceae and a highly specialized pollination. Rapid pollen presentation is best explained by the pollen presentation theory: the large proportion of pollinators coming shortly after a previous visit find little nectar and are more likely to move on to a different plant. The rapid presentation of pollen ensures that all these valuable ‘hungry pollinators’ are dusted with small pollen loads, thus increasing the male fitness of the plant by increasing the likelihood of siring outcrossed offspring. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 124–131.     

Relative effectiveness of insects versus hummingbirds as pollinators of Rubiaceae plants across elevation in Dominica,Caribbean

• Most angiosperms rely on animal pollination for reproduction, but the dependence on specific pollinator groups varies greatly between species and localities. Notably, such dependence may be influenced by both floral traits and environmental conditions. Despite its importance, their joint contribution has rarely been studied at the assemblage level.
• At two elevations on the Caribbean island of Dominica, we measured the floral traits and the relative contributions of insects versus hummingbirds as pollinators of plants in the Rubiaceae family. Pollinator importance was measured as visitation rate (VR) and single visit pollen deposition (SVD), which were combined to assess overall pollinator effectiveness (PE).
• In the wet and cool Dominican highland, we found that hummingbirds were relatively more frequent and effective pollinators than insects, whereas insects and hummingbirds were equally frequent and effective pollinators at the warmer and less rainy midelevation. Furthermore, floral traits correlated independently of environment with the relative importance of pollinators, hummingbirds being more important in plant species having flowers with long and wide corollas producing higher volumes of dilute nectar.
• Our findings show that both environmental conditions and floral traits influence whether insects or hummingbirds are the most important pollinators of plants in the Rubiaceae family, highlighting the complexity of plant–pollinator systems.

     

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.     

Unpredictability of nectar nicotine promotes outcrossing by hummingbirds in Nicotiana attenuata

Many plants use sophisticated strategies to maximize their reproductive success via outcrossing. Nicotiana attenuata flowers produce nectar with nicotine at concentrations that are repellent to hummingbirds, increasing the number of flowers visited per plant. In choice tests using native hummingbirds, we show that these important pollinators learn to tolerate high‐nicotine nectar but prefer low‐nicotine nectar, and show no signs of nicotine addiction. Nectar nicotine concentrations, unlike those of other vegetative tissues, are unpredictably variable among flowers, not only among populations, but also within populations, and even among flowers within an inflorescence. To evaluate whether variations in nectar nicotine concentrations increase outcrossing, polymorphic microsatellite markers, optimized to evaluate paternity in native N. attenuata populations, were used to compare outcrossing in plants silenced for expression of a biosynthetic gene for nicotine production (Napmt1/2) and in control empty vector plants, which were antherectomized and transplanted into native populations. When only exposed to hummingbird pollinators, seeds produced by flowers with nicotine in their nectar had a greater number of genetically different sires, compared to seeds from nicotine‐free flowers. As the variation in nectar nicotine levels among flowers in an inflorescence decreased in N. attenuata plants silenced in various combinations of three Dicer‐like (DCL) proteins, small RNAs are probably involved in the unpredictable variation in nectar nicotine levels within a plant.     

Effects of nectar robbing on pollinator behavior and plant reproductive success of Pitcairnia angustifolia (Bromeliaceae)

Nectar robbers may have direct and indirect effects on plant reproductive success but the presence of nectar robbing is not proof of negative fitness effects. We combined census data and field experiments to disentangle the complex effects of nectar robbing on nectar production rates, pollinator behavior, pollen export, and female reproductive success of Pitcairnia angustifolia. Under natural conditions flowers were visited by four different animal species including a robber‐like pollinator and a secondary robber. Natural levels of nectar robbing ranged from 40 to 100%. Natural variation in nectar robbing was not associated with fruit set in any year whereas seed set was weakly positively associated for 1 year only. Artificial nectar robbing did not increase nectar production or concentration, did not affect the behavior of long‐billed hummingbirds, and when faced with artificially robbed flowers, these visitors behaved as secondary nectar robbers. The number of stigmas within a patch that received pollen dye analogs and the average distance traveled by these analogs were not significantly different between robbing treatments (robbed flowers versus unrobbed flowers), but the maximum distance traveled by these pollen analogs was higher when nectar robbing was not prevented. Overall, the proportion of robbed flowers on an inflorescence had a neutral effect to a weak positive effect on the reproduction of individual plants (i.e. positive association between nectar robbing and fruit set in 2002) even when it clearly changed the behavior of its most efficient pollinator potentially increasing the frequency of nectar robbing within a plant.     

Floral antagonists counteract pollinator‐mediated selection on attractiveness traits in the hummingbird‐pollinated Collaea cipoensis (Fabaceae)

Pollinator‐mediated selection toward larger and abundant flowers is common in naturally pollen‐limited populations. However, floral antagonists may counteract this effect, maintaining smaller‐ and few‐flowered individuals within populations. We quantified pollinator and antagonist visit rates and determined a multiplicative female fitness component from attacked and non‐attacked flowers of the Brazilian hummingbird‐pollinated shrub Collaea cipoensis to determine the selective effects of pollinators and floral antagonists on flower size and number. We predicted that floral antagonists reduce the female fitness component and thus exert negative selective pressures on flower size and number, counteracting the positive effects of pollinators. Pollinators, mainly hummingbirds, comprised 4% of total floral visitation, whereas antagonist ants and bees accounted for 90% of visitation. Nectar‐robbers involved about 99% of floral antagonist visit rates, whereas florivores comprised the remaining 1%. Larger and abundant flowers increased both pollinator and antagonist visit rates and the female fitness component significantly decreased in flowers attacked by nectar‐robbers and florivores in comparison to non‐attacked flowers. We detected that pollinators favored larger‐ and many‐flowered individuals, whereas floral antagonists exerted negative selection on flower size and number. This study confirms that floral antagonists reduce female plant fitness and this pattern directly exerts negative selective pressures on flower size and number, counteracting pollinator‐mediated selection on floral attractiveness traits.     

Variability in nectar production and standing crop, and their relation to pollinator visits in a Mediterranean shrub

Nectar standing crops in flowers within an individual plant are often highly variable. This variability may be a by-product of the foraging activity of insect pollinators. Alternatively, plants may be selected to produce highly variable rewards to reduce consecutive visitation by risk-averse pollinators, thus diminishing within-plant pollen transfer. This study evaluated the roles of pollinator control vs. plant control over nectar variability in the bee-pollinated shrub Rosmarinus officinalis L. (Lamiaceae). We sampled nectar production, standing crop and pollinator visits in three shrubs of one population over 17 days during one blooming season. Nectar production rates were highly variable (CV = 1.48), and increased after rainy days. Nectar standing crops were even more variable (CV = 2.16), decreased with increasing temperatures, and increased with time since the last rain. Pollinator visit rates decreased with variability in nectar standing crops, increased with flower number per shrub, and were unaffected by variability in nectar production rates. Repeated sampling of marked flowers revealed no correlation between their nectar standing crops and production rates. These findings support the role of reward variance in reducing pollinator visits, but suggest that plants are not in complete control of this variability. Rather, plant-generated variability can be modified by intensive foraging activity of pollinators. Such pollinator control over nectar variability is likely to reduce the selective advantage of plant-generated reward variation. Handling Editor: Neal Williams.     

Pollinators shift to nectar robbers when florivory occurs,with effects on reproductive success in Iris bulleyana (Iridaceae)

• Studies have indicated that florivory and nectar robbing may reduce reproductive success of host plants. However, whether and how these effects might interact when plants are simultaneously attacked by both florivores and nectar robbers still needs further investigation.
• We used Iris bulleyana to detect the interactions among florivory, nectar robbing and pollination, and moreover, their effects on plant reproductive success. Field investigations and hand‐pollination treatments were conducted on two experimental plots from a natural population, in which Experimental plot was protected from florivores and Control plot was not manipulated.
• The flower calyx was bitten by sawflies to consume the nectary, and three bumblebee species were pollinators. In addition, the short‐tongued pollinator, Bombus friseanus, was the only robber when there was a hole made by a sawfly. The bumblebee had significantly shortened flower handling time when robbing, as compared to legitimate visits. Pollinator visitation and seed production decreased significantly in damaged flowers. However, seed production per flower after supplementary hand‐pollination did not differ significantly between damaged and undamaged flowers. Compared to the Experimental plot, bumblebees visited fewer flowers per plant in a foraging bout in the Control plot.
• The flowers damaged by florivory allowed B. friseanus to shift to a nectar robber. Florivory and nectar robbing collectively decreased plant reproductive success by consuming nectar resources, which may reduce attractiveness to pollinators of the damaged flowers. However, the changes in pollinator behaviour might be beneficial to the plant by reducing the risk of geitonogamous mating.

     

Specialised protagonists in a plant–pollinator interaction: the pollination of Blumenbachia insignis (Loasaceae)

• Analyses of resource presentation, floral morphology and pollinator behaviour are essential for understanding specialised plant‐pollinator systems. We investigated whether foraging by individual bee pollinators fits the floral morphology and functioning of Blumenbachia insignis, whose flowers are characterised by a nectar scale‐staminode complex and pollen release by thigmonastic stamen movements.
• We described pollen and nectar presentation, analysed the breeding system and the foraging strategy of bee pollinators. We determined the nectar production pattern and documented variations in the longevity of floral phases and stigmatic pollen loads of pollinator‐visited and unvisited flowers.
• Bicolletes indigoticus (Colletidae) was the sole pollinator with females revisiting flowers in staminate and pistillate phases at short intervals, guaranteeing cross‐pollen flow. Nectar stored in the nectar scale‐staminode complex had a high sugar concentration and was produced continuously in minute amounts (~0.09 μl·h^?1). Pushing the scales outward, bees took up nectar, triggering stamen movements and accelerating pollen presentation. Experimental simulation of this nectar uptake increased the number of moved stamens per hour by a factor of four. Flowers visited by pollinators received six‐fold more pollen on the stigma than unvisited flowers, had shortened staminate and pistillate phases and increased fruit and seed set.
• Flower handling and foraging by Bicolletes indigoticus were consonant with the complex flower morphology and functioning of Blumenbachia insignis. Continuous nectar production in minute quantities but at high sugar concentration influences the pollen foraging of the bees. Partitioning of resources lead to absolute flower fidelity and stereotyped foraging behaviour by the sole effective oligolectic bee pollinator.

     

Main sugar composition of floral nectar in three species groups of Scrophularia (Scrophulariaceae) with different principal pollinators

In some angiosperm groups, a parallelism between nectar traits and pollination syndromes has been demonstrated, whereas in others there is not such relationship and it has been explained as due to phylogenetic constraints. However, nectar trait information remains scarce for many plant groups. This paper focuses on three groups of Scrophularia species, with different flower sizes and principal pollinators, to find out whether nectar sugar composition is determined by pollinator type or reflects taxonomic affinities. Since the species we examined have protogynous flowers, and gender bias in nectar sugar composition has been noted in few plant groups, we also investigated whether sexual phase influenced Scrophularia nectar composition. The sugar composition was found to be similar in all species, having high‐sucrose nectar, except for the Macaronesian Scrophularia calliantha, which was the only species with balanced nectar; this last kind of nectar could be associated with the high interaction rates observed between S. calliantha and passerine birds. The nectar sugar composition (high in sucrose) was unrelated to the principal pollinator group, and could instead be considered a conservative taxonomic trait. No gender bias was observed between functionally female and male flowers for nectar volume or concentration. However, sexual phase significantly affected sucrose percentage in the largest‐flowered species, where the female phase flowers had higher sucrose percentages than the male phase flowers.     

Plant–hummingbird interactions in the West Indies: floral specialisation gradients associated with environment and hummingbird size

Floral phenotype and pollination system of a plant may be influenced by the abiotic environment and the local pollinator assemblage. This was investigated in seven plant–hummingbird assemblages on the West Indian islands of Grenada, Dominica and Puerto Rico. We report all hummingbird and insect pollinators of 49 hummingbird-pollinated plant species, as well as six quantitative and semi-quantitative floral characters that determine visitor restriction, attraction and reward. Using nonmetric multidimensional scaling analysis, we show that hummingbird-pollinated plants in the West Indies separate in floral phenotypic space into two gradients—one associated with the abiotic environment and another with hummingbird size. Plants pollinated by large, long-billed hummingbirds had flowers with long corolla tube, large amounts of nectar and showy orange-red colouration. These attracted few or no insect species, whereas plants pollinated by small, short-billed hummingbirds were frequently pollinated by insects, particularly lepidopterans. The separation of plants related to environmental factors showed that species in the wet and cold highlands produced large amounts of dilute nectar, possessed no or a weak odour, and were associated with few insects, particularly few hymenopterans, compared to plants in the dry and warm lowlands. The most specialised hummingbird-pollinated plants are found in the West Indian highlands where they are pollinated by mainly large, long-billed hummingbirds. At the other extreme, highly generalised plants growing in the dry and warm lowlands are pollinated by small, short-billed hummingbirds and numerous insect species. This illustrates that, even within the hummingbird-pollinated flora, pollination syndrome and the degree of specialisation may vary tremendously depending on pollinator morphology and environment. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Nectar yeasts enhance the interaction between Clematis akebioides and its bumblebee pollinator

• It has been hypothesised that intense metabolism of nectar‐inhabiting yeasts (NIY) may change nectar chemistry, including volatile profile, which may affect pollinator foraging behaviours and consequently plant fitness. However, empirical evidence for the plant–microbe–pollinator interactions remains little known.
• To test this hypothesis, we use a bumblebee‐pollinated vine Clematis akebioides endemic to southwest China as an experimental model plant. To quantify the incidence and density of Metschnikowia reukaufii, a cosmopolitan NIY in floral nectar, a combination of yeast cultivation and microscopic cell‐counting method was used. To examine the effects of NIY on plant–pollinator interactions, we used real flowers filled with artificial nectar with or without yeast cells. Then the volatile metabolites produced in the yeast‐inoculated nectar were analysed with coupled gas chromatography and mass spectrometry (GC‐MS).
• On average 79.3% of the C. akebioides flowers harboured M. reukaufii, and cell density of NIY was high to 7.4 × 10⁴ cells mm^?3. In the field population, the presence of NIY in flowers of C. akebioides increased bumblebee (Bombus friseanus) pollinator visitation rate and consequently seed set per flower. A variety of fatty acid derivatives produced by M. reukaufii may be responsible for the above beneficial interactions.
• The volatiles produced by the metabolism of M. reukaufii may serve as an honest signal to attract bumblebee pollinators and indirectly promote the female reproductive fitness of C. akebioides, forming a potentially tripartite plant–microbe–pollinator mutualism.

     

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.     

Convergence beyond flower morphology? Reproductive biology of hummingbird‐pollinated plants in the Brazilian Cerrado

Convergent reproductive traits in non‐related plants may be the result of similar environmental conditions and/or specialised interactions with pollinators. Here, we documented the pollination and reproductive biology of Bionia coriacea (Fabaceae), Esterhazya splendida (Orobanchaceae) and Ananas ananassoides (Bromeliaceae) as case studies in the context of hummingbird pollination in Cerrado, the Neotropical savanna of Central South America. We combined our results with a survey of hummingbird pollination studies in the region to investigate the recently suggested association of hummingbird pollination and self‐compatibility. Plant species studied here differed in their specialisation for ornithophily, from more generalist A. ananassoides to somewhat specialist B. coriacea and E. splendida. This continuum of specialisation in floral traits also translated into floral visitor composition. Amazilia fimbriata was the most frequent pollinator for all species, and the differences in floral display and nectar energy availability among plant species affect hummingbirds' behaviour. Most of the hummingbird‐pollinated Cerrado plants (60.0%, n = 20), including those studied here, were self‐incompatible, in contrast to other biomes in the Neotropics. Association to more generalist, often territorial, hummingbirds, and resulting reduced pollen flow in open savanna areas may explain predominance of self‐incompatibility. But it is possible that mating system is more associated with the predominance of woody hummingbird plants in the Cerrado plant assemblage than to the pollination system itself.     

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.