Reproductive ecology of distylous Palicourea Padifolia (Rubiaceae) in a tropical montane cloud forest. I. Hummingbirds' effectiveness as pollen vectors

The adaptiveness of distyly has been typically investigated in terms of its female function, specifically pollen receipt. However, pollen loads on stigmas can only provide moderate support for Darwin's hypothesis of the promotion of legitimate crosses. To determine the effectiveness of hummingbirds as pollen vectors between floral morphs and the consequences in terms of male (pollen transfer) and female function (pollen receipt) in Palicourea padifolia (Rubiaceae), floral visitors, their foraging modes, and temporal patterns of floral visitation were observed and documented. Differences in pollen and stigma morphology, pollen flow, rates of pollen deposition, and/or stigmatic pollen loads were then evaluated for their contribution toward differences in reproductive output between floral morphs. A pollination experiment with stuffed hummingbirds that varied in bill size was done to evaluate the contribution of bill variation toward differences between floral morphs in pollen receipt and pollen transfer and female reproductive output. Anthers of long-styled flowers contained significantly more and smaller pollen grains than those of short-styled flowers, independently of corolla and anther lengths. The shape and orientation of the stigma lobes differed between morphs and were significantly longer among short-styled flowers. Hummingbird visitation rates did not differ significantly between floral morphs, and foraging movements from focal plants towards neighboring plants were independent of floral morph. Stigmatic pollen loads under field conditions and those after controlled hummingbird visitation, along with rates of pollen accumulation through the day indicated that stigmas of short-styled flowers receive proportionately more legitimate (intermorph) pollen grains than did those of long-styled flowers. However, the species of hummingbird was marginally significant in explaining variation in pollen deposition on stigmas. Lastly, intermorph pollinations of P. padifolia resulted in significant differences in fruit production between floral morphs, independent of pollination treatment and pollinator species; short-styled flowers proportionately developed almost twice the number of fruits developed by long-styled flowers.     

Hummingbird color preference within a natural hybrid population of Mimulus aurantiacus (Phrymaceae)

Hummingbird flowers are typically red in color but the reasons for this are not well understood. Relatively few studies have examined hummingbird flower color preferences under natural conditions in which flower color varies within a species. We recorded hummingbird visitation rates to flowers that vary in color from yellow to red in a natural hybrid population between red‐ and yellow‐flowered Mimulus aurantiacus subspecies. We also examined whether there were any correlations between color and flower size or nectar content. Finally, we reviewed the literature on hummingbird color choice tests using feeders and flowers. There were no correlations in this population between flower color and flower size, nectar volume, or sugar concentration. Nevertheless, hummingbirds undervisited the two most yellow color classes, overvisited orange flowers, and visited the two most red color classes in proportion to their frequency in the population. While Hummingbirds preferred flowers expressing red pigments to those that did not, the flowers with the most red hue were not the most attractive, as has been observed in similar studies with other species of Mimulus. While feeder studies generally fail to show hummingbird preference for red, all studies using flowers, including those that control all floral traits other than color, find consistent preference for red. Experiments are suggested that might help disentangle hypotheses for why hummingbirds exhibit this preference.     

Hummingbird diversity, food niche characters, and assemblage composition along a latitudinal precipitation gradient in the Bolivian lowlands

As for many other taxa, hummingbird diversity declines away from the equator, but the causes for this decline are still disputed and might involve, among others, climatic factors or the availability of food resources. Because hummingbirds are one of the classical examples for plant–animal coevolution, it has been proposed that the diversity of hummingbird assemblages might depend on the diversity of food plants available. We tested this hypothesis by studying the hummingbird assemblages and their food plants for 1 year at six sites along a 660-km-long transect in Bolivian lowland forests extending from the southernmost Amazonian rain forests to dry Chaco forests. Hummingbird diversity was higher in the northern three sites as compared to the southern ones, with an abrupt decline in species numbers and a corresponding change in taxonomic composition at the boundary from evergreen to drought deciduous forests. Hummingbird diversity and abundance were only weakly correlated to climatic factors or to the diversity of humming-visited flowers, but strongly to the seasonal abundance of flowers. The overlap in nectar diet between hummingbird species depended on the number of plant species: when numerous species were available, the hummingbirds segregated by feeding preferences, but when few flowers were available, all hummingbirds fed on the same plants. We conclude that the local diversity of hummingbird species is not primarily determined by the diversity of food plants, but rather by the abundance of flowers available at any given point in time.     

Influence of plant reproductive systems on the evolution of hummingbird pollination

Many hummingbird‐pollinated plant species evolved from bee‐pollinated ancestors independently in many different habitats in North and South America. The mechanisms leading to these transitions are not completely understood. We conducted pollination and germination experiments and analyzed additional reproductive traits in three sister species pairs of which one species is bee‐ and the other hummingbird‐pollinated. All hummingbird‐pollinated species showed higher seed set and germination rates in cross‐pollinated than in self‐pollinated flowers. In the self‐compatible, bee‐pollinated sister species this difference did not exist. As expected, seed set and germination rate were higher after cross‐pollination in the largely self‐incompatible genus Penstemon independently of the pollination syndrome. However, the bird‐pollinated species produce only half of the amount of ovules and pollen grains per flower compared to the bee‐pollinated sister species. This indicates that hummingbird pollination is much more efficient in self‐incompatible populations because hummingbirds waste less pollen and provide higher outcrossing rates. Therefore, hummingbird pollination is less resource costly. Overall, we suggest that hummingbirds may increase the reproductive success compared to bees, influencing the evolution of hummingbird pollination in ecosystems with diverse bee assemblages.     

Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon

We compared pollen removal and deposition by hummingbirds and bumblebees visiting bird-syndrome Penstemon barbatus and bee-syndrome P. strictus flowers. One model for evolutionary shifts from bee pollination to bird pollination has assumed that, mostly due to grooming, pollen on bee bodies quickly becomes unavailable for transfer to stigmas, whereas pollen on hummingbirds has greater carryover. Comparing bumblebees and hummingbirds seeking nectar in P. strictus, we confirmed that bees had a steeper pollen carryover curve than birds but, surprisingly, bees and birds removed similar amounts of pollen and had similar per-visit pollen transfer efficiencies. Comparing P. barbatus and P. strictus visited by hummingbirds, the bird-syndrome flowers had more pollen removed, more pollen deposited, and a higher transfer efficiency than the bee-syndrome flowers. In addition, P. barbatus flowers have evolved such that their anthers and stigmas would not easily come into contact with bumblebees if they were to forage on them. We discuss the role that differences in pollination efficiency between bees and hummingbirds may have played in the repeated evolution of hummingbird pollination in Penstemon.     

Automated tracking of wild hummingbird mass and energetics over multiple time scales using radio frequency identification (RFID) technology

We examined the feasibility of automating the collection of hummingbird mass data facilitated by low‐cost, low‐power radio frequency identification (RFID) technology. In a field study in southern Ontario, wild hummingbirds were captured, subcutaneously implanted with passive integrated transponder (PIT) tags, and released over a three‐year period. Tagged hummingbirds were detected at specially designed feeder stations outfitted with low‐cost, low‐power RFID readers coupled with a perch secured to a digital balance. When tagged birds visited the feeder, transponder detection initiated the recording of the perched hummingbird's mass at regular intervals continuing as long as the bird remained. This permitted a nearly continuous record of mass during each visit. Mass data collected from tagged hummingbirds showed consistent trends at multiple temporal scales: the individual feeder visit, single days, and even whole seasons. These results further confirm that RFID technology is safe for use in the smallest birds. The effective detection range is a function of RFID reader power, antenna, and tag size. Yet, we find that careful arrangement of feeders and detectors allows for reliable detection even when detection range is low. When coupled with additional technologies, such as a precision electronic balance, this approach can yield robust serial measures of physiological parameters such as mass, an indicator of energy balance over time.     

Pollination ecology of Penstemon roseus (Plantaginaceae), an endemic perennial shifted toward hummingbird specialization?

Summary Pink-flowered tubular Penstemon roseus (Plantaginaceae), which has shifted partially to hummingbird pollination, blooms on high-elevation slopes in the mountains in Tlaxcala, Mexico. We studied the interactions between pollinator visitation rates to flowers, pollen removal and deposition, flower size, and nectar removal frequency on seed production in P. roseus. We combine observational and experimental studies in two contrasting natural populations. Our manual pollinations revealed that P. roseus is fully self-compatible. Autonomous self- and manual self-pollinated flowers matured as many seeds as when outcrossed, but outcrossing seems to become better than selfing as the flowering season progressed. Early in the season flowers that were bagged and hand-selfed, hand-outcrossed, or autonomously selfed, or unbagged and naturally pollinated had equal seed set in all four treatments. But later in the season, outcross pollen gave approximately twice as much seed set as the two self-treatments. Low levels of pollen receipt and pollen removal were consistent with the long time elapsed for a given plant to be visited by hummingbirds, which suggests pollen shortage in both sites. Despite differences in pollinator visitation rates to flowers, probability of flower visitation, removal and deposition of pollen, and nectar production rates between populations, we found that total nectar production had no effect on seed production at either site. The daily nectar secretion rate of 0.3–0.65 mg sugar per flower per 1–3 days was low relative to other hummingbird-adapted Penstemon species (typical range: 1.5–5 mg sugar per flower), and it might be intermediate between hummingbird- and bee-adapted Penstemon flowers. Our results support the hypothesis about a shift toward hummingbird pollination, and provide an example of a ‘despecialized’ Penstemon species, which attracts high-energy pollinators (hummingbirds) and profits from outcrossing, but retains bee-syndrome floral traits and low sugar production rates.     

The assembly of plants used as nectar sources by hummingbirds in a Cerrado area of Central Brazil

Studies on hummingbird–plant interactions commonly use a pollination approach emphasizing mutualistic relationships. But floral resources are often used opportunistically by these birds. Plant–pollinator assemblies and pollination sustainability will depend both on the well-adapted plants and other potential floral resources. The Cerrado, Neotropical savannas of Central Brazil, has ca. 7.5 % of its flora supposedly adapted to hummingbird pollination. But detailed information about flowers effectively used by hummingbirds at community level is still lacking. Hence, we recorded all plant species visited by hummingbirds, to determine how these nectariferous flowers were distributed in time and space in different plant formations of a Cerrado area, and also the hummingbird species that visit them. The study was conducted between March 2007 and December 2008 in the Panga Ecological Station. Data regarding flowering phenology, floral morphology and visitation were collected monthly. Forty-six nectariferous species from 39 genera and 17 families were recorded, most with annual flowering dynamics and tubular flowers. But only 21 species had a combination of traits fitting classic ornithophilous syndrome. For the remaining species hummingbird visitation was ascertained from observations at the study site or other sites in the region. Eight hummingbird species occurred in the area and were recorded visiting directly 36 plant species. The study area presented a relatively low number of ornithophilous plants, but a great habitat diversity and many non-ornithophilous plants that hummingbirds used as nectar sources. Therefore, in the studied Cerrado, the diversity of environments and nectariferous plants favour the maintenance of resident and migrant hummingbirds.     

Pollen flow in the distylous<Emphasis Type="Italic"> Palicourea fendleri</Emphasis> (Rubiaceae): an experimental test of the Disassortative Pollen Flow Hypothesis

The Disassortative Pollen Flow Hypothesis proposed by Darwin postulates that the relative position of anthers and stigmas in distylous flowers enhances pollen flow between flowers of different morphs (legitimate pollination), in comparison to flow between flowers of the same morph (illegitimate pollination). In order to test this hypothesis, we measured pollen transport, mediated by a trained Copper-rumped Hummingbird (Amazilia tobaci), between flowers of the distylous Palicourea fendleri under laboratory conditions. In individual tests, we offered to the hummingbird a pollen donor flower and two emasculated recipient flowers in a controlled sequence. After each foraging bout, we counted the number of pollen grains transported from the donor flower to the stigmas of both recipient flowers. In agreement with Darwin's hypothesis, we found that hummingbirds transport pollen of "pin" flowers in significantly higher numbers to legitimate "thrum" stigmas, even if previously visiting a "pin" flower. However, "thrum" pollen was deposited in greater numbers on illegitimate "thrum" stigmas. We interpret this asymmetry largely as the consequence of floral morphology; pollen flow was greater between anthers and stigmas that exhibit greater spatial matching. In P. fendleri, the position of floral organs along the corolla tube does not always precisely correspond. In our experimental system, the probability that the pollinator extracts a pollen grain from the anther and the probability of self-pollination were both dependent on the type of floral morph. We discuss the relevance of the latter findings in relation to other studies of pollen flow in heterostylous species.     

Functional structure and specialization in three tropical plant–hummingbird interaction networks across an elevational gradient in Costa Rica

Understanding causes of variation in multispecies assemblages along spatial environmental gradients is a long‐standing research topic in ecology and biogeography. Ecological networks comprising interacting species of plants and pollinators are particularly suitable for testing effects of environmental gradients on the functional structure and specialization in multispecies assemblages. In this study, we investigated patterns in functional assemblage structure and specialization of hummingbirds at the individual and species level along a tropical elevational gradient. We mist‐netted hummingbirds at three elevations in Costa Rica in seven temporally distinct sampling periods and used the pollen carried by hummingbird individuals to construct plant–hummingbird networks at each elevation. We measured four functional traits of hummingbird species and quantified different metrics of functional community structure. We tested the effect of elevation on functional metrics of hummingbird assemblages and specialization within the networks, employing the variability across sampling periods and hummingbird species to compare the respective metrics among elevations. Hummingbird species and individuals were more specialized at low and mid elevations than at the highest elevation. This pattern corresponded to a more even and over‐dispersed assemblage structure at the lower elevations throughout the year and suggests a high level of floral resource partitioning in functionally diversified communities. In contrast, an uneven and clustered functional structure of the highland assemblage across all sampling periods suggests that this assemblage was structured by environmental filtering and by niche expansion of hummingbird individuals and species at this elevation. We conclude that high degrees of specialization on specific floral resources might be crucial for the coexistence of hummingbird species in diversified lowland communities. Spatial variation in animal resource use may be an important crucial driver of spatial patterns in the functional structure of diversified species assemblages also in other types of ecological networks.     

The role of the endemic and critically endangered Colorful Puffleg Eriocnemis mirabilis in plant‐hummingbird networks of the Colombian Andes

Ecological network approaches may contribute to conservation practices by quantifying within‐community importance of species. In mutualistic plant‐pollinator systems, such networks reflect potential pollination of the plants and a considerable portion of the energy consumption by the pollinators, two key components for each party. Here, we used two different sampling approaches to describe mutualistic plant‐hummingbird networks from a cloud forest in the Colombian Western Andes, home to the Colorful Puffleg Eriocnemis mirabilis, an endemic and critically endangered hummingbird. We contrast networks between two localities (a protected area inside a National park vs. its buffer zone) and across sampling methods (floral visitation vs. pollen loads) to assess how the network structure and the importance of each hummingbird species within the networks may change. Visitation networks were characterized as having higher sampling completeness, yet pollen load network recorded more pollen types than plant species recorded by visitation. Irrespective of the sampling methods, the Colorful Puffleg was one of the most important hummingbird species in the network within the protected area inside the National park, but not in the buffer zone. Moreover, most species‐level network indices were related to hummingbirds’ abundance. This suggests that conservation initiatives aimed at the endangered Colorful Puffleg may both help on the survival of this endangered hummingbird, as well as on maintaining its key role in the mutualistic interaction network inside the National Park. Our study illustrates how conservation practitioners could assess the local importance of endangered species using interaction network approaches.     

Quantity versus quality: identifying the most effective pollinators of the hummingbird-pollinated Vriesea rodigasiana (Bromeliaceae)

Although hummingbirds are considered the major bromeliad pollinators, different species may contribute differently to pollination. This study analyses the importance of different hummingbirds to pollination of Vriesea rodigasiana (Bromeliaceae), based on visitation frequency (a quantity component) and germinated pollen load per visit (a quality component) in the Atlantic rainforest of southeastern Brazil. This bromeliad flowers for 3–4 months with a peak in March. Its yellow, tubular flowers last about 13 h and demonstrate approach herkogamy. During flowering peak, Thalurania glaucopis visited more flowers than Ramphodon naevius, whereas by the end of the flowering season the latter visited more. Differences in hummingbird bill length resulted in different pollen placement and stigma contact. The short-billed T. glaucopis received pollen on the top of its head, depositing it on the center of the stigma, while the long-billed R. naevius received it on the proximal part of its bill, depositing it on the lower lobe of the stigma. Flowers visited by T. glaucopis had six times more pollen tubes than those visited by R. naevius. Our results suggest that this functional group of hummingbirds may be split into even smaller groups, namely short-billed and long-billed hummingbirds, based on different sites of pollen placement. Although both species were pollen vectors of V. rodigasiana, the short-billed T. glaucopis was its most effective pollinator in the area supporting Stebbin’s principle, linking floral features and good pollinators.     

Forest fragmentation and loss reduce richness,availability, and specialization in tropical hummingbird communities

Hummingbirds are important pollinators of many native Neotropical plants but their abundance and diversity in landscapes dominated by intensive human uses such as agriculture have rarely been examined, despite such land‐uses prevailing in the tropics. We examined how tropical deforestation affects hummingbird community structure in premontane forest patches embedded in a tropical countryside of Coto Brus Canton, Costa Rica. We captured hummingbirds in fourteen landscapes representing a gradient in patch size and forest amount, and tested for the effects of these variables on (1) hummingbird captures at flowers (pollinator availability); (2) species richness; and (3) filtering of functional traits. After accounting for sampling effects, both hummingbird availability and species richness declined by 40% and 50%, respectively, across the gradient in deforestation that we observed (9–66% forest within 1000 m). Focal patch size was the strongest predictor, even after statistically accounting for the amount of forest and matrix composition of landscapes. These reductions in availability and richness were well predicted by functional traits; morphologically specialized species with the capacity to transport long‐distance outcrossed pollen and low functional redundancy within the pollinator network showed the greatest sensitivity to landscape change. We hypothesize that declines in hummingbird availability, diversity, and functional traits are important mechanisms driving the observed pollen limitation of ornithophilous flowers in fragmented tropical landscapes. Efforts to conserve large forest patches and enhance matrix permeability are critical for maintaining forest hummingbird communities and pollination services under current and predicted deforestation regimes.     

Erosion of a pollination mutualism along an environmental gradient in a south Andean treelet,Embothrium coccineum (Proteaceae)

The limit of a species’ distribution can be determined biotically if an environmental gradient causes the loss of critical mutualists such as pollinators. We assessed this hypothesis for Embothrium coccineum, a self‐incompatible red‐flowered treelet growing along a strong west‐east precipitation gradient from rainforest to forest‐steppe ecotone in the rain shadow of the southern Andes in northwestern Patagonia. For 16 populations along this gradient, we quantified composition of the pollinator assemblage, pollination efficiency and limitation, and reproductive output. The treelet has a generalized pollination system, but the hummingbird Sephanoides sephaniodes was the most effective pollinator. The relative importance of this hummingbird as a flower visitor within populations influenced pollen transfer and fruit set more strongly than local precipitation. As hummingbirds and other pollinators, including passerine birds and nemestrinid flies, were replaced by bees towards the dry eastern range limit, pollen limitation increased and reproduction eventually failed. These results support the hypothesis that pollinators can act as important biotic filters influencing plant distribution, and warn against predictions of geographical range shifts based solely on climatic variables.     

Pollination ecology of Ruellia angustiflora (Ness) Lindau ex Rambo (Acanthaceae) in the Serra da Bodoquena,Mato Grosso do Sul,Brazil

In Brazil, studies focusing on reproductive biology and aspects of pollination in the genus Ruellia have demonstrated common characteristics such as pollination by hummingbird, the predominance of self-fertility and spontaneous self-pollination. The objectives of this study were to describe the floral biology, nectar production, the reproductive system, the effect of pollination intensity and flowering phenology of Ruellia angustiflora, as well as keeping a record of the hummingbirds that visit the flowers of this species. Data collection was performed in a stretch of the Salobrinha stream in the Serra da Bodoquena, Mato Grosso do Sul, from August 2005 to July 2006. R. angustiflora flowered throughout most of the study period; it has diurnal anthesis and has increased nectar production in the morning hours with decreasing production rates during the day. The results of the reproduction experiments indicate self-fertility and pollen limitation in R. angustiflora. Among experiments with different pollination intensity there was no significant difference in fruit formation. Four hummingbird species were observed visiting the flowers of R. angustiflora, and Phaethornis pretrei was the most frequent followed by females of Thalurania furcata. According to its behavior and frequency of visits, P. pretrei can be considered the main pollinator of R. angustiflora in the study area. The experiments on flowers treated with different pollen loads indicate that most successful fruit formation in this species is obtained in flowers that received greater pollen loads on their stigmas. Besides, data suggest that major success in fruit set could be reached with more than three visits of P. pretrei.     

Ornithophily in the Rhamnaceae: The pollination of the Chilean endemic Colletia ulicina

Colletia ulicina, an endemic species from the central region of Chile, displays red, tubular, scented, nectariferous flowers at the tip of its branches. Observations at two sites during two consecutive years indicate that the hummingbird Sephanoides sephaniodes (Trochilidae) visits the flowers on a regular basis. Captured hummingbirds had C. ulicina pollen loads on body parts matching the location of anthers and stigmas. The C. ulicina–S. sephaniodes interaction is well established (hummingbird visits were frequent, systematical, and occurred at different sites) although it lacks specificity (S. sephaniodes is a generalist hummingbird and C. ulicina has another, seasonally important pollinator, the even more generalist bumblebee Bombus dahlbomii). To the best of our knowledge this is the first documented report on bird pollination in the Rhamnaceae.     

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.     

Effects of hummingbird morphology on specialization in pollination networks vary with resource availability

Specialization of species in interaction networks influences network stability and ecosystem functioning. Spatial and temporal variation in resource availability may provide insight into how ecological factors, such as resource abundance, and evolutionary factors, such as phylogenetically conserved morphological traits, influence specialization within mutualistic networks. We used independent measures of hummingbird abundance and resources (nectar), information on hummingbird traits and plant–hummingbird interactions to examine how resource availability and species' morphology influence the specialization of hummingbirds in three habitat types (forest, shrubs, cattle ranch) sampled over 10 sessions across two years in the southern Andes of Ecuador. Specialization of hummingbird species in the networks was measured by three indices: d' (related to niche partitioning), generality (related to niche width) and PSI (related to pollination services). Specialization indices d', generality and PSI of hummingbird species were influenced by resource availability. All indices indicated that specialization of hummingbirds increased when the availability of resources decreased. Variation in d' was also explained by an interaction between resource availability and bill length; hummingbirds with a long bill switched from being more specialized than other species when resource availability was low to being similarly specialized when availability was high. Overall, our results highlight the importance of ecological and evolutionary factors determining the specialization of species in interaction networks. We demonstrate in particular that ecological gradients in resource availability cause substantial changes in consumers' foraging behavior contingent on their morphology. Changes in pollinator specialization along resource gradients can have impacts on ecosystem functions, such as pollination by animals.     

Effects of nectar theft by flower mites on hummingbird behavior and the reproductive success of their host plant, Moussonia deppeana (Gesneriaceae)

Hummingbird flower mites are transported in the nares of hummingbirds and may compete with them by "robbing" nectar secreted by the host plants. We have shown that Tropicoseius sp. flower mites consume almost half the nectar secreted by the long-lived, protandrous flowers of Moussonia deppeana (Gesneriaceae) pollinated by Lampornis amethystinus (Trochilidae). In this paper, we ask whether mimicking nectar consumption of flower mites alters some aspects of hummingbird foraging patterns, and, if so, how this affects host plant seed production. We observed hummingbirds foraging on (a) plants in which nectar was removed from the flowers and then filled with a sugar solution to half the volume of nectar simulating nectar consumption by flower mites, and (b) plants where nectar was removed and then filled with the sugar solution up to normal nectar volumes. Flower mites were excluded from both groups of plants to control for mite activity. Hummingbirds made fewer but longer visits to plants and revisited more the flowers with nectar removal than those without the treatment. We then conducted a pollination experiment on pistillate flowers using a stuffed L. amethystinus hummingbird to evaluate the effect of pollination intensity (number of bill insertions into one flower) on seed production. Flowers with more insertions produced significantly more seeds than those flowers that received fewer insertions. We conclude that the simulation of nectar consumption by hummingbird flower mites can influence the behavior of the pollinator, and this may positively affect seed production.     

Anther evolution: pollen presentation strategies when pollinators differ

Male-male competition in plants is thought to exert selection on flower morphology and on the temporal presentation of pollen. Theory suggests that a plant's pollen dosing strategy should evolve to match the abundance and pollen transfer efficiency of its pollinators. Simultaneous pollen presentation should be favored when pollinators are infrequent or efficient at delivering the pollen they remove, whereas gradual dosing should optimize delivery by frequent and wasteful pollinators. Among Penstemon and Keckiella species, anthers vary in ways that affect pollen release, and the morphology of dried anthers reliably indicates how they dispense pollen. In these genera, hummingbird pollination has evolved repeatedly from hymenopteran pollination. Pollen production does not change with evolutionary shifts between pollinators. We show that after we control for phylogeny, hymenopteran-adapted species present their pollen more gradually than hummingbird-adapted relatives. In a species pair that seemed to defy the pattern, the rhythm of anther maturation produced an equivalent dosing effect. These results accord with previous findings that hummingbirds can be more efficient than bees at delivering pollen.