Mobility of Impatiens capensis flowers: effect on pollen deposition and hummingbird foraging

Flexible pedicels are characteristic of birdpollinated plants, yet have received little attention in studies of hummingbird-flower interactions. A major implication of flexible pedicels is that flowers may move during pollination. We examined whether such motion affected interactions between ruby-throated hummingbirds (Archilochus colubris) and jewelweed (Impatiens capensis) by increasing pollen deposition and by altering the effectiveness of nectar removal. For I. capensis, flower mobility enhanced pollen deposition: birds had significantly longer contact with anthers and more pollen deposited on their bills and crowns when foraging at mobile flowers than at flowers that had been experimentally immobilized. In contrast, flower mobility imposed a cost on hummingbirds by significantly increasing their handling times and reducing their extraction rates relative to their interactions with immobile flowers. Field observations indicated that the motion observed during hummingbird visits did not occur when bees (Bombus spp., Apis mellifera) visited I. capensis flowers, which suggests that the mobility of I. capensis flowers is an adaptation for hummingbird pollination.     

Nonadditive effects of flower damage and hummingbird pollination on the fecundity of Mimulus luteus

Flower herbivory and pollination have been described as interactive processes that influence each other in their effects on plant reproductive success. Few studies, however, have so far examined their joint effects in natural populations. In this paper we evaluate the influence of flower damage and pollination by the hummingbird Oreotrochilus leucopleurus on the fecundity of the Andean monkey flower Mimulus luteus. We performed a 2×2 factorial experiment, with artificial clipping of lower petals and selective exclusion of the hummingbird as main factors. In spite of the relatively low proportion (27.5%) of the variance in seed production accounted for by the full factorial model, artificial damage and hummingbird exclusion, as well as their interaction, were highly significant, indicating nonadditive effects of factors on plant fecundity. In the presence of hummingbirds, undamaged flowers had a seed production that was 1.7-fold higher than for damaged flowers, suggesting that the effect of flower damage on female reproductive success occurs probably as a consequence of hummingbird discrimination against damaged corollas. This result indicates that the impact of flower herbivory on plant fecundity was contingent on the presence or absence of hummingbirds, suggesting that pollinators may indirectly select for undamaged and probably resistant flower phenotypes. A second interaction effect revealed that undamaged flowers produced 78.5% more seeds in the absence of rather than in the presence of O. leucopleurus, raising the question of the ecological mechanism involved. We suggest that the strong territorial behavior exhibited by the bee Centris nigerrima may confine the foraging activities of the remaining bee species to safe sites within exclosures. Overall, our results provide evidence that hummingbird pollination and flower herbivory have interdependent effects on M. luteus fecundity, which indicates that it will be difficult to predict their ecological and evolutionary consequences unless interactions are analyzed in an integrated form.     

COMPETITION BETWEEN HERMIT HUMMINGBIRDS PHAETHORNINAE AND INSECTS FOR NECTAR IN A COSTA RICAN RAIN FOREST

Hummingbirds in the tropical rainforests of southwestern Costa Rica face intense competition from stingless bees Trigona that steal nectar from hummingbird flowers. Here we document both interference and exploitative competition between bees and hummingbirds at scarlet, hummingbird pollinated flowers of Passiflora vitifolia. Aggressive stingless bees prevented Long-tailed Hermit Hummingbirds Phaethornis superciliosus from feeding at nearly one-third of the passion flowers approached. In exclusion experiments, bees and hummingbirds each removed most of the nectar from treated flowers. Experimental exclusion of bees also increased hummingbird use of both natural and artificial flowers.     

The Role of Flower Width in Hummingbird Bill Length‐Flower Length Relationships1

Observations of hummingbirds feeding at flowers longer or shorter than their bills seem to contradict the view that bill lengths of hummingbirds evolved in concert with the lengths of their flowers. Recent experiments, however, indicate that a hummingbird's ability to feed at artificial flowers of different lengths depends on the widths of the flowers. We examined if the broad range of flower lengths visited by many hummingbird species can be explained by the widths of the flowers. We predicted that both short‐ and long‐billed hummingbirds would include long, wide flower species in their diets, but that short‐billed hummingbirds would not include long, narrow flower species because nectar in these species might be beyond the reach of their bills. If so, the slope of the regression for flower width versus flower length should be smaller for flower species visited by longer‐billed hummingbirds relative to those visited by shorter‐billed hummingbirds. Analyses of data sets for some North American and Monteverde hummingbirds and their food plants were consistent with this prediction, and bill lengths were significantly correlated with the slopes of the regressions of flower width versus length for seven hummingbird species. Comparisons of observed flower use by some Monteverde hummingbird species to flower assemblages generated at random suggest that these significant regressions were not simply a result of allometric relationships between flower lengths and widths, but in some cases reflected active choice by the birds. The two hummingbird–flower data sets also differed significandy in the scaling of corolla width relative to corolla length. In particular, the Monteverde data set contained a large number of long, narrow flower species, which we suggest is a consequence of a different floral evolutionary history and association with long‐billed hummingbird species. The evolutionary effects of hummingbirds and their flowers upon one another are more complex than has generally been realized, and a consideration of corolla length jointly with other floral characters may improve our understanding of hummingbird‐flower relationships.     

Bees provide pollination service to Campsis radicans (Bignoniaceae), a primarily ornithophilous trumpet flowering vine

1. Pollination syndromes refer to stereotyped floral characteristics (flower colour, shape, etc.) that are associated with a functional group of pollinators (bee, bird, etc.).
2. The trumpet creeper Campsis radicans, endemic to the southeast and mid‐west United States, has been assigned to the hummingbird‐pollination syndrome, due mainly to its red, trumpet‐shaped flowers.
3. Previous studies demonstrated that the ruby‐throated hummingbird Archilochus colubris is C. radicans' primary pollinator, but anecdotal data suggest various bee species may provide pollination service when hummingbirds are absent.
4. This study characterised C. radicans nectar volume and concentration by time of day. Nectar volume was suitable for hummingbirds, but concentration was higher than typical hummingbird‐pollinated plants (～20% w/w); at ～30% w/w, it approached the concentration expected in bee‐pollinated plants (～50% w/w). We also found substantial amounts of nectar at night.
5. Two C. radicans populations received virtually no hummingbird visits, but the number of bees were markedly higher than in the populations previously described. Interestingly, there were no night‐time visitors despite the large quantity of nocturnal nectar.
6. Based on previously published pollen delivery per visit by various species, this study estimated that cumulative deposition by bees routinely reached pollen deposition thresholds for setting fruit in C. radicans. They are, unequivocally, the predominant pollinators in these populations, thus providing pollination service in the absence of hummingbirds.
7. These results highlight C. radicans as a food source for native bees and add to the understanding of how floral phenotypes can facilitate pollination by disparate functional groups.

     

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.     

Oriole pollination ofErythrina breviflora (Leguminosae): Evidence for a polytypic view of ornithophily

Erythrina breviflora is visited by large numbers of passerine birds of which orioles (Icterus: Icteridae) are the primary pollinators. The flowers produce large quantities of nectar but they are rarely visited by hummingbirds. Inflorescence and floral morphology, and low levels of sucrose in the nectar probably explain the rarity of foraging hummingbirds. A comparison of Old WorldErythrina and their pollinators with New World species pollinated by orioles and hummingbirds suggests that parallel evolution has occurred. When the comparison is expanded to include other species pollinated by orioles, it is clear that various New WorldIcteridae, Thraupidae, etc. are ecological equivalents of Old WorldOriolidae, Pycnonotidae, Sturnidae, etc. and that flowers pollinated by these birds have similar characteristics.     

Pollination biology ofSymphonia globulifera (Clusiaceae)

The pollination biology ofSymphonia globulifera was studied in Central Amazonia, Brazil. As suggested by the bird syndrome of the flowers, these are mainly pollinated by hummingbirds. Occasional visits by other birds, butterflies and more rarely bees, as well as tamarin monkeys were also observed.Trigona bees partly destroy the flower tube to rob nectar. The possibility thatS. globulifera may not be primarily adapted to hummingbird pollination is discussed. The pollen is intermixed in an oily fluid secreted by the anthers (antheroil). Each of the five stigmas consists of a pore-like opening at the apex and a small chamber behind it. The antheroil mixed with pollen is absorbed by capillarity into the chamber when deposited on the pore. the pollen germinates inside the stigma. The presence of antheroil and pore-like stigmas in the flowers of the closely relatedPlatonia insignis indicate a similar mode of pollination. The results of this study are compared with observations in some otherClusiaceae (Caraipa, Clusia, Garcinia, Mahurea), where floral oils or floral resin occur. The role of these substances in the pollination process and their relation to the evolution of flower biology inClusiaceae are briefly discussed.     

New specimens of the early Oligocene Old World hummingbird Eurotrochilus inexpectatus

New specimens of the early Oligocene (32 million years ago) stem group hummingbird Eurotrochilus inexpectatus Mayr, 2004, are described from the type locality Frauenweiler in Southern Germany. One of these is the second slab of the holotype, whose existence has been hitherto unknown. The new fossils add significantly to our knowledge of the morphology of E. inexpectatus and allow more detailed comparisons with other stem and crown group Trochilidae. A new apomorphy of the clade (Eurotrochilus + crown group Trochilidae) is described. With species successively more closely related to the crown group, the temporal sequence of stem group hummingbirds in Europe indicates an Old World origin of Pan-Trochilidae. E. inexpectatus is the earliest long-beaked stem group hummingbird with hovering capabilities, and absence of modern-type hummingbirds before the early Oligocene may provide a maximum age for the origin of hummingbird-pollinated plants and the colonization of the New World by modern-type stem group hummingbirds.     

Flowering phenology,pollen flow and fruit production in the andean shrub Befaria resinosa

Summary In the eastern Andes of Colombia, the shrub Befaria resinosa (Ericaceae) has peaks of flowering that are separated by extended periods of low flower production. The effect that these fluctuations in flower production have on pollen flow was investigated by using fluorescent dye as a pollen analog. Dye applied to open flowers was dispersed over long distances more often during low flower production than during high flower production. Whether enhanced pollen dispersal during flowering lows is of benefit to individual plants is not clear. The proportion of flowers that set fruit is positively correlated with flower abundance, negating the possibility that increased pollen dispersal results in a higher rate of fruit production due to outbreeding effects. It is also difficult to attribute the pattern of fruit production to changes in pollinator visitation rates, which are negatively correlated with flower abundance in the case of hummingbirds and not correlated at all with flower abundance in the case of insects. An opportunistic, large-bodied hummingbird (Colibri coruscans) visits B. resinosa during high flowering and may be a particularly effective pollinator, accounting for some of the increase in the proportion of flowers setting fruit. Rainfall is positively correlated with flower production and may be an important factor in shaping flowering phenology, but it is not significantly correlated with the proportion of flowers setting fruits. The possibility that low-level flowering may counteract inbreeding that results from peak flowering is discussed.     

An Old World hummingbird from the Oligocene: a new fossil from Polish Carpathians

A near-complete, partially articulated skeleton of a hummingbird was recently found in the menilite shales of the Polish Flysh Carpathians. The specimen is dated to the Early Oligocene (Rupelian, approx. 31 Myr). It shares derived characters with extant hummingbirds and plesiomorphic characters with swifts. Its long, thin beak and short and stout humerus and ulna are typical for hummingbirds, but the coracoid resembles that observed in swifts. The osteology of the specimen is generally similar to that of the hummingbird described from the Early Tertiary of Germany but because it clearly differs in some characters from the German hummingbird Eurotrochilus inexpectatus, it is described as a new species of the same genus.     

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.     

Flowering patterns of long-lived Heliconia inflorescences: implications for visiting and resident nectarivores

Summary Flowering patterns of four Heliconia (Heliconiaceae) species in Trinidad, West Indies were examined for their predictability and availability to the nectarivores that rely on Heliconia floral nectar. Principal flower visitors are trapling hermit hummingbirds; inflorescences are inhabited by nectarivorous hummingbird flower mites that move between inflorescences by riding in the hummingbirds' nares. Heliconia inflorescences flower for 40–200 days, providing long-term sources of copious nectar (30–60 l per flower), but each Heliconia flower lasts only a single day. As an inflorescence ages the interval increases between open flowers within a bract; wet-season inflorescences produce open flowers more slowly than dry-season conspecifics.Estimated daily energy expenditures for hermit hummingbirds demonstrate that slow production of short-lived open flowers plus low inflorescence density preclude territorial defense of Heliconia by the hermits. Heliconia flowering patterns are viewed as a means of (i) regulating reproductive investment by the plants through staggered flower production over long periods of time, and (ii) maintaining outcrossing by necessitating a traplining visitation pattern by its hummingbird pollinators. I suggest that Heliconia exhibit a two-tiered pollination system by using hermit hummingbirds primarily for outcrossing and using hummingbird flower mites primarily for self-pollination.     

Nectar extraction by hummingbirds: response to different floral characters

Summary Handling times of hummingbirds (Amazilia rutila and Cynanthus latirostris) visiting artificial flowers were a positive function of corolla length, nectar volume and nectar concentration. Corolla angle had no consistent effects on handling times. A multiple regression model explained 83% of the variation in handling times for these two species. The model also closely fit independent data from another hummingbird, Archilochus colubris, suggesting that it is general enough to apply to other medium-sized, short-billed hummingbird species. When examined across the range of variation normally encountered by hummingbirds in nature, corolla length and nectar volume had the largest effect on nectar extraction rates. At corolla lengths longer than a hummingbird's bill handling time increases markedly. Hummingbirds maximize their net rate of energy intake by selecting flowers with the shortest corolla, the highest nectar concentrations and the highest nectar volume. Since there is a positive relation between bill length and nectar extraction rate, it is surprising that most hummingbirds have relatively short bills.     

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.     

Sugar and protein digestion in flowerpiercers and hummingbirds: a comparative test of adaptive convergence

Flowerpiercers are the most specialized nectar-feeding passerines in the Neotropics. They are nectar robbers that feed on the sucrose-rich diet of hummingbirds. To test the hypothesis that flowerpiercers have converged with hummingbirds in digestive traits, we compared the activity of intestinal enzymes and the gut nominal area of cinnamon-bellied flowerpiercers (Diglossa baritula) with those of eleven hummingbird species. We measured sucrase, maltase, and aminopeptidase-N activities. To provide a comparative context, we also compared flowerpiercers and hummingbirds with 29 species of passerines. We analyzed enzyme activity using both standard allometric analyses and phylogenetically independent contrasts. Both approaches revealed the same patterns. With the exception of sucrase activity, hummingbirds digestive traits were indistinguishable from those of passerines. Sucrase activity was ten times higher in hummingbirds than in passerines. Hummingbirds and passerines also differed in the relationship between intestinal maltase and sucrase activities. Maltase activity was two times higher per unit of sucrase activity in passerines than in hummingbirds. The sucrase activity of D. baritula was much lower than that of hummingbirds, and not unlike that expected for a passerine of its body mass. With the exception of aminopeptidase-N activity, the digestive traits of D. baritula were not different from those of other passerines.Abbreviations K_m Michaelis-Menten constant - PDAP phenotypic diversity analysis program - PIC phylogenetic independent contrast - V_max maximal reaction velocityCommunicated by G. Heldmaier     

Effect of sexual dimorphism in bill length on foraging behavior: an experimental analysis of hummingbirds

We examined whether sexual differences in trophic morphology are associated with sexual differences in foraging behavior through two laboratory experiments on rufous hummingbirds (Selasphorus rufus) designed to compare probing abilities (maximum extraction depths) and handling times of sexes at flowers. Bills of female S. rufus are about 10.5% longer than bills of males, and this difference was associated with sexual differences in foraging abilities. Maximum extraction depths of female S. rufus were significantly greater than those of males, and no overlap between the sexes was observed. Moreover, handling times of females were shorter than handling times of males at flowers having longer corollas (15 mm). Thus, because of their longer bills, female S. rufus have the potential to feed from longer flowers than males, and can do so more quickly. We suggest that no single mechanism is responsible for the evolution of sexual dimorphism in bill lengths of hummingbirds, but rather that the dimorphism probably reflects the combined effects of reproductive role division and intersexual food competition, and possibly, sexual selection.     

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.     

The pollination biology of two species of Helicteres (Malvaceae) with different mechanisms of pollen deposition

Species of Helicteres are pollinated mainly by hummingbirds and bats. Most species pollinated by hummingbirds have a mechanism of depositing pollen on the top of the pollinator's head such as is shown in this work for Helicteres sacarolha. H. brevispira has an unusual mechanism of depositing pollen grains under the tail or on the abdomen of the hummingbirds. The top of the birds’ head may be considered an efficient place to transport pollen grains, because it is plain, easily accessible for deposition and donation of pollen and not easily accessible for grooming, while the tail is movable and inclined. Thus, H. brevispira pollinators may carry or transfer fewer amounts of pollen grains than H. sacarolha pollinators from one flower to another. If a large amount of pollen grains is lost, a higher quantity of flower or pollen has to be produced to guarantee reproductive success. Plants of H. brevispira set higher number of flowers and pollen grains per flower than H. sacarolha and have also higher rates of fruit and flower abortion. Thus, pollination efficiency of H. brevispira may be reached by high pollen and flower production. Flower change mechanism presented in this species may be also involved with the optimization of pollinator feeding and pollination efficiency.     

Physical and ant-mediated refuges from parasitism: Implications for non-target effects in biological control

A promising natural enemy for release against the Asian soybean aphid, Aphis glycines Matsumura, in North America is the aphidiine braconid wasp Binodoxys communis (Gahan). The aphid Aphis monardae Oestlund, a native of North America’s tall-grass prairies, is a non-target species that may be at risk from releases of B. communis. This paper describes ecological facets of A. monardae populations in their native habitat that could protect them from attack by this exotic biological control agent. In prairie habitats, A. monardae populations aggregate in flower heads of their host plant, Monarda fistulosa L. On this host plant, aphids are also commonly tended by four ant species, and ant-tended colonies are larger than un-attended colonies. Laboratory studies showed that parasitism rates of A. monardae by B. communis are significantly higher on vegetative M. fistulosa than on M. fistulosa flower heads. In addition, attendance of A. monardae by the ant Lasius neoniger Emery significantly decreased parasitism by B. communis. Ants attacked and killed host-seeking adult parasitoids, and preyed upon B. communis mummies. No evidence was found that B. communis reared from A. monardae are less susceptible to attack by ants than parasitoids reared from A. glycines. M. fistulosa flower heads and attendance by L. neoniger may act as refuges for A. monardae against B. communis. Our work describes spatial refuges as ecological filters that separate non-target organisms from exotic natural enemies. Implications for classical biological control of A. glycines are discussed.