Geographical variation in floral traits of the tree tobacco in relation to its hummingbird pollinator fauna

Nicotiana glauca , a hummingbird pollinated plant, exhibits geographical variation in several floral traits. We examined whether geographical differentiation occurred for different flower characters and if this differentiation could be explained, at least in part, by the existence or abundance of different hummingbird species in the respective pollinator assemblages. The comparison between five populations showed significant variation in six floral traits and two female fitness measures. The traits that better discriminated between populations were corolla length and corolla width. There were metric correlations between corolla length and style length in all populations studied and, in four of the five populations, both corolla length and width were also correlated. Among plants in each population, seed weight was correlated positively and significantly with style exertion, suggesting that fruit quality is dependent on the degree of cross pollination. Assemblages of hummingbirds differed between populations in species composition, visitation frequencies, and bill length. Linear regression involving bill length of the more frequent hummingbird pollinators and corolla length yielded positive and significant relationships. Thus, there appears to be an adjustment between pollinators and flowers traits that have high incidence in the among population variation.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 657–667.     

Genetic structuring and secondary contact in the white‐chested Amazilia hummingbird species complex

Pleistocene climate cycles have been recognized to be a major driver of postglacial northward range expansion of North American bird populations. During glacial maxima, allopatric lineages that were reproductively isolated might have come into secondary contact with one another during expansion periods and the genetic signatures of past hybridization as a result of secondary contact events should produce detectable hybrid zones. The white‐chested hummingbirds Amazilia violiceps and A. viridifrons, constitute a species complex showing phenotypic similarity across its range. One exception is the subspecies found in the Central Depression of Chiapas (A. viridifrons villadai), which shares some plumage traits with the endemic but allopatric green‐fronted populations in Oaxaca. Phylogenetic relationships, taxonomy and species limits among violiceps, viridifrons and villadai have been controversial for decades. We assessed genetic structure of populations and introgression in this species complex by analysing 95 individuals at ten nuclear microsatellites and morphology. Bayesian analysis yielded four clusters. However, only two clusters generally match previously described mtDNA haplogroups, one parental taxon in the south (villadai) and a cluster with two admixed taxa (viridifrons and violiceps) that cannot be attributed to any pure parental population. High genetic admixture was recorded in the violiceps/viridifrons range, probably as a consequence of a postglacial northern expansion of violiceps. Signs of admixture and gene flow between violiceps/viridifrons and villadai were low. Historical and contemporary migration rates and Approximate Bayesian computations support a scenario of divergence with gene flow: a Pleistocene basal split separating A. violiceps and the other two clades are derived from a second split (villadai and viridifrons) or from a merger of violiceps and villadai into viridifrons due to gene flow.     

Mixed hummingbird: Long‐proboscid‐fly pollination in ‘ornithophilous’Embothrium coccineum (Proteaceae) along a rainfall gradient in Patagonia,Argentina

Abstract The pollination ecology of eight populations of the tree Embothrium coccineum was studied along a steep rainfall gradient in NW Patagonia, Argentina. The showy red flowers suggest an ornithophilous pollination syndrome and they have been reported to attract hummingbirds in Argentina and hummingbirds and passerines in Chile. At each population, flower visitors were recorded and floral rewards were analysed. We found a highly significant increase in nectar concentration towards the drier end of the gradient, but this change was not related to the turnover of species in the flower‐visitor assemblage of E. coccineum. In addition to the hummingbird Sephanoides sephaniodes (Green‐Backed Firecrown, Trochilidae) which is widespread throughout the temperate forest at this latitude, other species seem to be locally important as pollinators of E. coccineum in some sites in Argentina (e.g. two long‐tongued tanglewing flies (Nemestrinidae) of the genus Trichophthalma). The long‐dated occurrence of tanglewing flies in South America, relative to the more modern hummingbirds, suggests that ornithophily may be a derived character in E. coccineum, the ancestral condition being pollination by Nemestrinidae.     

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 tongues are elastic micropumps

Pumping is a vital natural process, imitated by humans for thousands of years. We demonstrate that a hitherto undocumented mechanism of fluid transport pumps nectar onto the hummingbird tongue. Using high-speed cameras, we filmed the tongue–fluid interaction in 18 hummingbird species, from seven of the nine main hummingbird clades. During the offloading of the nectar inside the bill, hummingbirds compress their tongues upon extrusion; the compressed tongue remains flattened until it contacts the nectar. After contact with the nectar surface, the tongue reshapes filling entirely with nectar; we did not observe the formation of menisci required for the operation of capillarity during this process. We show that the tongue works as an elastic micropump; fluid at the tip is driven into the tongue''s grooves by forces resulting from re-expansion of a collapsed section. This work falsifies the long-standing idea that capillarity is an important force filling hummingbird tongue grooves during nectar feeding. The expansive filling mechanism we report in this paper recruits elastic recovery properties of the groove walls to load nectar into the tongue an order of magnitude faster than capillarity could. Such fast filling allows hummingbirds to extract nectar at higher rates than predicted by capillarity-based foraging models, in agreement with their fast licking rates.     

BIRD EGGSHELL IN DOMINICAN AMBER

Abstract:  Here we report an eggshell in Dominican amber, representing the first vertebrate egg in any amber deposit. The eggshell is compared with present-day eggs of lizards, snails and birds. Based on the surface structure and type of shell breakage, it appears that the most likely candidate is a bird, and with that consideration, an avian group that produces eggs similar to the fossil in shape, size and colouration is the Trochilidae (hummingbirds). Several possible explanations of how the fossil could be preserved in amber are provided. If indeed a hummingbird was involved, this discovery would represent the first New World record of a fossil trochilid.     

Nectar bacteria,but not yeast,weaken a plant–pollinator mutualism

Mutualistic interactions are often subject to exploitation by species that are not directly involved in the mutualism. Understanding which organisms act as such ‘third-party’ species and how they do so is a major challenge in the current study of mutualistic interactions. Here, we show that even species that appear ecologically similar can have contrasting effects as third-party species. We experimentally compared the effects of nectar-inhabiting bacteria and yeasts on the strength of a mutualism between a hummingbird-pollinated shrub, Mimulus aurantiacus, and its pollinators. We found that the common bacterium Gluconobacter sp., but not the common yeast Metschnikowia reukaufii, reduced pollination success, seed set and nectar consumption by pollinators, thereby weakening the plant–pollinator mutualism. We also found that the bacteria reduced nectar pH and total sugar concentration more greatly than the yeasts did and that the bacteria decreased glucose concentration and increased fructose concentration whereas the yeasts affected neither. These distinct changes to nectar chemistry may underlie the microbes'' contrasting effects on the mutualism. Our results suggest that it is necessary to understand the determinants of microbial species composition in nectar and their differential modification of floral rewards to explain the mutual benefits that plants and pollinators gain from each other.     

Evolution of sexual dimorphism in bill size and shape of hermit hummingbirds (Phaethornithinae): a role for ecological causation

Unambiguous examples of ecological causation of sexual dimorphism are rare, and the best evidence involves sexual differences in trophic morphology. We show that moderate female-biased sexual dimorphism in bill curvature is the ancestral condition in hermit hummingbirds (Phaethornithinae), and that it is greatly amplified in species such as Glaucis hirsutus and Phaethornis guy, where bills of females are 60 per cent more curved than bills of males. In contrast, bill curvature dimorphism is lost or reduced in a lineage of short-billed hermit species and in specialist Eutoxeres sicklebill hermits. In the hermits, males tend to be larger than females in the majority of species, although size dimorphism is typically small. Consistent with earlier studies of hummingbird feeding performance, both raw regressions of traits and phylogenetic independent contrasts supported the prediction that dimorphism in bill curvature of hermits is associated with longer bills. Some evidence indicates that differences between sexes of hermit hummingbirds are associated with differences in the use of food plants. We suggest that some hermit hummingbirds provide model organisms for studies of ecological causation of sexual dimorphism because their sexual dimorphism in bill curvature provides a diagnostic clue for the food plants that need to be monitored for studies of sexual differences in resource use.     

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.     

Evolution and homology of bird pollination syndromes in Erythrina (Leguminosae)

Erythrina L. (Leguminosae: Phaseoleae) is a pantropical genus of over 100 species, all of which are either hummingbird or passerine pollinated. Phylogenetic hypotheses based on morphological and chloroplast DNA restriction site characters suggest that shifts from passerine to hummingbird pollination have occurred a minimum of four times in the genus. In hummingbird-pollinated species the inflorescences are held upright, the flowers are arranged radially along the axis, and the narrow standard petal is conduplicately folded to form a pseudotube. In most of the passerine-pollinated species, the inflorescences are held horizontally, the flowers are secund, and the standard petal is open so that the nectar and androecium are easily visible and accessible. Nectar amino acid concentrations and sucrose to hexose ratios are closely associated with pollination mode. Despite the general resemblance in flower and inflorescence morphology among species with the same pollination type, homology assessment reveals that petal morphology and size, and calyx and pollen morphology differ. Morphological characters, even if comprising modifications associated with adaptive pollination systems, therefore provide useful phylogenetic information.     

Structure of the vortex wake in hovering Anna's hummingbirds (Calypte anna)

Hummingbirds are specialized hoverers for which the vortex wake has been described as a series of single vortex rings shed primarily during the downstroke. Recent findings in bats and birds, as well as in a recent study on Anna''s hummingbirds, suggest that each wing may shed a discrete vortex ring, yielding a bilaterally paired wake. Here, we describe the presence of two discrete rings in the wake of hovering Anna''s hummingbirds, and also infer force production through a wingbeat with contributions to weight support. Using flow visualization, we found separate vortices at the tip and root of each wing, with 15% stronger circulation at the wingtip than at the root during the downstroke. The upstroke wake is more complex, with near-continuous shedding of vorticity, and circulation of approximately equal magnitude at tip and root. Force estimates suggest that the downstroke contributes 66% of required weight support, whereas the upstroke generates 35%. We also identified a secondary vortex structure yielding 8–26% of weight support. Lift production in Anna''s hummingbirds is more evenly distributed between the stroke phases than previously estimated for Rufous hummingbirds, in accordance with the generally symmetric down- and upstrokes that characterize hovering in these birds.     

Functional Significance of Interspecific Variation in Burmeistera Flower Morphology: Evidence from Nectar Bat Captures in Ecuador

What causes flowers to diverge? While a plant's primary pollinator should strongly influence floral phenotype, selective pressures may also be exerted by other flower visitors or competition with other plants for pollination. Species of the primarily bat‐pollinated genus Burmeistera (Campanulaceae) frequently cooccur, with up to four species in a given site, and broadly overlap in flowering phenology, typically flowering throughout the year. The genus displays extensive interspecific variation in floral morphology in the degree that the reproductive parts (anthers and stigma) are exserted outside of the corolla, and species can be roughly classified as either long or short‐exserted. I tested two hypotheses regarding the functional significance of such variation: (1) exsertion lengths correspond to pollination by bat species of different sizes; and (2) variation serves to partition pollinator's bodies spatially and thus reduces interspecific pollen transfer. I captured bats in Ecuador to evaluate the identity and location of the Burmeistera pollen they were carrying. Results show that exsertion does not correspond to specialization on different pollinators; different bat species carried pollen of both flower types just as frequently. In support of the second hypothesis, pollen from flowers of different exsertion lengths was found to occur on different regions of bats' heads. This may serve to reduce competition for pollination among coexisting Burmeistera.     

DNA from a 100-year-old holotype confirms the validity of a potentially extinct hummingbird species

We used mtDNA sequence data to confirm that the controversial 100-year-old holotype of the Bogotá sunangel (Heliangelus zusii) represents a valid species. We demonstrate that H. zusii is genetically well differentiated from taxa previously hypothesized to have given rise to the specimen via hybridization. Phylogenetic analyses place H. zusii as sister to a clade of mid- to high-elevation Andean species currently placed in the genera Taphrolesbia and Aglaiocercus. Heliangelus zusii, presumed extinct, has never been observed in nature by biologists. We infer that the species occupied a restricted distribution between the upper tropical and temperate zones of the northern Andes and that it was most probably driven to extinction by deforestation that accompanied human population growth during the nineteenth and early twentieth centuries. We demonstrate the feasibility of obtaining DNA from nearly microscopic tissue samples from old hummingbird specimens and suggest that these methods could be used to resolve the taxonomy of dozens of avian taxa known only from type specimens.     

Nectar regulation in Euphorbia tithymaloides L., a hummingbird‐pollinated Euphorbiaceae

Floral sexual phases can differ in nectar production and might be under selective pressure by pollinators. We studied Euphorbia tithymaloides, which has inflorescences that are initially female and then hermaphroditic. Volume and concentration of nectar were measured in both stages. Nectar production and the effect of extractions were determined using sets of bagged inflorescences; inflorescences in the hermaphroditic phase had higher values of nectar concentration, volume and sugar mass than inflorescences in the female phase. Nectar resorption was detected in senescent inflorescences. To test for homeostatic nectar regulation, artificial nectar was added and the response assessed after 24 h. The experiments showed that concentration and sugar mass are regulated within a narrow range, and the homeostatic points differ between the two sexual phases. These differences in nectar can be detected by hummingbirds, which prefer the female stage. Resorption and secretion seem to be part of a homeostatic mechanism by which nectar attributes are maintained to optimise sugar recovery.     

Low plant density enhances gene dispersal in the Amazonian understory herb Heliconia acuminata

In theory, conservation genetics predicts that forest fragmentation will reduce gene dispersal, but in practice, genetic and ecological processes are also dependent on other population characteristics. We used Bayesian genetic analyses to characterize parentage and propagule dispersal in Heliconia acuminata L. C. Richard (Heliconiaceae), a common Amazonian understory plant that is pollinated and dispersed by birds. We studied these processes in two continuous forest sites and three 1‐ha fragments in Brazil's Biological Dynamics of Forest Fragments Project. These sites showed variation in the density of H. acuminata. Ten microsatellite markers were used to genotype flowering adults and seedling recruits and to quantify realized pollen and seed dispersal distances, immigration of propagules from outside populations, and reproductive dominance among parents. We tested whether gene dispersal is more dependent on fragmentation or density of reproductive plants. Low plant densities were associated with elevated immigration rates and greater propagule dispersal distances. Reproductive dominance among inside‐plot parents was higher for low‐density than for high‐density populations. Elevated local flower and fruit availability is probably leading to spatially more proximal bird foraging and propagule dispersal in areas with high density of reproductive plants. Nevertheless, genetic diversity, inbreeding coefficients and fine‐scale spatial genetic structure were similar across populations, despite differences in gene dispersal. This result may indicate that the opposing processes of longer dispersal events in low‐density populations vs. higher diversity of contributing parents in high‐density populations balance the resulting genetic outcomes and prevent genetic erosion in small populations and fragments.     

Fluttering wing feathers produce the flight sounds of male streamertail hummingbirds

Sounds produced continuously during flight potentially play important roles in avian communication, but the mechanisms underlying these sounds have received little attention. Adult male Red-billed Streamertail hummingbirds (Trochilus polytmus) bear elongated tail streamers and produce a distinctive 'whirring' flight sound, whereas subadult males and females do not. The production of this sound, which is a pulsed tone with a mean frequency of 858 Hz, has been attributed to these distinctive tail streamers. However, tail-less streamertails can still produce the flight sound. Three lines of evidence implicate the wings instead. First, it is pulsed in synchrony with the 29 Hz wingbeat frequency. Second, a high-speed video showed that primary feather eight (P8) bends during each downstroke, creating a gap between P8 and primary feather nine (P9). Manipulating either P8 or P9 reduced the production of the flight sound. Third, laboratory experiments indicated that both P8 and P9 can produce tones over a range of 700-900 Hz. The wings therefore produce the distinctive flight sound, enabled via subtle morphological changes to the structure of P8 and P9.