African sunbirds hover to pollinate an invasive hummingbird-pollinated plant

Why do hummingbirds hover while Old World nectar‐feeding birds perch? A unique opportunity to explore this question is presented by the invasion into Africa of a plant adapted for pollination by hovering hummingbirds. Like other hover‐pollinated plants of the New World, the flowers of the tree tobacco Nicotiana glauca lack perches and are oriented towards open space. We find that Old World nectarivores, especially the malachite sunbird, Nectarinia famosa, hover 80% of the time when taking nectar from these flowers. They hover for up to 30 s, and are able to sustain this hovering lifestyle in an area where native nectar plants are absent. Nicotiana glauca greatly increases the local abundance of sunbirds compared with uninvaded areas. In turn, flowers visited by sunbirds formed significantly more capsules and set significantly more seed than sunbird‐excluded flowers, possibly facilitating the invasion. The results suggest a prominent role for plant, rather than bird traits in determining the occurrence of hover‐pollination, begging the question of why plants adapted for hover pollination do not occur outside the New World.     

Sunbird hovering behavior is determined by both the forager and resource plant

The long‐standing paradigm that pollination systems adapted to hovering birds evolved only in the New World was recently challenged by the discovery of hovering pollination by Old World specialized passerine pollinators. This raises the possibility that hovering pollination may evolve more easily than previously believed, given sufficient selective pressure on plant traits, on nectarivory, or both. We observed foraging behavior by the sunbird Cyanomitra oritis at flowers of the native Old World plant Impatiens sakeriana. We measured the length of pedicels and peduncles (PedPed length), which can make the flowers difficult to reach while the bird perches on the stem, and determined if it influenced sunbird hovering or perching at a flower. Detailed analyses of video recordings showed that sunbirds only hovered at flowers with a long PedPed, whereas they employed both foraging modes when an adequate perch was available. A hovering sunbird could deplete nectar in a shorter time than a perching one. The frequency of visits was not greater at flowers with longer PedPed or with more open I. sakeriana flowers in the vicinity. Our study provides evidence that sunbird behavior does not follow simple energetic models, and that some sunbird pollination systems in the Old World resemble highly specialized hummingbird systems in the New World much more than expected, especially the overall adaptation of the system to bird hovering.     

Pollen morphology in relation to pollinators in Papilionoideae (Leguminosae)

The surface sculpturing of the pollen of some species of the taxonomically widely separated genera Harpalyce (tribe Brongniartieae), Camoensia (tribe Sophoreae), Millettia (tribe Tephrosieae), and of the monotypic Dahlstedtia (tribe Tephrosieae) which have large red or white flowers adapted for pollination by birds or bats, is coarsely rugulate or verrucate. Related taxa with small insect pollinated flowers have pollen with simple reticulate or perforate surface sculpturing. The exine stratification of Alexa and Castanospermum (tribe Sophoreae), genera with large red bird-flowers, is complex with a layer of tectal columellae and differs from that of other genera in the tribe Sophoreae which have a normal pollen wall structure. These modifications of pollen structure and sculpture appear to be the result of convergent evolution and a secondary adaptation to pollination. The taxonomic and functional significance of the observations are briefly discussed.     

Why hummingbirds hover and honeyeaters perch

Evidence is presented in support of the suggestion that a hovering bird is able to move between flowers more quickly than one that is perching. This advantage to hovering may be offset, however, by the higher energetic costs of hovering as compared with perching. This trade-off is evaluated in two field situations, one for perching honeyeaters and the other for hovering hummingbirds. In each case it is estimated that the birds employ the foraging mode (hovering versus perching) that results in the greatest net rate of energy gain.     

Convergent evolution of sunbird pollination systems of Impatiens species in tropical Africa and hummingbird systems of the New World

The bird pollination systems of the New and Old Worlds evolved independently, and differ in many aspects. New World plants are often presented as those adapted to hovering birds while Old World plants to perching birds. Most Neotropical studies also demonstrate that in hummingbird species rich assemblages, only a small number of highly specialized birds exploits the most specialized plants with long corollas. Nevertheless, recent research on bird–plant pollination interactions suggest that sunbird pollination systems in the Old World have converged more with the highly specialized hummingbird pollination systems than previously thought. In this study we focus on the pollination systems of the bird pollination syndrome Impatiens species on Mt. Cameroon, West Africa. We show that despite the high diversity of sunbirds on Mt. Cameroon, only Cyanomitra oritis appear to be important pollinator of all Impatiens species. This asymmetry indicates the absence of pair wise co‐evolution and points to a diffuse co‐evolutionary process resulting in guilds of highly specialized plants and birds; a situation well known from hummingbirds and specialized plant communities of the New World. Additionally, the herbaceous habits of Impatiens species, the frequent adaptations to pollination by hovering birds, and the habitat preference for understory in tropical forests or epiphytic growth, resemble the highly specialized Neotropical plants. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 127–133.     

Hovering sunbirds in the Old World: occasional behaviour or evolutionary trend?

The nectarivory of sunbirds in the Old World and hummingbirds in the New World evolved independently. While both groups are specialised in their feeding apparatuses, hummingbirds are moreover famous for their adaptations to sustained hovering flight. Recently, an example of a pollination system of the invasive plant Nicotiana glauca has been used to show that less adapted sunbirds also are frequently able to hover. Nevertheless, the question has remained why plants adapted to bird hovering pollination do not occur outside the New World. In this paper we show that the long‐peduncle Cameroonian Impatiens sakeriana is not capable of autonomous selfing and can be pollinated only by two often hovering sunbirds, the Cameroon sunbird Cyanomitra oritis and the northern double‐collared sunbird Cinnyris reichenowi. Our study revealed that this plant is highly specialised for pollination by C. oritis. Cinnyris reichenowi hovers less frequently and often thieves nectar by piercing the flower spur when perching. This study shows that pollination systems occurring in the Old World follow similar evolutionary trends as systems including hovering hummingbirds in the New World.     

The Bizarre Inflorescence of Norantea brasiliensis (Marcgraviaceae): Visits of Hovering and Perching Birds1

The pollination biology of Norantea brasiliensis (Marcgraviaceae) was studied in the rain forest of southeastern Brazil. This plant presents bizarre, brush-type racemous inflorescences bearing numerous flowers and extrafloral cup-shaped nectaries. Flower anthesis is diurnal, nectar production is continuous and copious, and the sticky pollen is readily removed by visitors during the first morning hours. The ruby-coloured inflorescences were visited by eight species of hummingbirds (Trochilidae), and 10 species of passerine birds (three Coerebidae and seven Thraupidae). Hummingbirds hovered while probing for nectar and touched flowers occasionally, whereas passerine birds perched and made contact with flowers habitually. Due to differences in flower-visiting and general foraging behaviour, perching birds act as better pollen vectors than hovering birds. The inflorescence of Norantea brasiliensis seems well fitted for pollination by passerine birds, and the hexose-dominated nectar supports this idea. Pollination syndrome trends within Marcgraviaceae may stem from insect-pollinated, condensed and spike-like inflorescences which would give rise to bird-pollinated, brush-type inflorescences. From the same basic condensed inflorescence, bat-pollinated umbelliform inflorescence may be derived from bird-pollinated, pendulous and corymb-like inflorescences. These postulated inflorescence types are found among the extant species of Marcgraviaceae.     

Consequences of differences in body mass,wing length and leg morphology for nectar-feeding birds

Nectar-feeding birds are prominent in many parts of the world, and vary with respect to body size. Despite the availability of considerable morphometric data, few concerted efforts have been made to assess the influence of attributes such as mass, wing length and leg morphology upon the speed, acceleration, mode and energetic cost of movement by birds between flowers when foraging for nectar. This review attempts to consolidate and interpret available data and highlight areas where further investigations appear warranted. Australian honeyeaters are generally larger, and American hummingbirds smaller, than Hawaiian honeycreepers and sunbirds of Africa or Asia. Sunbirds, honeyeaters and honeycreepers generally perch while extracting nectar from flowers. Hummingbirds usually hover, apparently because suitable perches close to flowers are lacking, and not because hovering increases the speed at which flowers can be visited. Honeyeaters move from one flower to another at speeds that are at least as great as those for hummingbirds. Most passerine nectarivores need to ingest more nectar per day than hummingbirds in order to maintain energy balance, some species devoting more than 60% of the day to foraging. The major consequence of reduced foraging activity by hummingbirds, which spend only 5–30% of the day in this manner, appears to be male emancipation from nest construction and care of offspring. Large nectarivores have a greater capacity to store surplus food and to fast than smaller birds, and so can take advantage of short-lived peaks in nectar abundance. Nectarivores such as honeyeaters should therefore be favoured by the rapid diurnal changes in nectar availability which are characteristic of many Australian and African habitats. Body mass also determines the likely access to rich sources of nectar through size-related interspecific dominance hierarchies. In all families, larger species tend to monopolize the most rewarding nectar supplies, forcing smaller subordinate species to use poorer, more scattered sources. Within particular species, males usually have longer wings and greater masses than females. These variations imply that the two sexes differ with regard to their foraging ecology, although few supporting data are currently available.     

Why do some nectar foragers perch and others hover while probing flowers?

Diurnal hawkmoths, Hemaris fuciformis, and bumblebees, Bombus pasquorum, were observed foraging for nectar in flowers of Viscaria vulgaris. The hawkmoths hovered in front of the flowers, while the bees perched on them. The hawkmoths had a faster probing rate than the bees, and consequently also had higher gross and net rates of energy gain. A model is presented that shows that hovering only yields a higher net rate of energy gain (NREG) than perching when nectar volumes are high due to low competition for the resource. The difference in NREG of perchers and hoverers decreases with an increase of competition, and eventually perching yields the highest NREG. This is an effect of the higher cost of hovering. The results suggest that hovering can only evolve as a pure evolutionarily stable strategy (ESS) if competition is reduced, for example by co-evolutionary specializations with plants. The possibility that it has evolved as a mixed ESS (i.e. individuals can both hover and perch depending on the resource level) is discussed. The evolution of optimal foraging strategies is discussed, and it is pointed out that the rate of gain of an animal is independent of the strategy used when all competing foragers use the same strategy, but competitively superior strategies will nevertheless evolve because they are ESSs. Competition between strategies with different energy costs are special, because resource availability determines which strategy is competitively superior. A high-cost strategy can only evolve as a pure ESS at high resource levels, or as a mixed ESS at intermediate levels.     

The foraging behaviour of Australian honeyeaters: a review and some comparisons with hummingbirds

The foraging behaviour of Australian honeyeaters is reviewed in terms of diet, foraging selectivity, foraging flight mode, quality and quantity of nectar encountered per flower, flower densities encountered and effect of predation. At the same time comparisons are made between honeyeaters and hummingbirds. These two groups of birds are superficially similar. Both feed on nectar and insects. Both tend to have long curved bills and tongues adapted for removal of nectar from flowers. Both tend to feed at long, red flowers. However, on close inspection, honeyeaters and hummingbirds are quite dissimilar. For example, many honeyeaters include fruit in their diets. Hummingbirds almost never eat fruit. Honeyeaters appear to be considerably less nectarivorous and more insectivorous than hummingbirds. Honeyeaters are, for the most part, larger than hummingbirds and they usually perch while feeding whereas hummingbirds usually hover. Honeyeaters but not hummingbirds often flock while feeding. Predation appears to be considerably more important for honeyeaters than for hummingbirds. Territorial defense of flowers seems common in hummingbirds but uncommon in honeyeaters. These differences are discussed in detail and explanations are offered for them wherever possible.     

The north-east-Brazilian Liana, Adenocalymna dichilum (Bignoniaceae) pollinated by bats

BACKGROUND AND AIMS: Of the set of syndromes displayed by specialized (euphilic) flowers, adaptation to pollination by bats (chiropterophily) is the least known. Accumulated new evidence reveals that this pollination mode plays a considerable role in tropical communities, especially in the neotropics. One family in which bat-pollinated species are known in several genera is the Bignoniaceae. Here is reported, for the first time, bat pollination and floral ecology in Adenocalymna dichilum (tribe Bignonieae). METHODS: Floral features of this species growing in Bahia (north-east Brazil) indicated possible chiropterophily, which was subsequently confirmed by direct observation and from photographs of bat visits. Timing of anthesis and nectar parameters were monitored in the field, and floral morphology was investigated with fixed flowers. KEY RESULTS: One to two flowers open per night on the upright, simple racemes of A. dichilum during several weeks in a 'steady state' mode. The bilabiate, cream-coloured corollas are functional for only a single night and wilt during the following day. A stout corolla, with a musky odour, and a large nectary disc with large quantities of watery nectar also conform to the syndrome. Glossophaga soricina (Glossophaginae) visited and pollinated the flowers in a trap-lining manner. Whilst hovering, the bats put their heads into the corolla mouth for less than 1 s to feed, thereby effecting the transfer of pollen which is deposited on their backs. CONCLUSIONS: Adenocalymna, a New World genus comprising approx. 50 species, exhibits floral adaptive radiation including species pollinated by bees, birds and possibly moths. The discovery of chiropterophily in A. dichilum adds another facet to the array of floral syndromes represented in the genus.     

Nectar-feeding bird and bat niches in two worlds: pantropical comparisons of vertebrate pollination systems

Aim We review several aspects of the structure of regional and local assemblages of nectar‐feeding birds and bats and their relationships with food plants to determine the extent to which evolutionary convergence has or has not occurred in the New and Old World tropics. Location Our review is pantropical in extent and also includes the subtropics of South Africa and eastern Australia. Within the tropics, it deals mostly with lowland forest habitats. Methods An extensive literature review was conducted to compile data bases on the regional and local species richness of nectar‐feeding birds and bats, pollinator sizes, morphology, and diets. Coefficients of variation (CVs) were used to quantify the morphospace occupied by the various families of pollinators. The extent to which plants have become evolutionarily specialized for vertebrate pollination was explored using several criteria: number and diversity of growth forms of plant families providing food for all the considered pollinator families; the most common flower morphologies visited by all the considered pollinator families; and the number of plant families that contain genera with both bird‐ and bat‐specialized species. Results Vertebrate pollinator assemblages in the New World tropics differ from those in the Old World in terms of their greater species richness, the greater morphological diversity of their most specialized taxa, and the greater degree of taxonomic and ecological diversity and morphological specialization of their food plants. Within the Old World tropics, Africa contains more specialized nectar‐feeding birds than Asia and Australasia; Old World nectar‐feeding bats are everywhere less specialized than their New World counterparts. Main conclusions We propose that two factors – phylogenetic history and spatio‐temporal predictability (STP) of flower resources – largely account for hemispheric and regional differences in the structure of vertebrate pollinator assemblages. Greater resource diversity and resource STP in the New World have favoured the radiation of small, hovering nectar‐feeding birds and bats into a variety of relatively specialized feeding niches. In contrast, reduced resource diversity and STP in aseasonal parts of Asia as well as in Australasia have favoured the evolution of larger, non‐hovering birds and bats with relatively generalized feeding niches. Tropical Africa more closely resembles the Neotropics than Southeast Asia and Australasia in terms of resource STP and in the niche structure of its nectar‐feeding birds but not its flower‐visiting bats.     

A new Eocene swift-like bird with a peculiar feathering

A new taxon of swift-like birds is described from the Middle Eocene of Messel (Germany). It is tentatively assigned to the extinct family Jungornithidae and exhibits a completely unexpected feathering, which contrasts sharply with that of recent swifts. The short and rounded wings clearly show that it was not adapted to gliding, but might have caught its prey by sallying flights from a perch. The tail of the new taxon is very long and the tail feathers are broad and nearly symmetrical. The phylogenetic relationships between the Jungornithidae and other apodiform birds are still not convincingly resolved. The early Oligocene genus Jungornis itself shares unique derived characters with hummingbirds which are, however, absent in the Eocene genus Argornis and in the new taxon from Messel.     

Transfer of pollinaria on birds’ feet: a new pollination system in orchids

We report the discovery of a new mechanism of pollination in orchids: transfer of pollinaria on the feet of birds. Observations carried out in South Africa and Malawi showed that the orchids Disa chrysostachya Sw. and Disa satyriopsis Kraenzl. are pollinated by sunbirds. Pollinaria of these orchids become attached firmly to the birds toes when they perch on the tall narrow inflorescences which are packed tightly with numerous small orange flowers. Birds typically perch on the lower part of an inflorescence while reaching up to feed on nectar in flowers on the upper part, but occasionally reverse this position to probe the lower flowers. The nectar is contained within a short bulbous spur with a narrow entrance that permits entrance of a sunbirds slender tongue. Contrary to expectation, the pollination mechanism in D. chrysostachya is remarkably efficient with about 6.1% of pollen reaching stigmas on other plants and fruit set occurring in 95% of flowers at one site. Birds seldom move their feet once perched, thus minimizing the incidence of self-pollination, either within or between flowers on an inflorescence.     

Effects of density on perching behavior of broiler chickens

Exercise through perching has been suggested as a way to reduce the impact of leg problems in broiler chickens. It is possible that higher stocking densities may motivate birds to perch more, and perhaps reduce some of the detrimental effects to broiler health seen with high stocking densities. The goal of this research was to investigate the effects of density (10, 15, and 20birds/m(2)) and perch design on the frequency of perch utilization. Mixed sex broilers were assigned to 36 pens in a four perch treatmentxthree density factorial with three replications for each treatment/density combination in a randomized complete block design. Pens were assigned to one of four perch treatments: control (no perches), horizontal (three horizontal perches), angled (three 10 degrees angled perches), or mixed angle (one horizontal, one 10 degrees angled, and one 20 degrees angled perch), at each of the three densities. The results show that although the frequency of perch use was low, (2.6%+/-0.15), significant preferences were clear. Perching frequency was significantly higher when birds were raised at stocking densities of 15 (2.88+/-0.303) or 20birds/m(2) (2.76+/-0.211), as opposed to 10birds/m(2) (2.10+/-0.209) as indicated by a marginally significant main effect (p<0.0597), and a significant linear effect (P<0.0427). The birds used the horizontal perches the most, followed by 10 degrees angled and mixed angle perch treatments with decreasing frequency. An effect of age was found, in that perching increased during the first 4 weeks, and dropped off significantly at the end of the rearing period for all perch treatments. In general, perches closest to the hallway or outside of the house were used more than perches in the middle of the pen. Preferential use of the highest section of the 10 degrees angled perches was also found. The applied perch treatments or densities did not significantly affect final body weight or feed conversion. Percent mortality due to heat stress showed a significant increase with density, while mortality not caused by heat stress did not change with perch treatment or density.     

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.     

Ornithophilie auf den Canarischen Inseln

(1) On the Canary Islands and Madeira typical bird-flowers occur in at least twelve species of six genera, although true flower-birds are absent. This inconsistency is in part elucidated by field observations on exotic and wild plants of Tenerife. —(2) In the Botanical Garden of Orotava it could be observed that various ornithophilous plants, which were introduced there, were visited by indigenous birds for nectar and in one case (Orthostemon) for food tissue. Of the three bird species involved, an endemic race of Chiffchaff (Phylloscopus collybita) and resident Blackcaps (Sylvia atricapilla) exploit, and pollinate, flowers legitimously, while the Wild Canary (Serinus canaria) is predominantly a destructive nectar robber. —(3) The insular Chiffchaff also proved to be a regular pollinator in the wild, at least ofCanarina canariensis andIsoplexis canariensis, two ornithophilous paleoendemics. Ornithophily, thus, is naturally practised on the island, though by birds basically insectivorous. —(4) A list of Macaronesian plants bearing the more or less complete ornithophilous syndrome is presented, including newly recognizedTeucrium heterophyllum andScrophularia calliantha. —(5) On biogeographical and faunistic grounds it is presumed that the modern visitors of Canarian bird flowers are secondary rather than the original partners of the continental tertiary flora in which these plants originated. Palearctic immigrants, when becoming resident on the islands during and since the Pleistocene, adopted facultative nectar feeding, entering an orphaned food niche. Casual flower visits in Europe suggest a certain predisposition of the Chiffchaff and the Blackcap for the exploitation of flowers. — (6) The ability of unspecialized birds to acquire nectardrinking spontaneously and to pass this habit on to their offspring, is demonstrated by a population of Tree Sparrows (Passer montanus) which have visited ornithophilousKniphofia (Liliaceae) in Berlin for several years.

     

How Lovebirds Maneuver Rapidly Using Super-Fast Head Saccades and Image Feature Stabilization

Diurnal flying animals such as birds depend primarily on vision to coordinate their flight path during goal-directed flight tasks. To extract the spatial structure of the surrounding environment, birds are thought to use retinal image motion (optical flow) that is primarily induced by motion of their head. It is unclear what gaze behaviors birds perform to support visuomotor control during rapid maneuvering flight in which they continuously switch between flight modes. To analyze this, we measured the gaze behavior of rapidly turning lovebirds in a goal-directed task: take-off and fly away from a perch, turn on a dime, and fly back and land on the same perch. High-speed flight recordings revealed that rapidly turning lovebirds perform a remarkable stereotypical gaze behavior with peak saccadic head turns up to 2700 degrees per second, as fast as insects, enabled by fast neck muscles. In between saccades, gaze orientation is held constant. By comparing saccade and wingbeat phase, we find that these super-fast saccades are coordinated with the downstroke when the lateral visual field is occluded by the wings. Lovebirds thus maximize visual perception by overlying behaviors that impair vision, which helps coordinate maneuvers. Before the turn, lovebirds keep a high contrast edge in their visual midline. Similarly, before landing, the lovebirds stabilize the center of the perch in their visual midline. The perch on which the birds land swings, like a branch in the wind, and we find that retinal size of the perch is the most parsimonious visual cue to initiate landing. Our observations show that rapidly maneuvering birds use precisely timed stereotypic gaze behaviors consisting of rapid head turns and frontal feature stabilization, which facilitates optical flow based flight control. Similar gaze behaviors have been reported for visually navigating humans. This finding can inspire more effective vision-based autopilots for drones.     

A test of pollinator specificity and morphological convergence between nectarivorous birds and rainforest tree flowers in New Guinea

Interactions between flowering trees in a representative sample of vegetation, and the birds that fed at their flowers, were studied for 2 years in lowland tropical hill forest in New Guinea. All 2,200 trees in a 3-ha plot were tagged, identified, mapped, and monitored monthly. Approximately 60% of all individual trees flowered during the study; all species that these flowering individuals belonged to were evaluated for bird visitation. Approximately 13% of the 164 resident species of New Guinea avifauna at the study site, especially honeyeaters and parrots, visited flowers. In the forest inventory plot, approximately 15–22% of all 86 tree species that flowered during the study were visited by birds; most of these tree species were canopy species. Results showed that there was no statistically significant correlation between bird species grouped by bill morphology and flower species grouped as morphotypes and ranked by nectar accessibility, although strong but unexpected bird/plant associations were evident. These associations may be related to variables such as body mass or perch size. These results are discussed in comparison with results from the Neotropics and Australia, and in terms of morphological convergence and pollinator specificity in pollination systems.     

Evolutionary associations between nectar properties and specificity in bird pollination systems

A long-standing paradigm in biology has been that hummingbirds and passerine birds select for different nectar properties in the plants they pollinate. Here we show that this dichotomy is false and a more useful distinction is that between specialized and generalized bird pollination systems. Flowers adapted for sunbirds, which are specialized passerine nectarivores, have nectar similar to that of hummingbird flowers in terms of volume (approx. 10-30 microl), concentration (approx. 15-25% w/w) and sucrose content (approx. 40-60% of total sugar). In contrast, flowers adapted to generalized bird pollinators are characterized by large volumes (approx. 40-100 microl) of extremely dilute (approx. 8-12%) nectar with minimal sucrose (approx. 0-5%). These differences in nectar traits are highly significant even when statistical analyses are based on phylogenetically separate pairwise comparisons between taxa. We present several hypotheses for the association between nectar properties and specificity in bird pollination systems.