Bills and tongues of nectar-feeding birds: A review of morphology,function and performance,with intercontinental comparisons

The bills and tongues of nectar-feeding birds differ from continent to continent. The major differences are that: (i) the tongues of A Australian honeyeaters are broader any more fimbricated at the tip than the bifurcated tongues of sunbirds and hummingbirds; (ii) the bills of hummingbirds are more uniformly narrow and taper less markedly towards their tips than those of sun-birds and honeyeaters; and (iii) bill curvatures are generally greater for sunbirds and honey-creepers than for hummingbirds. A variety of hummingbirds has straight or even slightly upturned bills, while bills for all sunbirds, honeycreepers and honeyeaters are decurved to some extent. Despite differences in tongue morphology, hummingbirds, sunbirds and honeyeaters extract nectar at a similar range of rates, averaging approximately 40 γL s^?1 from ad libitum feeders, and 1–15 γL^?1 from flowers. All tongues collect nectar by capillarity, with licking rates of 6–17 s^?1. Licking behaviour has been little studied, although speeds of licking respond to changes in sugar concentration and corolla length. The tongues of honeyeaters are broad, and may need to be brush-tipped in order to allow capillary collection of nectar. Brush-tipped tongues can cover large surface areas on each lick, and may allow honeyeaters to exploit nectar and honeydew that is thinly spread over large surface areas. Bill lengths of nectarivorous birds are similar in all regions, though species of hummingbird have the shortest and longest bills. Bill lengths largely determine the range of floral lengths that can be legitimately probed. Maximum floral lengths exceed bill lengths, since hummingbirds, sunbirds and honeyeaters protrude their tongues beyond the tips of their bills. Rates of nectar extraction, however, decline rapidly once the floral length exceeds bill length. Decurved bills may have evolved in honeyeaters and sunbirds to enable perching birds to reach flowers at the ends of branches more easily. Consistent differences in bill length between the sexes suggest that males and females may exploit different floral resources or different proportions of the same resources. For honeyeaters and sunbirds, males have longer bills than females, but the reverse is true for many hummingbirds.     

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.     

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.     

Morphological relationships of passerine birds from Australia and New Guinea in relation to their diets

Beak, wing, leg and intestinal lengths, and gizzard widths, were all significantly related to body mass in 51 honeyeater species from Australia, 48 honeyeater species from New Guinea and 31 purely insectivorous passerine bird species from Australia. The nectar-feeding honeyeaters had smaller gizzards and intestines than wholly insectivorous birds of comparable size, although their wing and leg lengths did not differ; New Guinean and Australian honeyeaters were similar in these respects. Overall, honeyeaters had longer beaks than pure insectivores. Among Australian honeyeaters, those genera consuming more nectar than insects had longer beaks than the less nectarivorous, more insectivorous genera. Indeed, the latter group had beaks comparable in length to wholly insectivorous birds. All morphological differences revealed were attributable to known differences in diet.     

Behavioural evidence for ultraviolet vision in a tetraonid species – foraging experiment with black grouse Tetrao tetrix

In addition to wavelengths visible to humans (400–700 nm), many birds are able to detect near ultraviolet light (320–400 nm). Most studies of ultraviolet (UV) vision in birds have concentrated on the importance of UV vision in intraspecific signalling, especially in passerine birds. However, birds may also use UV vision for other purposes, e.g. foraging. We performed a laboratory experiment to test whether a tetraonid species, black grouse Tetrao tetrix , could detect the difference between UV-reflecting and non-UV-reflecting food items (two colour morphs of bilberry Vaccinium myrtillus ). Black grouse preferred UV-reflecting berries when UV light was used for illumination, but showed no preference in the absence of UV light. This observation establishes a potential UV sensitivity in this species; such a sensitivity should be considered in behavioural experiments with this species.     

Nitrogen requirements of an old world nectarivore, the orange-tufted sunbird Nectarinia osea

Nectarivorous birds are represented by three major radiations: honeyeaters and sunbirds in the Old World and hummingbirds in the New World. Costa's hummingbirds and New Holland honeyeaters have unusually low nitrogen requirements, which have been related to the species' low-protein, high-sugar diets. Therefore, we hypothesised that orange-tufted sunbirds (Nectarinia osea) would likewise have low-maintenance nitrogen requirements and low rates of endogenous nitrogen loss. To test this hypothesis, we measured nitrogen balance, total endogenous nitrogen loss, and body mass changes in captive birds, using insects as a nitrogen source. Nitrogen balance, estimated by regression analysis to be 3.9 mg d(-1), was less than one-half of that allometrically predicted, while total endogenous nitrogen loss (1.9+/-0.6 mg d(-1)) was less than one-third of the allometrically predicted value. Thus, orange-tufted sunbirds follow the same pattern of low nitrogen requirements found in hummingbirds and honeyeaters. Total endogenous losses of nitrogen in nectarivores are low because a fibreless, easily digestible liquid diet reduces nitrogen losses in the feces, while the protein-sparing effect of a diet containing largely sugar leads to low endogenous urinary nitrogen losses.     

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.     

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.     

Asymmetrical competition between the bell miner (Manorina melanophrys,Meliphagidae) and other honeyeaters: evidence from Southeastern Victoria,Australia

Summary The Bell Miner (Manorina melanophrys, Meliphagidae) is a medium-sized, colonial and co-operatively breeding honeyeater. Recent works show that the Bell Miner presents clear patterns of interspecific competition involving aggressive behaviour against many honeyeaters (Meliphagidae) and other bird species (Loyn et al. 1983; Clarke 1984). Nevertheless, those works have been based on short-term (1 year or less) studies only, and none of them have studied the effect territorial defence has on Bell Miners' fitness. We show how the population of honeyeaters decreased over 7 years at the Sir Colin Mackenzie Zoological Park (Southeastern Victoria, Australia). The decrease of honeyeaters in the study site was correlated with a local increase in the Bell Miner population which has been expanding since at least 1983. This process presumably led to the spatial zonation of Bell Miners and honeyeaters observed at present, while other passerine species show no sensitivity to either the invasion of Bell Miners in the recent past or to the present spatial distribution of the Bell Miner population. Finally, we show that Bell Miner reproductive activity is not affected by their interaction with competitors, which leads us to conclude that the interaction between the Bell Miner and other honeyeaters would be better described as asymmetrical competition.     

Interspecific competition in Australian honeyeaters—depletion of common resources

Many species of honeyeaters and other nectar-feeding birds occur in most habitats in South Australia. They frequently feed on nectar of the same species of plants. A succession of species of plants provide nectar for birds throughout the year. Nectar is most abundant in winter and early spring and least abundant in summer and autumn. There is more nectar per flower and more flowers in winter and spring. Nectar is often depleted by honeyeaters, and sometimes other visitors (silvereyes, lorikeets and insects) between December and May. It is at times reduced to a level at which it is uneconomical for some species to exploit. There are seasonal movements of honeyeaters into areas of abundant nectar and out of these areas when nectar becomes scarce. Breeding coincides with peak abundance of nectar. Diversity of honeyeaters is probably maintained by an interaction of two types of competition, exploitation and interference. The larger species use the richest sources of nectar and aggressively exclude the smaller species (interference) whereas the smaller species can use poorer sources of nectar because their energy requirements are less (exploitation).     

Ecomorphological constraints imposed by the kidney component measurements in honeyeater birds inhabiting different environments

The histological renal anatomy of 10 species of honeyeaters was examined quantitatively, using stereology. The kidneys of five species of predominantly wet zone inhabiting birds: the western spinebill Acanthorhynchus superciliosus , White-checked honeyeater Phylidonyris nigra . New Holland honeyeater Phylidonyris novaehollandiae , little wattlebird anthochaera chrysoptera and red wattlebird Anthochaera carunculata , were compared to five predominantly arid zone inhabiting birds: the grey-fronted honeyeater Meliphaga plumula , white-plumed honeyeater Meliphaga penicillata , white-fronted honeyeater Phylidonyris albifrons , spiny-checked honeyeater Acanthogenys rufogularis and yellow-throated miner Manorina flarigula. The kidneys were asymmetrical, with the left kidney being larger than the right kidney. Kidney mass was directly proportional to body mass (coefficient of correlation, r =+0·95), as was kidney volume to kidney mass (r =+1·0). Wet zone honeyeaters generally and a higher percentage and absolute volume of renal cortex, whilst arid zone honeyeaters generally had a significantly higher percentage and absolute volume of renal medulla. There were few differences between species, in either the percentage or absolute volume or luminal surface area of nephron components within the cortex. Within the medulla, wet zone honeyeaters generally had a higher percentage and absolute luminal surface area of collecting ducts, whilst arid zone honeyeaters had a higher percentage and absolute surface area of capillaries. This may be due to factors such as variations in diet and climate between habitats resulting in differences in honeyeater renal morphology which enable arid zone birds to conserve water and wet zone birds to conserve ions more efficiently.     

The predictive power of pollination syndromes: Passerine pollination in heterantherous Meriania macrophylla (Benth.) Triana (Melastomataceae)

The cloud forest species Meriania macrophylla (Benth.) Triana has pseudocampanulate flowers with bulbous stamen appendages, typical for the passerine pollination syndrome found in the Melastomataceae tribe Merianieae. The species is further characterized by strong stamen dimorphism (heteranthery), a condition otherwise associated with pollen‐rewarding bee‐pollinated species (both in Melastomataceae and beyond). In passerine‐pollinated Merianieae, however, flowers usually only show weak stamen dimorphism. Here, we conducted field and laboratory investigations to determine the pollinators of M. macrophylla and assess the potential role of strong heteranthery in this species. Our field observations in Costa Rica confirmed syndrome predictions and indeed proved pollination by passerine birds in M. macrophylla. The large bulbous set of stamens functions as a food‐body reward to the pollinating birds, and as trigger for pollen release (bellows mechanism) as typical for the passerine syndrome in Merianieae. In contrast to other passerine‐pollinated Merianieae, the second set of stamens has seemingly lost its rewarding and pollination function, however. Our results demonstrate the utility of the pollination syndrome concept even in light of potentially misleading traits such as strong heteranthery.     

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.     

Distinctive convergence in Australian floral colours seen through the eyes of Australian birds

We used a colour-space model of avian vision to assess whether a distinctive bird pollination syndrome exists for floral colour among Australian angiosperms. We also used a novel phylogenetically based method to assess whether such a syndrome represents a significant degree of convergent evolution. About half of the 80 species in our sample that attract nectarivorous birds had floral colours in a small, isolated region of colour space characterized by an emphasis on long-wavelength reflection. The distinctiveness of this ‘red arm’ region was much greater when colours were modelled for violet-sensitive (VS) avian vision than for the ultraviolet-sensitive visual system. Honeyeaters (Meliphagidae) are the dominant avian nectarivores in Australia and have VS vision. Ancestral state reconstructions suggest that 31 lineages evolved into the red arm region, whereas simulations indicate that an average of five or six lineages and a maximum of 22 are likely to have entered in the absence of selection. Thus, significant evolutionary convergence on a distinctive floral colour syndrome for bird pollination has occurred in Australia, although only a subset of bird-pollinated taxa belongs to this syndrome. The visual system of honeyeaters has been the apparent driver of this convergence.     

Colour‐variable birds have broader ranges,wider niches and are less likely to be threatened

Coloration fulfils a variety of adaptive functions in animals. Colour variability, both between and within species, can be caused by different colours being favoured for different functions and in different environments. Thus, species with highly variable coloration may have greater potential to persist in new and changing environments. As a consequence, such colour‐variable species may be more able to adapt, colonize new areas and niches, occupy larger ranges, speciate more readily and in general be less vulnerable to environmental change and extinction. These predictions have been supported by comparative analyses on amphibians and reptiles. However, as coloration in ectotherms plays a key role in thermoregulation, it is unclear whether these results can be generalized to endotherms, such as birds and mammals. Here, we test the hypothesis that more colour‐variable endotherms occupy larger ranges/niches and are less vulnerable to the threat of extinction by focussing on colour variation in Australian parrots and passerine birds. As predicted, colour variability was correlated with range size (parrots and passerines) and niche breadth (dietary heterogeneity, parrots only). These relationships support the predicted link between colour variability and adaptability, whereby range size and niche breadth may be a cause of colour variability or vice versa. Irrespective, and as predicted, colour variability was lower in threatened species, even after statistically controlling for other confounding variables. Hence, our study supports the hypothesis that colour‐variable species in general are more resilient to environmental change.     

Morphology,nectar characteristics and avian pollinators in five Andean Puya species (Bromeliaceae)

Five Andean Puya species (Puya alpestris, Puya chilensis, Puya coerulea, Puya raimondii and Puya venusta) were studied to determine the relationship between their avian visitors, and plant morphology and nectar characteristics. Our results showed a significant relationship between nectar concentration, presence of sterile apex and avian pollinators's species. In contrast, nectar composition was not related to the frequency of avian visits. We found that Puya species were mainly visited by specialist nectarivorous birds such as hummingbirds (i.e., P. coerulea and P. venusta), lacked a sterile apex and produced high nectar concentration in low volumes. In contrast, species mainly visited by generalist passerines (i.e., P. chilensis and P. alpestris) were characterized by the presence of a sterile apex and production of highly diluted nectar in large volumes. In a mono-specific group we found that P. raimondii produces highly concentrated nectar in large volumes, and its flowers were visited by hummingbirds and passerine birds. We found no effect of nectar composition on bird's visits. Our study highlights the interplay between morphological traits, nectar characteristics and the ecological framework to explain specialized and generalized birds pollination systems.     

Foraging differences between white and dark morphs of the Pacific Reef Heron Egretta sacra

Among the species of diurnal herons (Ardeinae) showing light-dark colour polymorphism in plumage, colour phase is age-related in one species, closely associated with geography in three species, and found in most populations in three closely related species of reef herons. In Pacific Reef Herons Egretta sacra white-phased birds sought prey by a flight, land, and freeze hunting style in breaking surf, while dark birds pursued prey by actively walking or running on reef flats. On Mangaia, in the southern Cook Islands, more white-phased birds used the windward side of the island and more dark-phased birds used the lee side. On Rarotonga, 204 km from Mangaia, reef herons foraged almost exclusively in shaded streams and no entirely white-phased bird was encountered. These results provide the first evidence of differences in hunting techniques associated with colour morph and only the second observation of differences in habitat use by white- and dark-phased herons at single localities. As such they support Murton's (1971) idea that colour polymorphism serves herons in their role as predators. For reasons discussed in the text such differences are more expected in reef herons than in most other colour-polymorphic herons.     

A phylogenetic hypothesis for passerine birds: taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data

Passerine birds comprise over half of avian diversity, but have proved difficult to classify. Despite a long history of work on this group, no comprehensive hypothesis of passerine family-level relationships was available until recent analyses of DNA-DNA hybridization data. Unfortunately, given the value of such a hypothesis in comparative studies of passerine ecology and behaviour, the DNA-hybridization results have not been well tested using independent data and analytical approaches. Therefore, we analysed nucleotide sequence variation at the nuclear RAG-1 and c-mos genes from 69 passerine taxa, including representatives of most currently recognized families. In contradiction to previous DNA-hybridization studies, our analyses suggest paraphyly of suboscine passerines because the suboscine New Zealand wren Acanthisitta was found to be sister to all other passerines. Additionally, we reconstructed the parvorder Corvida as a basal paraphyletic grade within the oscine passerines. Finally, we found strong evidence that several family-level taxa are misplaced in the hybridization results, including the Alaudidae, Irenidae, and Melanocharitidae. The hypothesis of relationships we present here suggests that the oscine passerines arose on the Australian continental plate while it was isolated by oceanic barriers and that a major northern radiation of oscines (i.e. the parvorder Passerida) originated subsequent to dispersal from the south.     

Mutualistic interdependence between mistletoes (Amyema quandang), and spiny-cheeked honeyeaters and mistletoebirds in an arid woodland

The mutualism involving mistletoes (Amyema quandangj, spiny-cheeked honeyeaters (Acan-thagenys rufogularis) and mistletoebirds (Dicaeum hirundinaceum) was studied in arid woodland in South Australia between 1980 and 1984. Plants and birds were locally interdependent: mistletoes supplied a continuous resource of fruits or nectar that sustained permanent populations of pollinators (honeyeaters) and dispersers (honeyeaters and mistletoebirds). The reproductive phenology of Amyema quandang was central to the interactions. Amyema quandang flowered in winter and annual fruit crops overlapped so that ripe fruit was continuously available. Spiny-cheeked honeyeaters obtained most of their energy requirements from mistletoe nectar in winter and mistletoe fruit in summer. Higher honeyeater densities were sustained by flowering in winter. Mistletoebirds were present in low density throughout the year and subsisted on a diet of mistletoe fruit and a few insects. The reproductive strategy of A. quandang probably evolved in response to the pollination and dispersal service provided by honeyeaters in inland Australia. Neither spiny-cheeked honeyeaters nor mistletoebirds have adaptations resulting from evolutionary interactions with A. quandang. The high specificity of their mutualism is a result of: (i) the abundance of A. quandang in relation to other nectar and fruit producing plants in the community: (ii) the year-round production by A. quandang of the primary source of fruit or nectar for honeyeaters and mistletoebirds: (iii) the facultative specialization of both birds on A. quandang; and (iv) the reluctance or inability of other frugivorous birds in the community to consume A. quandang fruit.     

Relationships of Australo-Papuan songbirds-protein evidence

Allelic frequencies determined by protein electrophoresis were used to assess relationships and familial groupings among the Australian-New Guinean songbirds. Hypotheses of relationships were generated from the data by UPGMA, distance-Wagner and cladistic analyses. The resulting protein-based topologies were compared with recent DNA-DNA hybridization studies which separate the major Australo-Papuan families from Eurasian-centred groups and cluster them in a single endemic radiation. Although both data sets are concordant in may areas, they differ significantly in their alignment of the Australo-Papuan Menuridae, Climacteridae, Ptilonorhynchidae, Maluridae, Eopsaltriidae and Orthonychidae. Possible explanations for these discrepancies are examined. Both data sets otherwise agree in identifying an endemic radiation of Australo-Papuan songbirds in which some 75% of regional species are clustered in two principal assemblages. One includes the honeyeaters Meliphagidae and their allies Epthianuridae, Acanthizidae, Pardalotidae and, arguably, Eopsaltriidae (Australo-Papuan robins) and Orthonychidae (logrunners). The other comprises corvoid birds (Corvoidea), including Pachycephalidae, Monarchidae, Cracticidae, Artamidae, Paradisaeidae, Corvidae, Oriolidae, Campephagidae and possibly Ptilonorhynchidae (bowerbirds) amongst others. Menuridae (lyrebirds), Climacteridae (treecreepers), and Maluridae (fairy wrens) are also members of the radiation but of less certain affinity. The remaining species are grouped in a number of families forming a third assemblage of apparent Eurasian origin, the parvorder Passerida. The concept of a Gondwanan origin for the Passeriformes is canvassed.