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.     

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.     

Nectar depletion and its implications for honeyeaters in heathland near Sydney

Several researchers have attempted to calculate whether depression of nectar resources by Australian honeyeaters is likely to limit their densities. Such calculations can be misleading, however, and do not directly test whether birds depress nectar availability. I monitored changes in nectar availability during the 8–9 months that honeyeaters bred in heathland near Sydney, and caged inflorescences to test whether nectar availability was being depressed by birds. There were pronounced seasonal changes in nectar availability in each of 2 years, and caging substantially increased the amounts of nectar in inflorescences during months when nectar production was low. The effects of caging must have resulted from exclusion of honeyeaters, as: (i) open-ended cage controls showed that the effects of caging resulted from exclusion of foragers, not from artifacts of caging; (ii) day-only and night-only caging showed that nectar was depleted only during the day: and (iii) observations showed that cages did not exclude any diurnal foragers other than honeyeaters. Resident honeyeaters spent more time foraging during months when nectar was scarce, implying that the rates at which they could obtain nectar were affected by changes in nectar availability. It is therefore possible that the depletion of nectar by honeyeaters could have limited their densities. However. I argue that such limitation could only be inferred safely if nectar-supplementation experiments showed survival and/or reproduction to be limited by nectar availability.     

Nectar utilization and pollination by Australian honeyeaters and insects visiting Calothamnus quadrifidus (Myrtaceae)

Nectar availability in Calothamnus quadrifidus flowers was studied at Wongamine Nature Reserve in late spring (November). Despite some overnight depletion by moths and other invertebrates, more nectar was present in flowers at dawn than at the preceding dusk. Significant nectar depletion occurred within a few hours after dawn, mainly due to foraging by two honeyeater species. Lichmera indistincta and Phylidonyris nigra. Thereafter, nectar availability was maintained at relatively low levels, principally because of foraging by honeyeaters and honey bees. Apis mellifera, that became active during the warmer part of the day. Although individual honeyeaters consumed more nectar than A. mellifera, honey bees were so abundant that their total impact was greater than that of either honeyeater species for much of the day. Transfer of C. quadrifidus pollen between flowers is necessary in order to achieve a high level of seed set, as the flowers appear to be protandrous. Honeyeaters appeared to be considerably more significant pollen vectors than A. mellifera.     

Nectar as food for birds: the physiological consequences of drinking dilute sugar solutions

 Nectarivory has evolved many times in birds: although best known in hummingbirds, sunbirds and honeyeaters, it also occurs on an opportunistic basis in a varied assortment of birds. We present a phylogenetic analysis of the distribution of nectarivory in birds. Specialised avian nectarivores are generally small, with an energetic lifestyle and high metabolic rates. Their high degree of dependence on nectar as a food source has led to convergence in morphological, physiological and behavioural adaptations. We examine the constituents of nectar which are most important to bird consumers, and how the birds deal with them in terms of physiology and behaviour. There are still unanswered questions: for example, the dichotomy between sucrose-rich nectars in hummingbird-pollinated plants and predominantly hexose-rich nectars in sunbird-pollinated plants appears to have little to do with bird physiologies and may rather reflect patterns of nectar secretion. Received November 28, 2002; accepted January 26, 2003 Published online: June 2, 2003     

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).     

Honeyeater population changes in relation to food availability in the Jarrah forest of Western Australia

The numbers of honeyeaters present at particular sites in the Jarrah forest varied significantly from month to month, with peak abundance occurring between May and September. Numbers also varied from site to site, depending upon the major plant species present. Honeyeater abundance was not limited by arthropod availability, but in many instances was closely correlated with the availability of nectar, particularly that produced by Dryandra sessilis. Large honeyeaters, such as Anthochaera chrysoptera and Phylidonyris novaehollandiae, were generally most abundant at times and sites of greatest nectar production. Small honeyeaters, such as Acanthorhynchus superciliosis, were never abundant but were present for most of the year. The production of nectar between October and December was such that more honeyeaters could have been supported than were actually present. Low numbers at these times can be explained in terms of reduced foraging efficiency that would have resulted from more widely dispersed flowers, and the possible availability of more rewarding nectar resources at other sites.     

Energy regulation by traplining hummingbirds

1. A published model of constant diurnal energy accumulation by territorial hummingbirds does not accurately reflect the temporal distribution of feeding behaviour of traplining hummingbirds, Phaethornis longirostris (Long-Tailed Hermit Hummingbirds).
2. In an enclosure study, gross nectar intake by P . longirostris decreased through the day, mirroring nectar production rates in its natural food-flowers and mimicking its natural foraging patterns.
3. Using a simulation model, the energetic consequences of constant and decreasing net energy intake rates for traplining hummingbirds are compared.
4. Given natural patterns of nectar production, model birds with decreasing diurnal net intake rates met their energetic needs with fewer flowers than those with constant net intake, and spent less time foraging.
5. It is concluded that P . longirostris do not satisfy the physiological assumptions of the published model, and that in this way they are different from the territorial species on which the model has previously been tested.     

Partitioning of nectar sources in an Australian honeyeater community

Feeding by honeyeaters was found to maintain nectar at low levels at three sites studied on Kangaroo Island in May-June 1978. The productivity of nectar at a site and position in a dominance hierarchy appeared to determine which bird species used each site. Correa was the main nectar source in the poorest area and produced 0.05 kJ m^?2 per day. The small eastern spinebill was the most abundant honeyeater. The purple-gaped honeyeater also occurred but fed mostly on honeydew. The medium sized New Holland honeyeater was common and territorial in the second area, where Banksia marginata and B. ornata inflorescences and Adenanthos flowers produced 0.7 kJ m^?2 of nectar per day. Spinebills and crescent honeyeaters also visited flowers and were sometimes chased by New Holland honeyeaters. The richest site was a flowering Eucalyptus cosmophylla tree (5.1 kJ m^?2 of nectar per day). A red wattlebird, the largest honeyeater, held a territory in part of this tree and chased other honeyeaters from the territory. New Holland, crescent and purple-gaped honeyeaters fed on flowers in other parts of the tree. The spinebill was absent. We conclude that nectar was partitioned along a spectrum of rich to poor sources. Larger more aggressive species used and sometimes defended the richest sources while the smaller birds used the poorer sources.     

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.     

What do foraging hummingbirds maximize?

Summary Hainsworth and Wolf (1976) reported that under certain conditions hummingbirds made food choices which did not maximize their net rate of energy intake while foraging. They concluded that the birds were not foraging optimally. We show here that their birds probably maximized a different utility function, the net energy per unit volume consumed (NEVC), which appears to be an optimal choice on a time scale longer than that of a foraging bout. Our own experiments with Archilochus colubris support the conclusion that hummingbirds make foraging decisions that maximize NEVC. A simulation model shows that, in nature, NEVC maximization would require fewer foraging trips and visits to fewer flowers per day to balance daily energy budgets. For territorial birds this can lead to smaller territory sizes and reduced costs of territorial defense. Plants that evolutionarily increase corolla length to enhance pollinator specificity need only increase nectar concentration slightly to maintain the same net energy per unit volume consumed (NEVC) by a given hummingbird pollinator.     

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.     

Sugar preferences and digestive efficiency in an opportunistic avian nectarivore, the Dark-capped Bulbul Pycnonotus tricolor

It has recently been recognized that flowers pollinated by generalist opportunistic nectarivores tend to have different nectar properties to those pollinated by specialist nectarivores (including both hummingbirds and specialist passerines). While renewed interest in specialist avian nectarivore sugar preferences and digestive physiology has helped explain the concentrated sucrose-dominated nectar of plants they feed on, there has been little progress in understanding why generalist or occasional nectar-feeding birds tend to be associated with flowers that have dilute hexose-dominated nectar. We examined sugar preferences and assimilation efficiencies over a range of concentrations, and concentration preferences, in Dark-capped Bulbuls Pycnonotus tricolor, one of the more common occasional avian nectarivores in southern Africa. Dark-capped Bulbuls showed significant preference for hexose sugar solutions, irrespective of concentration, when given a choice between hexose and sucrose solutions in equicaloric pair-wise choice tests conducted at five different concentrations (5–25%). This contrasts with results from specialist nectarivore groups which generally show a significant concentration-dependant switch in preference from hexose at low concentrations to sucrose at high concentrations for equicaloric solutions. In addition, Dark-capped Bulbuls showed an unusual lack of preference for solutions of higher sugar concentration when simultaneously offered four solutions varying in concentration from 10 to 25%. Dark-capped bulbuls also showed a unique effect of concentration on sugar assimilation efficiency, assimilating relatively more energy on 5% diets than on 25% diets. Although able to assimilate sucrose effectively, assimilation rates of hexose sugars were marginally higher. These results shed new light on pollination systems involving occasional nectarivores and, in particular, help to explain the prevalence of low concentration hexose-dominated nectars in flowers pollinated by these birds.     

Response of avian nectarivores to the flowering of Aloe marlothii : a nectar oasis during dry South African winters

In southern Africa, Aloe marlothii flowers during the dry winter season and offers copious dilute nectar to a variety of birds. Avian abundance and community composition were monitored at an A. marlothii forest at Suikerbosrand Nature Reserve, South Africa. Sampling occurred during two summer months (February–March) when no flowers were present, and six months (May–October) that spanned the winter flowering. We hypothesized that an influx of occasional nectarivores to the A. marlothii forest during flowering would lead to significant changes in the avian community. Overall bird abundance increased 2–3 fold at the peak of nectar availability (August). We recorded 38 bird species, of 83 species detected during transects, feeding on A. marlothii nectar; this diverse assemblage of birds belonged to 19 families, including Lybiidae, Coliidae, Pycnonotidae, Sylviidae, Cisticolidae, Muscicapidae, Sturnidae, Ploceidae and Fringillidae. Surprisingly, only two species of sunbird (Nectariniidae) were observed feeding on A. marlothii nectar, and both occurred in low abundance. We predicted that competition for nectar resources would be high, but few aggressive inter- and intra-specific interactions occurred between birds while feeding on inflorescences. During peak flowering, insect feeders (insectivores, omnivores, nectarivores) fed on nectar during the cold morning when insect activity was low, whilst non-insect feeders (frugivores and granivores) fed on nectar in the middle of the day. Our study highlights the importance of A. marlothii nectar as a seasonal food and water source for a diverse assemblage of occasional nectarivores.     

Timing in free-living rufous hummingbirds, Selasphorus rufus

Animals organize their lives around circannual and circadian rhythms, but little is known of their use of much shorter intervals. In the laboratory, some animals can learn the specific duration (seconds or minutes) between periods of food access. It has been supposed that wild nectarivores, such as hummingbirds, might also learn short time intervals so as to avoid revisiting emptied flowers until the nectar has been replenished. We provided free-living, territorial rufous hummingbirds each with eight artificial flowers containing sucrose solution. Four flowers were refilled 10 min after the bird emptied them, and the other four were refilled 20 min after being emptied. Throughout the day, birds revisited the 10 min flowers significantly sooner than they revisited the 20 min flowers, and return visits to the flowers matched their refill schedules. Hummingbirds remembered the locations and timing of eight rewards, updating this information throughout the day. Not only is this the first time that this degree of timing ability has been shown in wild animals, but these hummingbirds also exhibit two of the fundamental aspects of episodic-like memory (where and when), the kind of memory for specific events often thought to be exclusive to humans.     

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.     

Diurnal foraging‐mode shifts and food availability in nectarivore assemblages during winter

Abstract Temporal fluctuations of food resources and foraging activities have been studied extensively, especially at longer timescales (monthly, seasonally, among years). However, short‐term variation (e.g. within days) is less well understood. Here we systematically quantified diurnal patterns of foraging by nectarivorous birds (meliphagid honeyeaters) that numerically dominated stands of a winter‐flowering eucalypt, the red ironbark, Eucalyptus tricarpa, in central Victoria, Australia. Diurnal variation in food resources also was measured. Data were collected in winter. Anecdotal observations that honeyeaters change from almost exclusive nectarivory early in the day to a higher fraction of insectivory – especially aerial hawking – later in the day were confirmed, although in areas of high flowering intensity, nectar‐feeding remained the dominant foraging activity throughout the day. Local climatic factors (ambient temperature, windiness and cloud cover) all varied systematically through the day. Together, results were consistent with a change in foraging emphasis to greater insectivory as a function of elevated activities of insects (especially aerial ones), which was probably fostered by higher ambient temperatures. Contrary to energetic expectations, the nectarivores were very active early in the morning when ambient temperatures averaged approximately 3°C, well below thermoneutral temperatures. We deduced that the potential benefits of gathering as much energy‐rich nectar as possible before it was depleted outweighed the high costs of activities at low temperatures.     

Ornithophilous canopy species in the Atlantic rain forest of southeastern Brazil

ABSTRACT.   In tropical ecosystems, birds play a relevant role in plant reproduction. Although hummingbirds are regarded as the most important vertebrate pollinators in the Neotropics, the possible role of perching birds as pollinators has been neglected. From 2003 to 2005, we observed 68 species of plants visited by birds in an Atlantic rainforest in southeastern Brazil, including three canopy species: Spirotheca rivieri (Malvaceae, Bombacoidea), Schwartzia brasiliensis (Marcgraviaceae), and Psittacanthus dichrous (Loranthaceae). Flowers of these three species were visited by 15 different species of perching birds and by hummingbirds. The flowers of these three plants are colorful, ranging from deep red or purple to orange. Spirotheca rivieri blooms during the austral winter and Schwartzia brasiliensis during the summer. The flowers of these two species produce copious amounts of dilute nectar in easily accessible structures and both species appear to depend primarily on perching birds as pollinators, with hummingbirds being secondary or minor pollen vectors. The tubular, narrow flowers of P. dichrous are produced during the austral summer and are visited primarily by hummingbirds. Perching birds also visit the flowers, but destroy them. Our results suggest that previous estimates of the number of perching birds that feed on nectar may be too low and that flowers pollinated by perching birds may be more common in the canopy of Neotropical forests than previously thought.     

Competition between hummingbirds and bumble bees for nectar in flowers of Impatiens biflora

Summary Using removal experiments and concurrent measurement of resource levels, evidence was obtained for exploitation competition between Ruby-throated hummingbirds and two bumble bee species (Bombus fervidus and B. vagans) foraging for nectar on Impatiens biflora.When all three species were active, flower visitors showed a complex pattern of resource partitioning involving both diel and spatial changes. Hummingbirds foraged almost exclusively from the outermost exposed flowers on plants from which they drained nectar levels beyond the reach of bees over most of the day. In contrast the longtongued bee species (B. fervidus), and the shorter-tongued B. vagans, displayed a preference for the innermost flowers on plants which were protected from hummingbird visitation by surrounding vegetation. The two Bombus spp. began foraging at different times during the day: B. vagans were most active in early morning but were replaced by B. fervidus later in the day.When hummingbirds were rare, only B. fervidus showed evidence of competitive release: an increase in the number of foragers and a broadening of flower choice to include more outer flowers. Workers of B. vagans showed a similar response to temporary removal of B. fervidus and also extended their foraging over the entire day. These responses were consistent with changes in the availability of nectar to different species.Removal experiments demonstrated that individuals of one species can be largely excluded from access to nectar resources as a direct result of exploitation of nectar by foragers of other species with longer tongues. Thus in this system interspecific exploitation is an important mechanism involved in resource partitioning.     

The exploitation of floral nectar in Eucalyptus incrassata by honeyeaters and honeybees

Summary During October and November, 1977, a study of nectar production and nectarivore foraging in Eucalyptus incrassata was conducted at Wyperfeld National Park in south-eastern Australia in order to evaluate the extent to which introduced honeybees (Apis mellifera) compete with native honeyeaters for floral nectar. Data on nectar production, nectar availability, ambient air temperature and the numbers of visiting honeyeaters and honeybees were collected. Most of the daily nectar production in E. incrassata occurs early in the morning when temperatures are too low for insects to forage. In addition, insects, particularly honeybees, are unable to exploit nectar in the youngest flowers because the stamens are clustered tightly around the style. As a result of these temporal and structural characteristics of the flowers, honeyeaters are able to harvest most of the nectar. Honeybees potentially have access to 35–47% of the average daily production of floral nectar in E. incrassata and actually harvest considerably less. These data show that E. incrassata flowers are adapted to restrict insect foragers despite their superficially unspecialized appearance. Eight forest and woodland eucalypts do not have a flower stage which excludes insects and the significance of this difference is discussed.