The role of size and dominance in the feeding behaviour of coexisting hummingbirds

Interspecific competition can strongly influence community structure and limit the distribution and abundance of species. One of the main factors that determine hummingbird community structure is competition for food. The temporal and spatial distribution of nectar has a strong impact on hummingbird assemblages, shaping foraging niches according to hummingbird dominance and foraging strategy. We investigated whether body size and the degree of aggressive dominance influence feeding behaviour of hummingbirds in a temperate forest in northwestern Mexico (El Palmito, Mexico) when winter migrant hummingbirds are present in the community. First, we determined the dominance status of hummingbirds and evaluated the relationship between dominance and body mass, wing disc loading and migratory status. Secondly, we determined how hummingbird species used plant species differently. Thirdly, we examined whether the most dominant hummingbird species defended floral patches with more energy and/or with a larger number of flowers. At each flower patch, hummingbird species, number of hummingbird interactions, feeding time and number of flowers present were recorded. The total number of calories available within each floral patch was also determined. Our results demonstrate that the dominance hierarchy of 13 hummingbird species (migratory and resident) was correlated with body size but not wing disc loading, and that members of the hummingbird community showed a clear separation in resource use (by plant species). Hummingbirds at the top of the dominance hierarchy defended and fed on the best flower patches, defined by the quantity of calories available. Hence, the feeding behaviour of hummingbirds at El Palmito depends on the abundance of plant species used by hummingbirds and on the amount of energy available from each flower patch. Thus, hummingbird body size, aggressive dominance and defence of quality flower patches determines niche partitioning among species.     

Nectar extraction by hummingbirds: response to different floral characters

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

The organization of a honeyeater community in an unpredictable environment

The honeyeater community of an open-layered forest was studied in the New England National Park over a 2.5 year period. Various aspects of honeyeater behaviour (aggression, social and foraging) were examined during transects and by use of time-budgets. Time-budgets were used to estimate the daily energy requirements for each species. Since nectar availability in the study area was variable, the energy produced per day by the nectar sources was occasionally insufficient to meet the daily energy demands of the honeyeater community. No strong spatial partitioning of the nectar resources by the birds was found. Use of the resources appeared to be based primarily on dominance interactions (interspecific aggression), with the larger species tending to dominate the smaller ones. Smaller species survive in the area because of their behavioural attributes and greater foraging efficiency which enables them to use the sparse supply of nectar on poor days. Temporal gradients in nectar richness may be just as important as spatial gradients in permitting the coexistence of species which use the same resource in the same habitat. Most of the results from this study fail to support the predictions made elsewhere concerning the organization of communities in unpredictable environments.     

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.     

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

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

Floral resources and hummingbirds on an island of flooded forest in Central Brazil

Nectar availability for hummingbirds was studied for two and a half years in an island of flooded forest in Uberlândia, MG, in the Cerrado region, the Neotropical savanna areas in Central Brazil. Flowering individuals of ten plant species from eight families that offered resources potentially used by hummingbirds were recorded along transects crisscrossing the area, which were surveyed every other week. The number of flowers was estimated for each plant. The volume and concentration of nectar were measured for a sample of flowers of each species, and the data were used to estimate the caloric content available per flower and the general resource availability in the area throughout the study period. Focal observations of hummingbird visits were carried out on blooming individuals of all plant species. Hummingbird flowers occurred throughout the study period between January 2001 and June 2003. Only three of the studied plants did not present clear ornithophilous features. Six hummingbird species were recorded in the area, but total nectar availability in the area was seldom sufficient for the daily energy requirements of a single bird. Therefore, it can be inferred from the study that these hummingbirds need to move among the mosaic of different plant physiognomies in the region in order to obtain enough energy for their survival. These movements may also contribute to increasing gene flow and regeneration of plant populations isolated in forest patches as the one studied here.     

Nectar robbing in Ipomopsis aggregata : effects on pollinator behavior and plant fitness

Hummingbirds foraging in alpine meadows of central Colorado, United States, face a heterogeneous distribution of nectar rewards. This study investigated how variability in nectar resources caused by nectar-robbing bumblebees affected the foraging behavior of hummingbird pollinators and, subsequently, the reproductive success of a host plant (Ipomopsis aggregata). We presented hummingbirds with experimental arrays of I. aggregata and measured hummingbird foraging behavior as a function of known levels of nectar robbing. Hummingbirds visited significantly fewer plants with heavy nectar robbing (over 80% of available flowers robbed) and visited fewer flowers on those plants. These changes in hummingbird foraging behavior resulted in decreased percent fruit set as well as decreased total seed set in heavily robbed plants. These results indicate that hummingbird avoidance of nectar-robbed plants and flowers reduces plant fitness components. In addition, our results suggest that the mutualisms between pollinators and host plants may be affected by other species, such as nectar robbers. Received: 22 April 1998 / Accepted: 12 May 1998     

The effect of hummingbird flower mites on nectar availability of two sympatric Heliconia species in a Brazilian Atlantic forest

BACKGROUND AND AIMS: Hummingbird flower mites feed and reproduce in flowers of host plants pollinated by hummingbirds, and use the nostrils and bill of the hummingbird to move from plant to plant. These mites compete with the pollinator for the nectar produced by flowers. An investigation was made of the relationship between the pattern of nectar production and the effects of hummingbird flower mites in the flowers of two sympatric species of Heliconia (Heliconiaceae). METHODS: Nectar production was sampled by carrying out two experiments: 2-hour intervals and accumulated nectar. Flowers with and without mites were used in both experiments. KEY RESULTS: Exclusion of mites increased nectar production, especially in accumulated daily production (a maximum of 49 % more nectar). Both Heliconia species had the same pattern of nectar production: a high concentration in the morning, which was progressively reduced as the day passed. This pattern of nectar production coincides with the behaviour of the pollinator, which makes more frequent visits in the morning, as observed in a previous study. CONCLUSIONS: The results suggest that the impact of mites on nectar availability of Heliconia is more important with regard to total volume of nectar produced irrespective of flower longevity. A high variation among individuals in nectar produced in the populations was also observed. Hummingbird flower mites strongly affect availability of nectar for hummingbirds.     

Effects of nectar theft by flower mites on hummingbird behavior and the reproductive success of their host plant, Moussonia deppeana (Gesneriaceae)

Hummingbird flower mites are transported in the nares of hummingbirds and may compete with them by "robbing" nectar secreted by the host plants. We have shown that Tropicoseius sp. flower mites consume almost half the nectar secreted by the long-lived, protandrous flowers of Moussonia deppeana (Gesneriaceae) pollinated by Lampornis amethystinus (Trochilidae). In this paper, we ask whether mimicking nectar consumption of flower mites alters some aspects of hummingbird foraging patterns, and, if so, how this affects host plant seed production. We observed hummingbirds foraging on (a) plants in which nectar was removed from the flowers and then filled with a sugar solution to half the volume of nectar simulating nectar consumption by flower mites, and (b) plants where nectar was removed and then filled with the sugar solution up to normal nectar volumes. Flower mites were excluded from both groups of plants to control for mite activity. Hummingbirds made fewer but longer visits to plants and revisited more the flowers with nectar removal than those without the treatment. We then conducted a pollination experiment on pistillate flowers using a stuffed L. amethystinus hummingbird to evaluate the effect of pollination intensity (number of bill insertions into one flower) on seed production. Flowers with more insertions produced significantly more seeds than those flowers that received fewer insertions. We conclude that the simulation of nectar consumption by hummingbird flower mites can influence the behavior of the pollinator, and this may positively affect seed production.     

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.     

Sugar Preferences in Nectar‐ and Fruit‐Eating Birds: Behavioral Patterns and Physiological Causes1

Sucrose, glucose, and fructose are the three sugars that commonly occur in floral nectar and fruit pulp. The relative proportions of these three sugars in nectar and fruit in relation to the sugar preferences of pollinators and seed dispersers have received considerable attention. Based on the research of Herbert and Irene Baker and their collaborators, a dichotomy between sucrose‐dominant hummingbird‐pollinated flowers and hexose‐dominant passerine flowers and fruits was proposed. Data on sugar preferences of several hummingbird species (which prefer sucrose) vs. a smaller sample of passerines (which prefer hexoses) neatly fitted this apparent dichotomy. This hummingbird–passerine dichotomy was strongly emphasized until the discovery of South African plants with sucrose‐dominant nectars, which are pollinated by passerines that are able to digest, and prefer sucrose. Now we know that, with the exception of two clades, most passerines are able to assimilate sucrose. Most sugar preference studies have been conducted using a single, relatively high, sugar concentration in the nectar (ca 20%). Thus, we lack information about the role that sugar concentration might play in sugar selection. Because many digestive traits are strongly affected not only by sugar composition, but also by sugar concentration, we suggest that preferences for different sugar compositions are concentration‐dependent. Indeed, recent studies on several unrelated nectar‐feeding birds have found a distinct switch from hexose preference at low concentrations to sucrose preference at higher concentrations. Finally, we present some hypotheses about the role that birds could have played in molding the sugar composition of plant rewards.     

The assembly of plants used as nectar sources by hummingbirds in a Cerrado area of Central Brazil

Studies on hummingbird–plant interactions commonly use a pollination approach emphasizing mutualistic relationships. But floral resources are often used opportunistically by these birds. Plant–pollinator assemblies and pollination sustainability will depend both on the well-adapted plants and other potential floral resources. The Cerrado, Neotropical savannas of Central Brazil, has ca. 7.5 % of its flora supposedly adapted to hummingbird pollination. But detailed information about flowers effectively used by hummingbirds at community level is still lacking. Hence, we recorded all plant species visited by hummingbirds, to determine how these nectariferous flowers were distributed in time and space in different plant formations of a Cerrado area, and also the hummingbird species that visit them. The study was conducted between March 2007 and December 2008 in the Panga Ecological Station. Data regarding flowering phenology, floral morphology and visitation were collected monthly. Forty-six nectariferous species from 39 genera and 17 families were recorded, most with annual flowering dynamics and tubular flowers. But only 21 species had a combination of traits fitting classic ornithophilous syndrome. For the remaining species hummingbird visitation was ascertained from observations at the study site or other sites in the region. Eight hummingbird species occurred in the area and were recorded visiting directly 36 plant species. The study area presented a relatively low number of ornithophilous plants, but a great habitat diversity and many non-ornithophilous plants that hummingbirds used as nectar sources. Therefore, in the studied Cerrado, the diversity of environments and nectariferous plants favour the maintenance of resident and migrant hummingbirds.     

Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbirds and bees

In order to compare the effectiveness of birds and insects as pollinators, we studied the floral biology of the bromeliad Aechmea nudicaulis (L.) Grisebach in the biome of the Atlantic rain forest, southern Brazil. On Santa Catarina Island, flowering extends from mid-September to the end of December, with diurnal anthesis. The reproductive system is obligatory xenogamy, thus pollinator-dependent. Flowers secrete 31.84 μl of nectar per day, with a mean sugar concentration of 23.2%. Highest nectar volume and sugar concentration occur at the beginning of anthesis. Most floral traits are characteristic for ornithophily, and nectar production appears to be adapted to the energy demand of hummingbirds. Continued secretion of the sucrose-dominated nectar attracts and binds visitors to inflorescences, strengthening trapline foraging behaviour. Experiments assessing seed set after single flower visits were performed with the most frequent visitors, revealing the hummingbird Thalurania glaucopis as the most effective pollen vector. In addition, bees are also functional pollinators, as substantiated by their high visitation frequency. We conclude that this pollination system is bimodal. Thus, there is redundancy in the pollination service provided by birds and bees, granting a high probability of successful reproduction in Ae. nudicaulis.     

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

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

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.     

Nectar Sugar Composition in Relation to Pollination Syndromes in Sinningieae (Gesneriaceae)

A putative correlation between nectar sugar composition andpollination syndrome was evaluated in the tribe Sinningieae(Neotropical Gesneriaceae). Sucrose, fructose and glucose werequantified in the nectar of 45 species using high performanceanion-exchange chromatography. Representative species of thehummingbird, bee, bat and moth pollination syndromes were sampledin relation to their numeric importance in the tribe. In hummingbirdand bee flowers, which represent 95% of the species in Sinningieae,nectar was sucrose-dominant (ratio [sucrose]/[hexose] > 1).Sugar ratios below one were only found in the nectar of threespecies with moth and bat syndromes. Sugar concentration averaged23.9 ± 10.6% (wt/total wt) in hummingbird flowers and28.7 ± 10.6% in bee flowers, whereas diluted nectar (7.1± 3.4%) was restricted to bat flowers. Similarities inthe nectar of hummingbird and bee flowers contrast with thepresence of specific morphological traits associated with thesetwo syndromes, indicating that plant-pollinator relationshipsrely on flower display rather than on nectar characteristics.By contrast, distinct nectar chemistry is correlated with thebat syndrome in which a particularly low sucrose productionis responsible for hexose dominance. Copyright 2001 Annals ofBotany Company Nectar sugar composition, pollination syndrome, Sinningia, Gesneriaceae, Brazil     

Efficiency of facultative frugivory in the nectar-feeding bat Glossophaga commissarisi: the quality of fruits as an alternative food source

The efficiency of food exploitation correlates positively with the extent of dietary specialization. Neotropical nectar-feeding bats (Glossophaginae) have one of the most specialized diets among mammals, as floral nectar constitutes a sugar-rich and highly digestible but protein and fiber depleted food source. However, dietary constraints, such as a temporary scarcity of nectar, or protein demands may sometimes require the uptake of alternative food items. We investigated the influence of a diet switch from nectar to fruit on intestinal morphology, body mass, and energy budget in the nectar-feeding bat Glossophaga commissarisi and quantified feeding efficiency. We hypothesized that these nectar specialists depend on a constant supply of nectar, if they were lacking the ability for morphological and physiological plasticity in response to a fiber-rich diet. Although capable of harvesting infructescences of Piper hispidum, G. commissarisi was less efficient in extracting energy from fruits (48% digestive efficiency of total fruit energy content) than from nectar (c. 99% digestive efficiency). The intestinal morphology and organ masses did not change after bats were switched from nectar to fruits. Captive bats exhibited lower daily energy expenditures and flight activity when feeding on fruits than during nectarivory. Possibly, this may have been a deliberate regulation to balance reduced feeding efficiency, or simply the consequence of extended digestive pauses. The low digestibility of Piper, in combination with slow digestion and the bats’ inability for morphological and physiological plasticity may cause nectar-feeders to reduce their maximum energy expenditure when feeding on fruits. We argue that although fruits may substitute for nectar, they may cause restricted maximum energy assimilation compared with nectar.     

Visitation rate of pollinators and nectar robbers to the flowers and inflorescences of Tabebuia aurea (Bignoniaceae): effects of floral display size and habitat fragmentation

Large floral displays favour pollinator attraction and the import and export of pollen. However, large floral displays also have negative effects, such as increased geitonogamy, pollen discounting and nectar/pollen robber attraction. The size of the floral display can be measured at different scales (e.g. the flower, inflorescence or entire plant) and variations in one of these scales may affect the behaviour of flower visitors in different ways. Moreover, the fragmentation of natural forests may affect flower visitation rates and flower visitor behaviour. In the present study, video recordings of the inflorescences of a tree species (Tabebuia aurea) from the tropical savannah of central Brazil were used to examine the effect of floral display size at the inflorescence and tree scales on the visitation rate of pollinators and nectar robbers to the inflorescence, the number of flowers approached per visit, the number of visits per flower of potential pollinators and nectar robbers, and the interaction of these variables with the degree of landscape disturbance. Nectar production was quantified with respect to flower age. Although large bees are responsible for most of the pollination, a great diversity of flower insects visit the inflorescences of T. aurea. Other bee and hummingbird species are highly active nectar robbers. Increases in inflorescence size increase the visitation rate of pollinators to inflorescences, whereas increases in the number of inflorescences on the tree decrease visitation rates to inflorescences and flowers. This effect has been strongly correlated with urban environments in which trees with the largest floral displays are observed. Pollinating bees (and nectar robbers) visit few flowers per inflorescence and concentrate visits to a fraction of available flowers, generating an overdispersed distribution of the number of visits per inflorescence and per flower. This behaviour reflects preferential visits to young flowers (including flower buds) with a greater nectar supply.     

Comparative energetics of the giant hummingbird (Patagona gigas)

Hummingbirds (family Trochilidae) represent an extreme outcome in vertebrate physiological design and are the only birds capable of sustained hovering. The giant hummingbird (Patagona gigas) is the largest trochilid, with a mass of ~20 g, and is found over an altitudinal range from 0 to 4,500 m above sea level. We report here measurements of daily, basal, and hovering rates of oxygen consumption in the giant hummingbird; compare these values with data from smaller hummingbirds; and assess overall metabolic and allometric limits to trochilid body size. The sustained metabolic scope (i.e., the ratio of daily energy expenditure to basal metabolic rate) in the giant hummingbird is higher than that in smaller hummingbirds but lies below a proposed theoretical maximum value for endotherms. Scaling exponents in the allometric relationships for different modes of energetic expenditure were comparable, suggesting that the giant hummingbird, although a clear outlier in terms of body size, does not obviously deviate from metabolic relationships derived from other trochilid taxa.     

Temporal and microclimatic partitioning of the floral resources of Justicia aurea amongst a concourse of pollen vectors and nectar robbers

Summary The flowers of Justicia aurea, morphologically characteristic of ornithophily, attracted a diverse array of foragers where they occurred as a dense stand in the tropical forests at La Selva, Costa Rica, and so provided an arena for this study of competition and coexistence. Two hummingbird species (Phaethornis superciliosus and Campylopterus hemileucurus) visited the flowers legally early in the morning, and defended the nectar resource; a third smaller bird (P. longuemareus) foraged for nectar throughout the day but collected it illegally by piercing the corollas. In addition, nectar was harvested illegally by four species of stingless bee (Trigona) and by ants, creating a further drain on the limited floral resources.Consideration of the diurnal patterns of foraging activities in combination with a spatial axis (defined here in terms of microclimate and insolation) nevertheless showed a good separation of flower visits for the different nectarivores. Hummingbirds visited flowers in zones where the reward was highest, while insects foraged to minimise their energetic costs; each of these factors could in turn be related to microclimatic considerations. A comprehensive scheme of resource utilisation could therefore be extracted from the field observations and interpreted in these terms. The limited area of niche overlap thus revealed corresponded closely with the situations where direct interference competition was observed, between hummingbird species or between bees and aggressive ants.