Hummingbird foraging and the relation between bioenergetics and behaviour

Because of their small size and expensive mode of flight, hummingbirds display some of the highest known mass-specific rates of aerobic metabolism among vertebrates. High enzymatic flux capacities through pathways of carbohydrate and long-chain fatty acid oxidation indicate that either substrate can fuel flight. Although hummingbirds are known to rely on fat to fuel migratory flight, short foraging bouts are fueled by the oxidation of carbohydrate, not fat. This allows birds refueling at meadows during migration to deposit fat at higher rates and avoids the energetic inefficiency that results from synthesizing fat from dietary sugar, and then breaking down the fat to fuel foraging flight. On cold mornings in subalpine meadows, refueling hummingbirds achieve net energy gain despite the high energetic costs of thermoregulation and flight. In doing so, they sustain the highest known time-averaged metabolic rates among vertebrates. However, low sucrose concentrations, provided in volumes large enough to allow the maintenance of energy balance at low temperature, result in energy deficit and mass loss. The problem of disposing of dietary water at low ambient temperature when intake rates are elevated suggests that the kidneys may be involved in establishing the upper limit to intake rates and, therefore, maximum sustained metabolic rates. It is suggested that hummingbird behaviour and metabolism have coevolved to maximize net energy gain. Further, the energetics of hummingbird thermoregulation and flight may have influenced the evolution of sucrose content in floral nectar.     

The power of feeder-mask respirometry as a method for examining hummingbird energetics

Many birds spend important portions of their time and energy flying. For this reason, quantification of metabolic rates during flight is of crucial importance to understanding avian energy balance. Measurement of organismal gas exchange rates using a mask enclosing the whole head or respiratory orifices has served as an important tool for studying animal energetics because it can free the rest of the body, permitting movement. Application of so-called “mask respirometry” to the study of avian forward flight energetics presents unique challenges because birds must be tethered to gas analysis equipment thus typically necessitating use of a wind tunnel. Resulting potential alterations to a study organism's behaviour, physiology, and aerodynamics have made interpretation of such studies contentious. In contrast, the study of hovering flight energetics in hummingbirds using a specialized form of mask respirometry is comparatively easy and can be done without a wind tunnel. Small size, hovering flight, and a nectarivorous diet are characteristics shared by all hummingbird species that make these birds ideally suited for this approach. Specifically, nectar feeders are modified to function as respirometry masks hummingbirds voluntarily respire into when hover-feeding. Feeder-mask based respirometry has revealed some of the highest vertebrate metabolic rates in hovering hummingbirds. In this review I discuss techniques for the successful measurement of metabolic rate using feeder-mask respirometry. I also emphasize how this technique has been used to address fundamental questions regarding avian flight energetics such as capacities for fuel use and mechanisms by which ecology, behaviour and energy balance are linked.     

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.     

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.     

Energy and water balance in the lesser double-collared sunbird (Nectarinia chalybea) feeding on different nectar concentrations

The water balance of nectarivores is tightly linked to their energy balance. When nectar is dilute, consumption of a large water excess is inevitable. We investigated energy and water balance in lesser double-collared sunbirds, Nectarinia chalybea (8 g), kept at 20 °C and fed different nectar concentrations (0.4, 0.8 M sucrose or 1.2 M sucrose). The mass of sucrose consumed, body mass, day-time mass gain and night-time mass loss were the same irrespective of diet, the birds compensating energetically for changes in sucrose concentration by drinking greater volumes of the more dilute solutions. Sunbirds consumed between 0.5 times and 1.8 times their body mass in preformed water per day, depending on sucrose concentration, and excreted around 75% of the water. The difference between water gain (preformed and metabolic water) and excreted water is assumed to equal evaporative water loss, and was similar on 1.2 M and 0.8 M sucrose, but was higher on a diet of 0.4 M sucrose. The osmolalities and K⁺ and Na⁺ concentrations of the excreted fluid were extremely low, so that sunbird urine resembled that of hummingbirds and freshwater vertebrates rather than that of typical terrestrial vertebrates. N. chalybea is able to maintain energy and water balance over a range of nectar concentrations by adjusting the volume of solution consumed and by excreting copious, dilute fluid. Accepted: 2 January 1999     

Gastrointestinal and renal responses to water intake in the green-backed firecrown (Sephanoides sephanoides), a South American hummingbird

To maintain water balance, nectar-feeding vertebrates oscillate between meeting the challenges of avoiding overhydration and preventing dehydration. To understand how green-backed firecrowns (Sephanoides sephanoides) accomplish this, we examined the response of water-handling processes in the gastrointestinal tract (GIT) and kidney to different rates of water intake during the evening, night, and morning. Fractional water absorption in the GIT was independent of water intake rate (evening: 0.91 +/- 0.08; morning: 0.88 +/- 0.04). Consistent with this nonregulated water absorption, we found linear increases in water flux, fractional turnover of body water, and the rate of renal water loading as water intake rate increased during both the evening and morning. Despite these relationships, glomerular filtration rate (GFR) was insensitive to water loading (evening: 2.08 +/- 0.56 ml/h; morning: 1.84 +/- 0.68 ml/h) and less than the allometric expectation (2.92 ml/h). During the evening, fractional renal water reabsorption decreased linearly as the rate of water intake increased. At night, a period of natural fasting for hummingbirds, mean GFR was not different from zero (0.00 +/- 0.05 ml/h). These findings indicate that green-backed firecrowns eliminate excess ingested water by decreasing water reabsorption in the kidney; to conserve water, it appears that hummingbirds arrest whole kidney GFR, effectively preventing urinary water losses. After discounting evaporative water losses, our results show that hummingbirds rely principally on their renal system to resolve the osmoregulatory quandary posed by nectarivory.     

Automated tracking of wild hummingbird mass and energetics over multiple time scales using radio frequency identification (RFID) technology

We examined the feasibility of automating the collection of hummingbird mass data facilitated by low‐cost, low‐power radio frequency identification (RFID) technology. In a field study in southern Ontario, wild hummingbirds were captured, subcutaneously implanted with passive integrated transponder (PIT) tags, and released over a three‐year period. Tagged hummingbirds were detected at specially designed feeder stations outfitted with low‐cost, low‐power RFID readers coupled with a perch secured to a digital balance. When tagged birds visited the feeder, transponder detection initiated the recording of the perched hummingbird's mass at regular intervals continuing as long as the bird remained. This permitted a nearly continuous record of mass during each visit. Mass data collected from tagged hummingbirds showed consistent trends at multiple temporal scales: the individual feeder visit, single days, and even whole seasons. These results further confirm that RFID technology is safe for use in the smallest birds. The effective detection range is a function of RFID reader power, antenna, and tag size. Yet, we find that careful arrangement of feeders and detectors allows for reliable detection even when detection range is low. When coupled with additional technologies, such as a precision electronic balance, this approach can yield robust serial measures of physiological parameters such as mass, an indicator of energy balance over time.     

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.     

Respiratory evaporative water loss during hovering and forward flight in hummingbirds

Hummingbirds represent an end point for small body size and water flux in vertebrates. We explored the role evaporative water loss (EWL) plays in management of their large water pool and its use in dissipating metabolic heat. We measured respiratory evaporative water loss (REWL) in hovering hummingbirds in the field (6 species) and over a range of speeds in a wind tunnel (1 species) using an open-circuit mask respirometry system. Hovering REWL during the active period was positively correlated with operative temperature (T_e) likely due to some combination of an increase in the vapor-pressure deficit, increase in lung ventilation rate, and reduced importance of dry heat transfer at higher T_e. In rufous hummingbirds (Selasphorus rufus; 3.3 g) REWL during forward flight at 6 and 10 m/s was less than half the value for hovering. The proportion of total dissipated heat (TDH) accounted for by REWL during hovering at T_e > 40 °C was < 40% in most species. During forward flight in S. rufus the proportion of TDH accounted for by REWL was ~ 35% less than for hovering. REWL in hummingbirds is a relatively small component of the water budget compared with other bird species (< 20%) so cutaneous evaporative water loss and dry heat transfer must contribute significantly to thermal balance in hummingbirds.     

Influence of normal daytime fat deposition on laboratory measurements of torpor use in territorial versus nonterritorial hummingbirds

Fat deposition and torpor use in hummingbirds exhibiting distinct foraging styles should vary. We predicted that dominant territorial hummingbirds will use torpor less than subordinate nonterritorial species because unrestricted access to energy by territory owners allows for fat storage. Entry into torpor was monitored using open-flow respirometry on hummingbirds allowed to accumulate fat normally during the day. Fat accumulation was measured by solvent fat extraction. Territorial blue-throated hummingbirds (Lampornis clemenciae) had the highest fat accumulation and used torpor only 17% of the time. Fat storage by L. clemenciae averaged 26% of lean dry mass (LDM) in 1995 and 18% in 1996, similar to that measured for other nonmigratory birds. Fat storage by magnificent hummingbirds (Eugenes fulgens; trapliner) and black-chinned hummingbirds (Archilochus alexandri; nectar robber) averaged 19% and 16% of LDM, respectively, and they used torpor frequently (64% and 92% of the time, respectively). All species initiated torpor if total body fat dropped below 10% of LDM, indicating the existence of a torpor threshold. The ability of L. clemenciae to store enough fat to support nighttime metabolism is likely an important benefit of territoriality. Likewise, frequent torpor use by subordinates suggests that natural restrictions to energy intake can impact their energy budget, necessitating energy conservation by use of torpor.     

Energy intake rates and nectar concentration preferences by hummingbirds

Summary In a series of daul choice tests with large volume feeders, rufous hummingbirds preferred sucrose concentrations near those that maximized their instantaneous rates of energy intake. As predicted on theoretical grounds, energy intake rates increased with increasing sucrose concentration to a maximum then decreased above this maximum. Earlier experimental studies suggested that hummingbirds always prefer the highest available concentration. Our results are consistent with the data of these studies, but by using a wider range of concentrations than previous workers, we found that the hummingbirds discriminated against very concentrated solutions.     

Are hummingbirds facultatively ammonotelic? Nitrogen excretion and requirements as a function of body size

Most birds are uricotelic. An exception to this rule may be nectar-feeding birds, which excrete significant amounts of ammonia under certain conditions. Although ammonia is toxic, because it is highly water soluble its excretion may be facilitated in animals that ingest and excrete large amounts of water. Bird-pollinated plants secrete carbohydrate- and water-rich floral nectars that contain exceedingly little protein. Thus, nectar-feeding birds are faced with the dual challenge of meeting nitrogen requirements while disposing of large amounts of water. The peculiar diet of nectar-feeding birds suggests two hypotheses: (1) these birds must have low protein requirements, and (2) when they ingest large quantities of water their primary nitrogen excretion product may be ammonia. To test these hypotheses, we measured maintenance nitrogen requirements (MNR) and total endogenous nitrogen losses (TENL) in three hummingbird species (Archilochus alexandri, Eugenes fulgens, and Lampornis clemenciae) fed on diets with varying sugar, protein, and water content. We also quantified the form in which the by-products of nitrogen metabolism were excreted. The MNR and TENL of the hummingbirds examined were exceptionally low. However, no birds excreted more than 50% of nitrogen as ammonia or more nitrogen as ammonia than urates. Furthermore, ammonia excretion was not influenced by either water or protein intake. The smallest species (A. alexandri) excreted a significantly greater proportion (>25%) of their nitrogenous wastes as ammonia than the larger hummingbirds ( approximately 4%). Our results support the hypothesis that nectar-feeding birds have low protein requirements but cast doubt on the notion that they are facultatively ammonotelic. Our data also hint at a possible size-dependent dichotomy in hummingbirds, with higher ammonia excretion in smaller species. Differences in proportionate water loads and/or postrenal modification of urine may explain this dichotomy.     

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.     

Hummingbirds have a greatly enlarged hippocampal formation

Both field and laboratory studies demonstrate that hummingbirds (Apodiformes, Trochilidae) have exceptional spatial memory. The complexity of spatial-temporal information that hummingbirds must retain and use daily is probably subserved by the hippocampal formation (HF), and therefore, hummingbirds should have a greatly expanded HF. Here, we compare the relative size of the HF in several hummingbird species with that of other birds. Our analyses reveal that the HF in hummingbirds is significantly larger, relative to telencephalic volume, than any bird examined to date. When expressed as a percentage of telencephalic volume, the hummingbird HF is two to five times larger than that of caching and non-caching songbirds, seabirds and woodpeckers. This HF expansion in hummingbirds probably underlies their ability to remember the location, distribution and nectar content of flowers, but more detailed analyses are required to determine the extent to which this arises from an expansion of HF or a decrease in size of other brain regions.     

Energy,predators and the behavior of feeding hummingbirds

Summary Current evidence suggests that many animals trade off energy gain against the risk of predation while feeding. In contrast, energetic considerations alone have proven successful in explaining and predicting the behaviour of feeding hummingbirds. This success may reflect the relative lack of natural predation on hummingbirds, but this study suggests that it may additionally reflect the lack of studies taking a predation perspective. In particular, when Anna's hummingbirds (Calypte anna) are faced with an obstructed view of their surroundings, they engage in behaviour suggestive of anti-predatory vigilance. In doing so, they voluntarily reduce their rate of energy intake. These birds also forgo better feeding opportunities that occur close to the ground, where observations suggest they are wary of opportunistic predators such as roadrunners (Geococcys californianus). While energy-based concepts will remain useful in the study of hummingbird feeding behaviour, the lack of predation on these birds should not be equated with an insensitivity to the risk of predation. This realization may lead to further insights into hummingbird-plant interactions, and hummingbird biology in general.     

Feeding: Models of Costs and Benefits in Energy Regulation

Models to predict feeding behavior at the level of consumptionand use of energy involve either details of internal (physiological)controls or economic principles of regulation based on optimal(evolutionary) foraging theory. These two approaches will ultimatelybe related, but the former requires more information for specificpredictions. The latter can provide predictions based on selectedcriteria for regulation. Meal sizes and feeding frequencies of hummingbirds are examinedrelative to two regulatory, criteria: maximizing rate of netenergy gain and maximizing efficiency (intakes/expenditures)through a "crop emptying" model that incorporates energy intakefrom food and energy expenditures for short-term (meal to meal)maintenance and longer-term (overnight) energy storage. Experimentalresults suggest that the feeding behavior of hummingbirds isdifferentially sensitive to short-term and daily uses of energy.Changes in overnight energy storage requirements result primarilyin changes in meal size, while changes in meal to meal maintenancerequirements result primarily in feeding frequency changes.The economic models predict these responses. The feeding behaviorof hummingbirds also appears to be sensitive to food quality,time spent flying to and from a food source, and costs associatedwith the weight of ingested food.     

The ability of rufous hummingbirds Selasphorus rufus to dilute and concentrate urine

Most terrestrial animals face the challenge of having to conserve water in a desiccating environment. Not surprisingly, the ability to produce concentrated urine has been relatively well studied in birds. Nectar-feeding birds are unusual among terrestrial animals in that they often ingest and excrete prodigious water volumes to obtain adequate energy. Thus, they confront the unusual challenge of having to conserve electrolytes. The diluting abilities of birds and the renal mechanisms that may correlate with them have been relatively neglected. To elucidate diluting and concentrating abilities in nectar-feeding birds, we fed rufous hummingbirds Selasphorus rufus an electrolyte-free nectar and a nectar containing a range of NaCl concentrations. Hummingbirds had a spectacular (and possibly unique) diluting ability: when fed on electrolyte-free food they produced excreta containing less than 0.5 mM l⁻¹ each of sodium and potassium. Hummingbirds also had a poor concentrating ability, retaining sodium and chloride when their food (0.632 M l⁻¹ sucrose) contained more than 35 mM l⁻¹ of NaCl. The kidneys of hummingbirds do not appear to be suited for concentrating urine, and possibly contain structural features that give them a unique diluting ability compared with those of birds that do not feed on nectar.     

Flying in the rain: hovering performance of Anna's hummingbirds under varied precipitation

Flight in rain represents a greater challenge for smaller animals because the relative effects of water loading and drop impact are greater at reduced scales given the increased ratios of surface area to mass. Nevertheless, it is well known that small volant taxa such as hummingbirds can continue foraging even in extreme precipitation. Here, we evaluated the effect of four rain intensities (i.e. zero, light, moderate and heavy) on the hovering performance of Anna's hummingbirds (Calypte anna) under laboratory conditions. Light-to-moderate rain had only a marginal effect on flight kinematics; wingbeat frequency of individuals in moderate rain was reduced by 7 per cent relative to control conditions. By contrast, birds hovering in heavy rain adopted more horizontal body and tail positions, and also increased wingbeat frequency substantially, while reducing stroke amplitude when compared with control conditions. The ratio between peak forces produced by single drops on a wing and on a solid surface suggests that feathers can absorb associated impact forces by up to approximately 50 per cent. Remarkably, hummingbirds hovered well even under heavy precipitation (i.e. 270 mm h(-1)) with no apparent loss of control, although mechanical power output assuming perfect and zero storage of elastic energy was estimated to be about 9 and 57 per cent higher, respectively, compared with normal hovering.     

Hummingbird avoidance of nectar-robbed plants: spatial location or visual cues

Broad-tailed and rufous hummingbirds avoid plants and flowers that have recently been visited by nectar-robbing bees. However, the cues the hummingbirds use to make such choices are not known. To determine the proximate cues hummingbirds use to avoid visiting nectar-robbed plants, I conducted multiple field experiments and one aviary study using the nectar-robbed, hummingbird-pollinated plant Ipomopsis aggregata . In the first field experiment, free-flying hummingbirds were presented with plants in which I manipulated nectar volume and the presence of nectar-robber holes. Hummingbirds visited significantly more plants with nectar and probed more available flowers on those plants, regardless of the presence of nectar-robber holes. Thus, I hypothesized that hummingbirds may avoid robbed plants based on their spatial memory of unrewarding plants and/or visual cues that nectar absence provides. In an aviary study, I removed spatial cues by re-randomizing the position of plants after each hummingbird-foraging bout, but hummingbirds still selected plants with nectar. Nectar may provide a visual cue in I. aggregata flowers because corollas are translucent, and nectar is visible through the side of the corolla. To determine if hummingbirds use this visual cue to avoid plants with no nectar, I masked corolla translucence in a field study by painting flowers with acrylic paint. Hummingbirds still visited significantly more plants with nectar and probed more flowers on those plants, whether or not the corollas were painted. These results suggest that hummingbirds use nectar as a proximate cue to locate and avoid non-rewarding, nectar-robbed plants, even in the absence of spatial cues and simple visual cues.     

Blood-sucking bugs as a gentle method for blood-collection in water budget studies using doubly labelled water

During doubly-labelled water (DLW) experiments, blood collection by venous puncture may traumatize animals and consequently affect the animals' behaviour and energy budget. Recent studies have shown that blood-sucking bugs (Triatominae; Heteroptera) can be used instead of conventional needles to obtain blood from animals. In this paper, we validate the bug method in captive nectar-feeding bats, Glossophaga soricina, for water budget analysis by comparing the daily water flux estimated with the DLW method with values measured by an energy balance method. As the mean daily water flux of the DLW method was not significantly deviating from the expected value, blood-sucking bugs may substitute more invasive methods of blood collection in DLW experiments. Based on the DLW estimates, daily energy and water intake rates were calculated and compared to values measured with the energy balance method. The DLW method and the energy balance method yielded on average similar results regarding the daily energy intake (DLW method: 48.8+/-14.2 kJ d(-1) versus energy balance method: 48.1+/-9.9 kJ d(-1)) and daily water intake (DLW method: 13.7+/-2.4 mL d(-1) versus energy balance method: 14.7+/-3.0 mL d(-1)). Based on the calculated water and sugar intake per day, we estimated the sugar concentration of ingested nectar to equal on average 16.2+/-2.4% (mass/mass), which fell close to the measured sugar concentration of 17% (mass/mass) bats fed on during the experiment. We conclude that it is possible to extrapolate mean daily energy and water intake for animal groups, populations and species based on DLW estimates, but due to the large variance of results (low accuracy), it seems inadequate to calculate values for single individuals.