Donald R. Powers

Aerodynamics of the Hovering Hummingbird

Despite profound musculoskeletal differences, hummingbirds (Trochilidae) are widely thought to employ aerodynamic mechanisms similar to those used by insects. The kinematic symmetry of the hummingbird upstroke and downstroke has led to the assumption that these halves of the wingbeat cycle contribute equally to weight support during hovering, as exhibited by insects of similar size. This assumption has been applied, either explicitly or implicitly, in widely used aerodynamic models and in a variety of empirical tests. Here we provide measurements of the wake of hovering rufous hummingbirds (Selasphorus rufus) obtained with digital particle image velocimetry that show force asymmetry: hummingbirds produce 75% of their weight support during the downstroke and only 25% during the upstroke. Some of this asymmetry is probably due to inversion of their cambered wings during upstroke. The wake of hummingbird wings also reveals evidence of leading-edge vortices created during the downstroke, indicating that they may operate at Reynolds numbers sufficiently low to exploit a key mechanism typical of insect hovering. Hummingbird hovering approaches that of insects, yet remains distinct because of effects resulting from an inherently dissimilar—avian—body plan.

Lift production in the hovering hummingbird

Aerodynamic theory and empirical observations of animals flying at similar Reynolds numbers (Re) predict that airflow over hummingbird wings will be dominated by a stable, attached leading edge vortex (LEV). In insects exhibiting similar kinematics, when the translational movement of the wing ceases (as at the end of the downstroke), the LEV is shed and lift production decreases until the energy of the LEV is re-captured in the subsequent half-cycle translation. We here show that while the hummingbird wing is strongly influenced by similar sharp-leading-edge aerodynamics, leading edge vorticity is inconsistent, varying from 0.7 to 26 per cent (mean 16%) of total lift production, is always generated within 3 mm of the dorsal surface of the wing, showing no retrograde (trailing to leading edge) flow, and does not increase from proximal to distal wing as would be expected with a conical vortex (class III LEV) described for hawkmoths. Further, the bound circulation is not shed as a vortex at the end of translation, but instead remains attached and persists after translation has ceased, augmented by the rotation (pronation, supination) of the wing that occurs between the wing-translation half-cycles. The result is a near-continuous lift production through wing turn-around, previously unknown in vertebrates, able to contribute to weight support as well as stability and control during hovering. Selection for a planform suited to creating this unique flow and nearly-uninterrupted lift production throughout the wingbeat cycle may help explain the relatively narrow hummingbird wing.

Field Metabolic Rate and Food Consumption by Free-Living Anna's Hummingbirds (Calypte Anna)

We measured CO2 production and water flux using doubly labeled water in wild Annas hummingbirds living in the Santa Ana Mountains of Southern California during autumn (September) of 1981. The estimated field metabolic rate (FMR) of a hummingbird maintaining a constant body mass (mean 4.48 g) is about 32 kJ/day, which is 5.2 times basal metabolic rate (BMR). Metabolic rates during daylight hours were about 6.8 × BMR, less than one-half that expected for an Annas hummingbird in continuous hovering flight. We estimated nighttime metabolism to be near 2.1 × BMR, which is about what would be expected for a normothermic, resting bird experiencing cool air temperatures (as low as 15 C) but much higher than expected if torpor were employed. Water influx was about 164% of body mass per day in birds maintaining a constant mass. Most of this water intake was in the form of sucrose solution from feeders in the area, but some probably came from insects eaten by the birds. Hummingbirds probably did not drink liquid water from streams or ponds during the measurement period.

Take-off mechanics in hummingbirds (Trochilidae).

SUMMARY Initiating flight is challenging, and considerable effort has focused on understanding the energetics and aerodynamics of take-off for both machines and animals. For animal flight, the available evidence suggests that birds maximize their initial flight velocity using leg thrust rather than wing flapping. The smallest birds, hummingbirds (Order Apodiformes), are unique in their ability to perform sustained hovering but have proportionally small hindlimbs that could hinder generation of high leg thrust. Understanding the take-off flight of hummingbirds can provide novel insight into the take-off mechanics that will be required for micro-air vehicles. During take-off by hummingbirds, we measured hindlimb forces on a perch mounted with strain gauges and filmed wingbeat kinematics with high-speed video. Whereas other birds obtain 80–90% of their initial flight velocity using leg thrust, the leg contribution in hummingbirds was 59% during autonomous take-off. Unlike other species, hummingbirds beat their wings several times as they thrust using their hindlimbs. In a phylogenetic context, our results show that reduced body and hindlimb size in hummingbirds limits their peak acceleration during leg thrust and, ultimately, their take-off velocity. Previously, the influence of motivational state on take-off flight performance has not been investigated for any one organism. We studied the full range of motivational states by testing performance as the birds took off: (1) to initiate flight autonomously, (2) to escape a startling stimulus or (3) to aggressively chase a conspecific away from a feeder. Motivation affected performance. Escape and aggressive take-off featured decreased hindlimb contribution (46% and 47%, respectively) and increased flight velocity. When escaping, hummingbirds foreshortened their body movement prior to onset of leg thrust and began beating their wings earlier and at higher frequency. Thus, hummingbirds are capable of modulating their leg and wingbeat kinetics to increase take-off velocity.

BLUE-THROATED HUMMINGBIRD SONG: A PINNACLE OF NONOSCINE VOCALIZATIONS

Abstract Little is known about the structure and function of hummingbird vocalizations. We studied the vocalizations of Blue-throated Hummingbirds (Lampornis clemenciae) at two sites in southeastern Arizona. Songs were produced by males and females. Male songs consisted of arrays of notes organized in clusters of “song units.” Within sites, all males shared the same song units. Individual differences occurred in some temporal aspects of song, and slight but consistent differences in note structure occurred between the two sites. The organization of units within songs was marked by rigid syntax, and long songs were produced by agglutination of units. Male songs may function in territorial advertisement and mate attraction. Female songs were very different acoustically from those of males and typically were given when females were within a few centimeters of a male. In these situations, the females song often overlapped temporally with the males song. Of the hummingbird species studied so far, the Blue-throated Hummingbird has the most complex songs and is the only known species with complex female songs. Blue-throated Hummingbirds show convergence with oscines in vocal complexity, song organization, song function, and possible learning of some song elements.

Effects of flight speed upon muscle activity in hummingbirds

SUMMARY Hummingbirds have the smallest body size and highest wingbeat frequencies of all flying vertebrates, so they represent one endpoint for evaluating the effects of body size on sustained muscle function and flight performance. Other bird species vary neuromuscular recruitment and contractile behavior to accomplish flight over a wide range of speeds, typically exhibiting a U-shaped curve with maxima at the slowest and fastest flight speeds. To test whether the high wingbeat frequencies and aerodynamically active upstroke of hummingbirds lead to different patterns, we flew rufous hummingbirds (Selasphorus rufus, 3 g body mass, 42 Hz wingbeat frequency) in a variable-speed wind tunnel (0–10 m s−1). We measured neuromuscular activity in the pectoralis (PECT) and supracoracoideus (SUPRA) muscles using electromyography (EMG, N=4 birds), and we measured changes in PECT length using sonomicrometry (N=1). Differing markedly from the pattern in other birds, PECT deactivation occurred before the start of downstroke and the SUPRA was deactivated before the start of upstroke. The relative amplitude of EMG signal in the PECT and SUPRA varied according to a U-shaped curve with flight speed; additionally, the onset of SUPRA activity became relatively later in the wingbeat at intermediate flight speeds (4 and 6 m s−1). Variation in the relative amplitude of EMG was comparable with that observed in other birds but the timing of muscle activity was different. These data indicate the high wingbeat frequency of hummingbirds limits the time available for flight muscle relaxation before the next half stroke of a wingbeat. Unlike in a previous study that reported single-twitch EMG signals in the PECT of hovering hummingbirds, across all flight speeds we observed 2.9±0.8 spikes per contraction in the PECT and 3.8±0.8 spikes per contraction in the SUPRA. Muscle strain in the PECT was 10.8±0.5%, the lowest reported for a flying bird, and average strain rate was 7.4±0.2 muscle lengths s−1. Among species of birds, PECT strain scales proportional to body mass to the 0.2 power (∞Mb0.2) using species data and ∞Mb0.3 using independent contrasts. This positive scaling is probably a physiological response to an adverse scaling of mass-specific power available for flight.

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 (≈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.

Size dependence in non-sperm ejaculate production is reflected in daily energy expenditure and resting metabolic rate

ABSTRACT The non-sperm components of an ejaculate, such as copulatory plugs, can be essential to male reproductive success. But the costs of these ejaculate components are often considered trivial. In polyandrous species, males are predicted to increase energy allocation to the production of non-sperm components, but this allocation is often condition dependent and the energetic costs of their production have never been quantified. Red-sided garter snakes (Thamnophis sirtalis parietalis) are an excellent model with which to quantify the energetic costs of non-sperm components of the ejaculate as they exhibit a dissociated reproductive pattern in which sperm production is temporally disjunct from copulatory plug production, mating and plug deposition. We estimated the daily energy expenditure and resting metabolic rate of males after courtship and mating, and used bomb calorimetry to estimate the energy content of copulatory plugs. We found that both daily energy expenditure and resting metabolic rate were significantly higher in small mating males than in courting males, and a single copulatory plug without sperm constitutes 5–18% of daily energy expenditure. To our knowledge, this is the first study to quantify the energetic expense of size-dependent ejaculate strategies in any species. Highlighted Article: The daily energy expenditure and resting metabolic rate of red-sided garter snakes are significantly higher in small mating males than in courting males, and a single copulatory plug without sperm constitutes 5–18% of daily energy expenditure.

Citizen‐science data provides new insight into annual and seasonal variation in migration patterns

Current rates of global environmental and climate change pose potential challenges for migratory species that must cope with or adapt to new conditions and different rates of change across broad spatial scales throughout their annual life cycle. North American migratory hummingbirds may be especially sensitive to changes in environment and climate due to their extremely small body size, high metabolic rates, and dependence on nectar as a main resource. We used occurrence information from the eBird citizen-science database to track migratory movements of five North American hummingbird species (Archilochus alexandri, A. colubris, Selasphorus calliope, S. platycercus, and S. rufus) across 6 years (2008–2013) at a daily temporal resolution to describe annual and seasonal variation in migration patterns. Our findings suggest that the timing of the onset of spring migration generally varies less than the arrival on the wintering grounds. Species follow similar routes across years, but exhibit more variation in...

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.