Hovering flight in the honeybee Apis mellifera: kinematic mechanisms for varying aerodynamic forces.

During hovering flight, animals can increase the wing velocity and therefore the net aerodynamic force per stroke by increasing wingbeat frequency, wing stroke amplitude, or both. The magnitude and orientation of aerodynamic forces are also influenced by the geometric angle of attack, timing of wing rotation, wing contact, and pattern of deviation from the primary stroke plane. Most of the kinematic data available for flying animals are average values for wing stroke amplitude and wingbeat frequency because these features are relatively easy to measure, but it is frequently suggested that the more subtle and difficult-to-measure features of wing kinematics can explain variation in force production for different flight behaviors. Here, we test this hypothesis with multicamera high-speed recording and digitization of wing kinematics of honeybees (Apis mellifera) hovering and ascending in air and hovering in a hypodense gas (heliox: 21% O2, 79% He). Bees employed low stroke amplitudes (86.7° ± 7.9°) and high wingbeat frequencies (226.8 ± 12.8 Hz) when hovering in air. When ascending in air or hovering in heliox, bees increased stroke amplitude by 30%-45%, which yielded a much higher wing tip velocity relative to that during simple hovering in air. Across the three flight conditions, there were no statistical differences in the amplitude of wing stroke deviation, minimum and stroke-averaged geometric angle of attack, maximum wing rotation velocity, or even wingbeat frequency. We employed a quasi-steady aerodynamic model to estimate the effects of wing tip velocity and geometric angle of attack on lift and drag. Lift forces were sensitive to variation in wing tip velocity, whereas drag was sensitive to both variation in wing tip velocity and angle of attack. Bees utilized kinematic patterns that did not maximize lift production but rather maintained lift-to-drag ratio. Thus, our data indicate that, at least for honeybees, the overall time course of wing angles is generally preserved and modulation of wing tip velocity is sufficient to perform a diverse set of vertical flight behaviors.

The effects of artificial wing wear on the flight capacity of the honey bee Apis mellifera.

The wings of bees and other insects accumulate permanent wear, which increases the rate of mortality and impacts foraging behavior, presumably due to effects on flight performance. In this study, we investigated how experimental wing wear affects flight performance in honey bees. Variable density gases and high-speed videography were used to determine the maximum hovering flight capacity and wing kinematics of bees from three treatment groups: no wing wear, symmetric and asymmetric wing wear. Wing wear was simulated by clipping the distal-trailing edge of one or both of the wings. Across all bees from treatment groups combined, wingbeat frequency was inversely related to wing area. During hovering in air, bees with symmetric and asymmetric wing wear responded kinematically so as to produce wingtip velocities similar to those bees with no wing wear. However, maximal hovering flight capacity (revealed during flight in hypodense gases) decreased in direct proportion to wing area and inversely to wing asymmetry. Bees with reduced wing area and high asymmetry produced lower maximum wingtip velocity than bees with intact or symmetric wings, which caused a greater impairment in maximal flight capacity. These results demonstrate that the magnitude and type of wing wear affects maximal aerodynamic power production and, likely, the control of hovering flight. Wing wear reduces aerodynamic reserve capacity and, subsequently, the capacity for flight behaviors such as load carriage, maneuverability, and evading predators.

The effects of age and behavioral development on honey bee (Apis mellifera) flight performance.

A critical but seldom-studied component of life history theory is how behavior and age affect whole-organism performance. To address this issue we compared the flight performance of honey bees (whose behavioral development and age can be assessed independently via simple manipulations of colony demographics) between distinct behavioral castes (in-hive nurse bees vs out-of-hive foragers) and across lifespan. Variable-density gases and high-speed video were used to determine the maximum hovering flight capacity and wing kinematics of age-matched nurse bees and foragers sampled from a single-cohort colony over a period of 34 days. The transition from hive work to foraging was accompanied by a 42% decrease in body mass and a proportional increase in flight capacity (defined as the minimum gas density allowing hovering flight). The lower flight capacity of hive bees was primarily due to the fact that in air they were functioning at a near-maximal wing angular velocity due to their high body masses. Foragers were lighter and when hovering in air required a much lower wing angular velocity, which they were able to increase by 32% during maximal flight performance. Flight performance of hive bees was independent of age, but in foragers the maximal wingbeat frequency and maximal average angular velocity were lowest in precocious (7-14 day old) foragers, highest in normal-aged (15-28 day old) foragers and intermediate in foragers older than 29 days. This pattern coincides with previously described age-dependent biochemical and metabolic properties of honey bee flight muscle.

Short-amplitude high-frequency wing strokes determine the aerodynamics of honeybee flight.

Most insects are thought to fly by creating a leading-edge vortex that remains attached to the wing as it translates through a stroke. In the species examined so far, stroke amplitude is large, and most of the aerodynamic force is produced halfway through a stroke when translation velocities are highest. Here we demonstrate that honeybees use an alternative strategy, hovering with relatively low stroke amplitude (approximately 90 degrees) and high wingbeat frequency (approximately 230 Hz). When measured on a dynamically scaled robot, the kinematics of honeybee wings generate prominent force peaks during the beginning, middle, and end of each stroke, indicating the importance of additional unsteady mechanisms at stroke reversal. When challenged to fly in low-density heliox, bees responded by maintaining nearly constant wingbeat frequency while increasing stroke amplitude by nearly 50%. We examined the aerodynamic consequences of this change in wing motion by using artificial kinematic patterns in which amplitude was systematically increased in 5 degrees increments. To separate the aerodynamic effects of stroke velocity from those due to amplitude, we performed this analysis under both constant frequency and constant velocity conditions. The results indicate that unsteady forces during stroke reversal make a large contribution to net upward force during hovering but play a diminished role as the animal increases stroke amplitude and flight power. We suggest that the peculiar kinematics of bees may reflect either a specialization for increasing load capacity or a physiological limitation of their flight muscles.