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

Victor Manuel Ortega-Jimenez 1 Robert Dudley 0 1 0 Smithsonian Tropical Research Institute , PO Box 2072, Balboa , Republic of Panama 1 Department of Integrative Biology, University of California , Berkeley, CA 94720 , USA 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 h21) 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. 1. INTRODUCTION Rainfall is a conspicuous environmental phenomenon that can potentially influence animal flight performance. Adhered water increases the effective mass of the wings and body and alters the wings moment of inertia, whereas drop impact imparts downward momentum to the body and elevates the power required to stay airborne [1,2]. Raindrops impacting wings can also produce superficial roughness and, depending on hydrophilic surface characteristics, can increase aerodynamic drag [3]. Moreover, non-uniform distribution of drops across the body and wings may adversely influence control and manoeuverability. Potential damage to wing microstructures caused by high impact pressures of falling drops, as observed for airfoils [4], might also be expected. Surprisingly, some birds [5], bats [6] and insects [7] have been observed flying even during heavy rain, although the various aforementioned mechanical penalties while doing so have not yet been characterized. Theoretical and experimental research on airfoils indicates dramatic reduction in the aerodynamic efficiency (i.e. in the lift : drag ratio) as precipitation rate increases above middle-range values [1 3]. For medium-size bats, moderate rain has only a marginal effect on flight performance, although associated fur wetting increases their flight metabolism by a factor of 2 [6]. In contrast to mammalian fur, the microstructural configuration of feathers confers both water repellency as well as resistance to water penetration [8,9]. Thus, we hypothesize that birds face primarily aerodynamic rather than thermoregulatory challenges owing to wetting when they fly in the rain. Hummingbirds are of special interest in this regard because they approach lower size limits of volant vertebrates [10], possess distinctive hovering abilities similar to those of insects [11,12] and remain active even during heavy rain ([5], V.M.O. & R.D. 2011, personal observation). The more than 325 trochilid species are also most abundant in mid-montane cloud forest regions of the Neotropics as well as in lowland rainforest where heavy rains are common. Persistent inclement weather is particularly characteristic of eastern Andean slopes, a well-known hotspot of hummingbird diversity. We accordingly evaluated the effects of light, moderate and heavy precipitation, as simulated in the laboratory, on the hovering flight of Annas hummingbirds (Calypte anna). Furthermore, we explored the consequences of raindrop impact forces and total mass of water adhered to the body and wings for estimates of mechanical power produced during flight. 2. MATERIAL AND METHODS Hover-feeding of five male Annas hummingbirds was studied under three precipitation rates (light: 6.4 + 0.01 mm h21; moderate: 14.9 + 0.56 mm h21; and heavy: 22.4 + 0.26 mm h21) and under control conditions of no rain. Birds were placed individually in a Plexiglas cube (0.6 0.6 0.6 m) that contained a perch and a feeder. Two nozzles were connected via metal tubing to the cold water tap of the laboratory sink; a water gauge (with accuracy of 7 kPa) was used to control water pressure. One nozzle (Viper flexible Downloaded from http://rspb.royalsocietypublishing.org/ on November 13, 2014 Hummingbirds flying in the rain V. M. Ortega-Jimenez and R. Dudley Table 1. Physical characteristics for three different conditions of experimentally generated precipitation. Data are shown as mean + s.e. (sample size n). intensity, Hw (mm 5 min21) drop diameter, ddrop (mm) drop speed, Udrop (m s21) drops per second, ndrops a Fsd (mN)b energy flux, Ek ( J m22 h21)c Weber number, Wed mist stand) was placed in the centre of the cubes ceiling 35 cm above the feeder, and was used to produce light and moderate rain (at water pressures of 70 and 210 kPa, respectively). The other nozzle (obtained from a garden water-gun) was oriented upwards on the bottom of one of the cube walls such that emitted water drops followed a ballistic path and fell almost vertically near the feeder. A plastic square mesh (with openings of 15 15 mm) was placed vertically in front of this latter nozzle to reduce volume flow and to increase size variability of drops. This nozzle was used to produce heavy rain at a water pressure of 112 kPa. To estimate flow rates for different rain conditions, a calibrated glass cylinder (external diameter dcyl of 1.82 cm) was used to measure the height of accumulated water (Hw) as measured over 5 min. Mean values for drop diameter (ddrop) and drop speed (Udrop) were obtained from high-speed video recordings at 1000 Hz; only those drops in focus in the approximate centre of the rain field (corresponding to the typical position of a feeding hummingbird) were analysed (see electronic supplementary material, video SA1). Drop mass (md) was calculated as rwp(ddrop)3/6, where rw is the water density (assumed to be 1 103 kg m23). Physical parameters for each of the three precipitation conditions are provided in table 1. Lateral video recordings were also obtained (at 1000 frames per second) of water drops (n 5) falling from a 35 cm height and impacting on an isolated hummingbird wing (obtained from a salvage specimen of a male Annas hummingbird) that was positioned horizontally with its planform area nominally perpendicular to gravity. The contact times (ti) were measured from the videos (see electroni (...truncated)