Home Search Collections Journals About Contact us My IOPscience Hovering and intermittent flight in birds This article has been downloaded from IOPscience. Please scroll down to see the full text article. 2010 Bioinspir. Biomim. 5 045004 (http://iopscience.iop.org/1748-3190/5/4/045004) View the table of contents for this issue, or go to the journal homepage for more Download details: IP Address: 150.131.190.2 The article was downloaded on 03/02/2012 at 22:34 Please note that terms and conditions apply. IOP PUBLISHING BIOINSPIRATION &BIOMIMETICS Bioinsp. Biomim. 5 (2010) 045004 (10pp) doi:10.1088/1748-3182/5/4/045004 Hovering and intermittent flight in birds Bret W Tobalske Field Research Station at Fort Missoula, Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA E-mail: [email protected] Received 8 March 2010 Accepted for publication 28 June 2010 Published 24 November 2010 Online at stacks.iop.org/BB/5/045004 Abstract Two styles of bird locomotion, hovering and intermittent flight, have great potential to inform future development of autonomous flying vehicles. Hummingbirds are the smallest flying vertebrates, and they are the only birds that can sustain hovering. Their ability to hover is due to their small size, high wingbeat frequency, relatively large margin of mass-specific power available for flight and a suite of anatomical features that include proportionally massive major flight muscles (pectoralis and supracoracoideus) and wing anatomy that enables them to leave their wings extended yet turned over (supinated) during upstroke so that they can generate lift to support their weight. Hummingbirds generate three times more lift during downstroke compared with upstroke, with the disparity due to wing twist during upstroke. Much like insects, hummingbirds exploit unsteady mechanisms during hovering including delayed stall during wing translation that is manifest as a leading-edge vortex (LEV) on the wing and rotational circulation at the end of each half stroke. Intermittent flight is common in small- and medium-sized birds and consists of pauses during which the wings are flexed (bound) or extended (glide). Flap-bounding appears to be an energy-saving style when flying relatively fast, with the production of lift by the body and tail critical to this saving. Flap-gliding is thought to be less costly than continuous flapping during flight at most speeds. Some species are known to shift from flap-gliding at slow speeds to flap-bounding at fast speeds, but there is an upper size limit for the ability to bound (∼0.3 kg) and small birds with rounded wings do not use intermittent glides. (Some figures in this article are in colour only in the electronic version) 1. Introduction (Taeniopygia guttata) can hover for ∼30 s (Norberg 1975, Tobalske et al 1999). In the first part of this paper, I explore Although there is a growing tradition of insects being used the unique abilities, anatomy, physiology and aerodynamics as inspiration for the design of micro-air vehicles (Ellington of hummingbirds. 1999, Madangopal et al 2005, Zufferey 2008), small- and Unlike hummingbirds that tend to flap their wings medium-sized birds exhibit flight styles that will likely prove continuously, the vast majority of other small and medium useful as models for furthering the development of flying sized birds use forms of intermittent flight during which they robots. The smallest birds, hummingbirds (2–20 g in body regularly interrupt flapping phases to hold their wings either in mass), have converged with insects upon the ability to sustain a flexed-wing ‘bound’ posture during which the wings are held hovering flight (Stolpe and Zimmer 1939, Greenewalt 1962, tightly against the body or in an extended-wing ‘glide’ (Rayner Weis-Fogh 1972, Wells 1993, Tobalske et al 2007, Clark and 1985, Tobalske 2001). Mathematical models of mechanical Dudley 2009), yet they are also capable of cruising flight at power output that are based on aerodynamic theory suggest that speeds up to 12 m s−1 and migrating long distances (Tobalske these flight styles offer savings in mechanical power relative to et al 2007, Clark and Dudley 2009, Robinson et al 1996). the cost of flapping continuously (Rayner 1977, 1985, Rayner Other birds may hover for very brief intervals, presumably et al 2001, DeJong 1983, Ward-Smith 1984a, 1984b). In the using anaerobic metabolism. For example, small passerines second part of this paper, I describe how intermittent flight such as pied flycatcher (Ficdula hypoleuca) and zebra finch varies with body size, wing design and flight speed. 1748-3182/10/045004+10$30.00 1 © 2010 IOP Publishing Ltd Printed in the UK Bioinsp. Biomim. 5 (2010) 045004 B W Tobalske (A) (C) (B) (D)(E) Figure 1. Wing kinematics during hovering in the rufous hummingbird (Selasphorus rufus). (A) Dorsal view of posture at mid-downstroke and traces of the paths of wingtips (filled circles) and wrists (open circles) as obtained from 500 frames s−1 video. (B) Lateral view of posture at upstroke–downstroke transition and traces of the paths of wingtips (filled circles) and wrists (open circles) that are synchronous with paths in (A). (C) Chord angle relative to the frontal plane of the body during one wingbeat cycle. The shaded region indicates downstroke. The dashed line represents wrist elevation relative to frontal plane. Values are means ± SD for five birds. (D) Mid-upstroke wing posture showing wing supination and twist along the long axis. The mid-wing is illuminated by laser light used for particle-image velocimetry. (E) Mid-downstroke wing posture revealing different wing camber and chord angle compared with upstroke. Laser light illuminates the middle of the wing as in (D). From Warrick et al (2005) and Tobalske et al (2007). 2. Hovering Hummingbirds are unique among birds in their ability to almost fully supinate their wings during upstroke so that 2.1. Kinematics the underside of the wing faces upward (Stolpe and Zimmer 1939, Tobalske et al 2007, figures 1(C) and (D)). This reverses Wingbeat frequency scales negatively with increasing body the pronated posture typical of all birds during downstroke mass in hummingbirds, ranging from 8 Hz in the 20 g giant (figure 1(E)), but the postures are not mirror images in part hummingbird (Patagonia gigas)to80Hzinthe2gAmethyst because upstroke features greater long-axis twist of the wing. woodstar (Calliphlox amethystina, Greenewalt 1962). During ∼ ◦ ◦ Long axis rotation of the wing through the wingbeat is 140 hovering near sea level, wingbeat amplitude is ∼110 (Stolpe and occurs symmetrically with wing turnaround at the end of and Zimmer 1939, Tobalske et al 2007, figures 1(A), (B)), each half stroke. The wings are held fully extended during and hummingbirds increase their amplitude to accommodate the entire wingbeat cycle, and the wingtips trace a figure- greater power demands during load lifting or with decreased eight pattern as projected in the lateral view. Downstroke air density at higher altitude (Altshuler and Dudley 2002, features higher angular velocity and higher chord angle than 2003, Altshuler et al 2004, 2010). Although wingbeat upstroke (Tobalske et al 2007). In contrast with the wingbeat frequency does not vary significantly across flight speeds pattern in hummingbirds, when flying slowly, diverse species (Tobalske et al 2007, Clark and Dudley 2010), it does increase with pointed wings exhibit hand-wing supination (tip-reversal) during transitory load-lifting when the flight muscles are used and a partially flexed wing during upstroke and birds with anaerobically (Altshuler and Dudley 2003). rounded wings fully flex them against the body during upstroke 2 Bioinsp. Biomim. 5 (2010) 045004 B W Tobalske (Tobalske 2000). Swifts are sister taxa to the hummingbirds in the Apodiformes (Karhu 1992, Mayr 2003). Although swifts (A) 4000 also fly with extended wings, they do not accomplish wing supination, and they are severely limited in their ability to fly slowly (Warrick 1998). Vorticity (s-1) 2.2. Aerodynamics Hummingbirds appear to have converged upon the hovering style of insects (Warrick et al 2005, 2009). Hummingbirds 1 cm are the only birds that clearly demonstrate an aerodynamically -4000 active upstroke during hovering in still air (Warrick et al 2005, 2000 2009, Altshuler et al 2009). There is debate about whether the (B) tip-reversal upstroke of other bird species is aerodynamically active, but the evidence to date is equivocal (Tobalske 2000). In steady hovering in a hummingbird, downstroke supports ∼75% of the body weight and upstroke supports ∼25% (Warrick et al 2005, 2009). In addition to having an aerodynamically active upstroke, hummingbirds exploit two unsteady aerodynamic mechanisms during hovering that are considered to be the key elements of Vorticity (s-1) insect flight (Dickinson et al 1999, Lehmann 2004). These are leading-edge vortices (LEVs) and rotational circulation. During wing sweep in the middle of both downstroke and upstroke, hummingbirds exhibit LEVs on the uppermost surface of their wings (figure 2(A)). LEVs are interpreted to represent delayed stall at high angles of attack, and they enhance coefficients of lift and drag during wing sweep relative to coefficients during linear translation at the same angles of attack (Lehmann 2004). The LEV contributes ∼16% to -2000 the total bound circulation of the hummingbird wing, and Figure 2. Velocity (vectors) and vorticity fields (background) measurable LEVs are not always present. In contrast, LEVs illustrating near-field flow and bound circulation on the wing of a dominate fruit-fly (Drosophila melanogaster) aerodynamics rufous hummingbird (Selasphorus rufus) during hovering. (A) LEV is apparent on the upper surface of the wing at mid-downstroke. The (Birch et al 2004) and contribute up to 40% of the circulation dashed line indicates the outline of the bird’s body. The dark area on the wing in slow-flying, nectar-feeding bats that are among behind the bird is a shadow due to the wing interrupting the laser the smallest extant species of bats (Muijres et al 2008).