© 2015. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2015) 218, 3520-3527 doi:10.1242/jeb.126458 RESEARCH ARTICLE Aeroelastic flutter of feathers, flight and the evolution of non-vocal communication in birds Christopher J. Clark*,‡ and Richard O. Prum ABSTRACT the evolutionary modification of behavior or morphology (e.g. Tonal, non-vocal sounds are widespread in both ordinary bird flight feather shape) must produce variation in acoustic qualities that may and communication displays. We hypothesized these sounds are then be the target of selection for communication. Here, we focus on attributable to an aerodynamic mechanism intrinsic to flight feathers: one mechanism by which feathers produce sound, aeroelastic aeroelastic flutter. Individual wing and tail feathers from 35 taxa (from flutter, previously demonstrated for hummingbirds (Clark et al., 13 families) that produce tonal flight sounds were tested in a wind 2013a,b, 2011) and snipe (Reddig, 1978). We present data tunnel. In the wind tunnel, all of these feathers could flutter and suggesting that aeroelastic flutter and the ensuing flutter-induced generate tonal sound, suggesting that the capacity to flutter is intrinsic sounds satisfy both of the aforementioned requirements. to flight feathers. This result implies that the aerodynamic mechanism Ordinary flight produces locomotion-induced sounds by several of aeroelastic flutter is potentially widespread in flight of birds. poorly described mechanisms, which can be distinguished in part by However, the sounds these feathers produced in the wind tunnel their acoustic properties. Four such mechanism categories are as replicated the actual flight sounds of only 15 of the 35 taxa. Of the 20 follows. (1) Whooshing sounds produced by turbulent airflow shed negative results, we hypothesize that 10 are false negatives, as the with each wingbeat (Blake, 1986; Sarradj et al., 2011). Whooshes acoustic form of the flight sound suggests flutter is a likely acoustic tend to be quiet and atonal, with most acoustic energy <1 kHz mechanism. For the 10 other taxa, we propose our negative wind (Sarradj et al., 2011), but they can be loud in fast flight, such as a tunnel results are correct, and these species do not make sounds via falcon (Falco sp.) chasing prey at high speed (e.g. falcon chasing a flutter. These sounds appear to constitute one or more mechanism(s) dove in Audio 1; band-tailed pigeon flock in Audio 2). (2) Rustling we call ‘wing whirring’, the physical acoustics of which remain sounds, which are atonal, complex, time varying, and contain sound unknown. Our results document that the production of non-vocal energy at higher frequencies. Their physical acoustic mechanism is communication sounds by aeroelastic flutter of flight feathers is unclear, possibly slip and stick friction (Patek, 2001), because widespread in birds. Across all birds, most evolutionary origins of feathers slide over each other as the flight feathers flex and wing- and tail-generated communication sounds are attributable to reposition during the wingbeat. Such sounds seem common in the three mechanisms: flutter, percussion and wing whirring. Other flight of some birds, such as in gallinaceous birds. (3) Snaps and mechanisms of sound production, such as turbulence-induced claps, which are percussive sounds caused by forced airflow and whooshes, have evolved into communication sounds only rarely, collisions between the wings and another body part (e.g. black- despite their intrinsic ubiquity in ordinary flight. tailed trainbearer in Audio 3; booted racket-tail in Audio 4; and wire-crested thorntail in Audio 5). They are short, broad frequency KEY WORDS: Locomotion, Pennaceous feather, Sonation, Sound, and impulsive (Bostwick and Prum, 2003). Claps regularly occur in Wing whirring ordinary flight, such as the clapping sounds rock doves (Columba livia) occasionally produce during takeoff. (4) Tonal flight sounds, INTRODUCTION which are generated during ordinary flight of birds such as hornbills Darwin (1871) observed that birds such as snipe, hummingbirds or and ducks (e.g. black-and-white-casqued hornbill in Audio 6; black manakins make extensive use of non-vocal ‘instrumental music’ vulture in Audio 7; and eared dove in Audio 8). This final category during courtship. To explain how such sounds arise, he suggested: includes the sounds that are the focus of this study: tonality implies a ‘…birds during their courtship flutter, shake, or rattle their stable, oscillatory source. It is out of passive mechanisms such as unmodified feathers together; and if the females were led to select these that communication sounds may arise. the best performers, the males which possessed the strongest or During aerial displays, some hummingbirds produce thickest, or most attenuated feathers… would be the most communication sounds by aeroelastic flutter of their wing and tail successful’ (p. 67). In other words, incidental non-vocal sounds feathers (Clark et al., 2013a,b, 2011). Aeroelastic flutter (hereafter, that accompany motions may become salient to receivers and evolve flutter) results from dynamic coupling of aerodynamic forces with into communication signals (Bostwick and Prum, 2003, 2005; the geometry and stiffness of a wing or tail feather, to produce a limit Prum, 1998). For this to occur, first, a mechanism of sound cycle vibration (i.e. a stable oscillation) of a portion of a feather. In production must be a passive byproduct of locomotion and, second, essence, at a particular orientation, when air velocity over the feather exceeds a threshold (U*), a feather becomes an aerodynamically driven oscillator. Flutter of hummingbird feathers usually produces Department of Ecology & Evolutionary Biology, and Peabody Museum of Natural History, Yale University, New Haven, CT 06511, USA. tonal sound with strong harmonics (Clark et al., 2013a,b, 2011; *Present address: Department of Biology, University of California, Riverside, Clark and Feo, 2008, 2010). We hypothesized that the capacity to CA 92521, USA. flutter is intrinsic to all pennaceous flight feathers in the right ‡ ’ Author for correspondence ([email protected]) airflow. If so, congruent with Darwin s (1871) hypothesis, flutter- induced acoustic signals may readily evolve out of initially Received 9 June 2015; Accepted 3 September 2015 involuntary, incidental byproducts of avian flight mechanics. Journal of Experimental Biology 3520 RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3520-3527 doi:10.1242/jeb.126458 To test this hypothesis, we gathered reports in the literature of et al. (2013b) and is repeated here briefly. The feathers were mounted by sounds produced with the wings or tail, to assess the diversity of inserting an insect pin (small feathers) or dissecting pin (large feathers) into flight sounds. Then, we surveyed sound collections including the the calamus and anchored with a small amount of cyanoacrylate glue. The other end of this pin was then inserted into a pin vise, which projected Macaulay Library, Xeno-Canto and the British Library of Wildlife ’ Sounds for recordings of non-vocal avian sounds. We used acoustic vertically on a sting down into the freestream of the tunnel, with the feather s long axis perpendicular to flow, as in fig. 2 of Clark et al. (2013b). Because of characters in these sounds to develop hypotheses of their physical the floor and ceiling boundary layers (Clark et al., 2013b), there was only origin. To test the flutter hypothesis in particular, we measured the approximately 20 cm of usable space within the working section. For feathers capacity of individual feathers to flutter and produce tonal sounds in longer than 20 cm (from ducks and common raven), either the feather shaft a wind tunnel. Our sample included feathers with modified shapes was cut and only the distal portion was tested, or the sting was retracted into hypothesized to have evolved to produce display sounds, such as tail the roof of the tunnel so that the distal portion of the feather projected out of feathers of an adult male lyre-tailed honeyguide (Melichneutes the boundary layer into the freestream. Orientation of the feather could be robustus; Friedmann, 1955), and feathers lacking any obvious varied by bending the pin, or by rotating the sting. modifications for sound production, from taxa that produce tonal To measure a feather, the wind tunnel was initially set to a speed slightly −1 sound during ordinary flight, such as ducks. above the presumed flight speed of the bird from which it came (12 m s −1 ’ Previous results on hummingbird feathers suggested that all for small passerines, up to 25 m s for ducks). The feather s orientation was then adjusted to find modes of flutter, and airspeed was increased, as individual, isolated feathers can flutter under the right aerodynamic needed. If a mode of flutter was found that was similar to the flight sound of conditions (Clark et al., 2013b). Many of the inducible modes of the bird from which the feather came, we then collected data at constant flutter do not correspond to sounds produced by birds in flight and orientation, over a range of airspeeds, as in Clark et al. (2013b). If after are thus spurious (Clark et al., 2013a). Therefore, the ability to testing 5–10 orientations/airspeeds, no matching mode of flutter was found, flutter in a wind tunnel does not indicate that a feather actually we returned to conditions that elicited the mode of flutter that produced the flutters during natural behavior of the bird. We developed four loudest sound and/or was the most stable over varying airspeeds, and criteria for whether a mode of flutter induced in the wind tunnel was obtained measurements over a range of speeds, at a constant orientation. a match to the flight sound. (1) The motion was a limit cycle We recorded the feather’s sounds with a microphone positioned close to oscillation (i.e. stable and periodic, not chaotic), with a frequency the feather (often <10 cm), though not in the aerodynamic wake, with all of within 25% of the fundamental frequency, 2nd or 3rd harmonic of the same methodological caveats described in Clark et al.