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Integrative and Comparative Biology Integrative and Comparative Biology, Volume 60, Number 5, Pp Integrative and Comparative Biology Integrative and Comparative Biology, volume 60, number 5, pp. 1160–1172 doi:10.1093/icb/icaa051 Society for Integrative and Comparative Biology SYMPOSIUM ARTICLE Specialized Feathers Produce Sonations During Flight in Columbina Downloaded from https://academic.oup.com/icb/article/60/5/1160/5849933 by University of California, Riverside user on 23 November 2020 Ground Doves Robert L. Niese,1,* Christopher J. Clark ,† and Bret W. Tobalske* *Field Research Station at Fort Missoula, Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA; †Department of Evolution, Ecology, and Organismal Biology, University of California Riverside, CA 92521, USA From the symposium “Bio-inspiration of Quiet Flight of Owls and Other Flying Animals: Recent Advances and Unanswered Questions” presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2020 at Austin, Texas 1E-mail: [email protected] Synopsis The shape of remiges (primary and secondary feathers) is constrained and stereotyped by the demands of flight, but members of the subfamily of New World ground doves (Peristerinae) possess many atypical remex shapes with which they produce sonations of alarm. Within the genus Columbina specifically, the seventh primary feathers (P7) have elongated barbs that create a protrusion on the trailing vane which varies in size and shape between species. These feathers are hypothesized to have been coopted to produce communicative sounds (i.e., sonations) during flight, but the mechanism of this sound production is unknown. We tested the sound-producing capabilities of spread wing specimens from three species of ground doves (C. inca, C. passerina, and C. talpacoti) in a wind tunnel. High speed video and audio analyses indicated that all wings of adult birds produced buzzing sounds in the orientation and flow velocity of mid- upstroke. These buzzing sounds were produced as the protrusion of elongated barbs fluttered and collided with adjacent P6 feathers at a fundamental frequency of 200 and 400 Hz, respectively. Wings from juvenile C. inca produced signif- icantly quieter buzzes and most (three of four individuals) lacked the elongated barbs that are present in adults. Buzzing sounds produced in the wind tunnel were similar to those produced by wild birds indicating that these P7 feathers have been coopted to produce acoustic signals (sonations) during flight. The shape and mechanism of sound production described here in Columbina appear to be unique among birds. Introduction wing in volant species, are constrained to be mor- Feathers are the most phenotypically diverse (Prum phologically stereotyped by the physical demands of and Brush 2002; Stoddard and Prum 2011) and flight (e.g., Ennos et al. 1995; Swaddle et al. 1996; structurally complex (Prum and Williamson 2001; Bachmann et al. 2012). Even minor deviations in this Feo et al. 2015) integumentary structures in verte- stereotyped remex shape can reduce aerodynamic brates. They vary in size, shape, color, structure, and force production (Niese and Tobalske 2016). chemical composition between species, between loca- Therefore, remiges that diverge from aerodynami- tions on the body, and within a single feather follicle cally stereotyped forms may be an evidence of func- across an individual’s lifetime (Lucas and tional specializations other than flight. Stettenheim 1972). But not all feathers vary to the Remiges deviate from aerodynamically stereotyped same degree across species. Primary and secondary shapes in three ways: as sexually selected visual sig- feathers (collectively, the remiges), for example, are nals, as specialized sonation-producing structures, morphologically conserved and show comparatively and as specialized aerodynamic devices. Remex shape little variation across disparate taxa, individual life- has been modified to function in sexually selected spans, and evolutionary time (Prum and Brush 2002; visual signals in only three species—the Great Heers and Dial 2012; Feo et al. 2015). The remiges, Argus (Argusianus argus, Phasianidae) and two spe- which make up the majority of the surface area of a cies of nightjars (Caprimulgus longipennis and C. Advance Access publication June 1, 2020 ß The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. Sonations during flight in Columbina 1161 vexillarius, Caprimuligidae). Conversely, selection on nearly a third (101 species) of all Columbids possess the remiges to produce non-vocal acoustic signals, or some form of highly modified remex (Goodwin sonations, is common (Clark and Prum 2015)and 1983; Mahler and Tubaro 2001; Gibbs et al. 2001; has resulted in diverse, specialized morphologies Niese 2019). These modified remiges are not sexually such as those in the Club-winged Manakin dimorphic (implying they serve the same function in (Machaeropteris deliciosus, Pipridae; Bostwick et al. both sexes), and sexually selected sonations involving 2010), Crested Pigeon (Ocyphaps lophotes; Murray modified remiges have not been identified among Downloaded from https://academic.oup.com/icb/article/60/5/1160/5849933 by University of California, Riverside user on 23 November 2020 et al. 2017), American Woodcock (Scolopax minor, pigeons and doves (Goodwin 1983; Gibbs et al. Scolopacidae; Clark and Prum 2015), Scissor-tailed 2001; Niese 2019). While naturalists have speculated Flycatcher (Tyrannus forficatus, Tyrannidae; Clark on the function of these modified feathers for cen- and Prum 2015; Gomez et al. this ICB issue), and turies (Cuvier 1829; Swainson 1825; Selby 1850), to others. Most sonations produced by remiges are date, acoustic function has only been tested in one part of sexually selected displays and their associated species, the Crested Pigeon (O. lophotes; Murray morphologies are often sexually dimorphic (Clark and et al. 2017). In this species, individuals possess a Prum 2015; Clark 2018), but remiges can also be spe- modified interior remex (P8) which flutters to pro- cialized for a naturally-selected sonation (alarm sig- duce tonal sounds on the downstroke and possibly nals) that is performed by both sexes (e.g., Murray on the upstroke. These sounds vary intrinsically with et al. 2017). Lastly, it has been hypothesized wingbeat frequency and are therefore reliable indica- (Goodwin 1983; Mahler and Tubaro 2001)thatremex tors of the speed of take-off and thus function as morphology may become dramatically modified as a alarm signals in this species (Murray et al. 2017). specialized aerodynamic device with functions akin to New World ground doves (Peristerinae; Pereira slotted primaries (KleinHeerenbrink et al. 2017)or et al. 2007; Sweet et al. 2017) possess several unique the alula (Lee et al. 2015). remex morphologies (Fig. 1), and species in the clade Remiges that are specialized to produce sonations can have one, two, three, or even four modified often do so via aeroelastic flutter (47% of wing/tail feathers of different shapes (Johnston 1961; sounds identified by Clark and Prum (2015)), a phe- Goodwin 1983). In some species (Claravis pretiosa, nomenon common to all light, stiff airfoils (Clark Claravis mondetoura, Claravis geoffroyi, and et al. 2013a, 2013b). Airflow excites resonance fre- Columbina cyanopis), modified outermost remiges quencies within a damped airfoil which, when a crit- (P10) are thought to be specialized aerodynamic ical velocity is exceeded, energy input from the airflow devices (Goodwin 1983; Niese 2019). The largest ge- exceeds the structural damping of the feather, causing nus in this clade, Columbina, has eight members it to enter stable oscillations (Clark et al. 2013a). which possess several forms of a modified P7 feather, These aeroelastic oscillations can produce tones (for and, in some species, an additional modified P6 more details, see Clark et al. 2013b). In addition to (Johnston 1960, 1961; Gibbs et al. 2001). In mem- aeroelastic flutter tones, wing sounds produced during bers of this genus, these more proximal modified flight can occur as atonal sounds produced as turbu- feathers (i.e., interior remiges) have been hypothe- lence is formed and shed into the wake (“wooshes”; sized to produce sonations (Johnston 1960, 1961). Clark and Prum 2015), as feathers reposition and Most members of the Peristerinae are well-known move during each wingbeat, generating frictional for their wing sounds, some of which were described noise (“rustles”; Matloff et al. 2020), or as flutter well before the species’ vocalizations (e.g., Areta and induces collisions between adjacent feathers (“buzzes” Monteleone 2011). Columbina doves specifically pro- here; Clark and Prum 2015). In all cases, these wing duce a unique buzzing sound during flight sounds can be produced incidentally as a byproduct (Supplementary Audio 1). The physical mechanism of locomotion; therefore, their presence alone is not that produces this sound and its function (if any) is sufficient evidence to conclude that they are sonations unknown, but the presence of modified primary (i.e., a signal), rather than a cue (Clark and Prum feathers in the clade has led some to suggest that 2015; Clark 2018). Rather, the presence of a highly the two are linked (Johnston 1960, 1961). Here, we modified morphology in which the shape clearly func- describe the modified remex morphologies present in tions to produce the
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