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 significantly 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 wing sounds is evidence that the this clade, and test these modified feathers in feather(s) evolved specifically to produce the sound Columbina ground doves to determine their ability and hence that the sounds are sonations (Clark 2018). to produce such buzzing wing sounds. Using dried, Modified remex morphologies in pigeons and spread-wing specimens from the University of doves (Columbidae) produce naturally-selected sona- Washington’s Burke Museum, we recorded the tions in some species (Murray et al. 2017), but acoustic and kinematic behavior of feathers as they 1162 R. L. Niese et al. Downloaded from https://academic.oup.com/icb/article/60/5/1160/5849933 by University of California, Riverside user on 23 November 2020

Fig. 1 Remex morphologies in three species of Columbina ground doves. (A) Ventral view of a wing of C. passerina (UWBM90791) showing a modified P7 morphology (arrow). (B) Occasionally P6 feathers show modified morphologies. A magnified view of P7 and P6 in a C. talpacoti specimen (UWBM84051). The presence of a modified P6 varies by species and age. (C) The region of interest (dashed lines) are shown in D, E, and F. In D, E, and F, two barbs on each feather have been darkened to emphasize their shape and length. The lower barb (proximal to feather insertion) is an unmodified barb and the upper barb is modified. (D) C. inca P7. Unmodified barb length ¼ 10.3 mm. Modified barb length ¼ 18.7 mm (E) C. passerina P7. Unmodified barb length ¼ 10.8 mm. Modified barb length ¼ 22.3 mm. (F) C. talpacoti P7. Unmodified barb length ¼ 9.7 mm. Modified barb length ¼ 24.7 mm. Scale bars indicate 10 mm for all images. produced sounds in an aeroacoustic wind tunnel Materials and methods (Clark and Mistick 2018). Then, we compared the acoustic qualities of sounds recorded in the wind P7 morphology throughout Columbina tunnel to sounds produced by wild birds in flight To characterize the morphology of remiges within using recordings from XenoCanto.org and the the genus Columbina and the evolutionary history Macaulay Library of Sound to determine if these of these morphologies across the subfamily of New modified feathers produce the wing sounds charac- World ground doves (Peristerinae) and their rela- teristic of the genus. tives, we surveyed spread wing specimens from the Sonations during flight in Columbina 1163

University of Washington Burke Museum (UWBM), separately on account of reports that their wing University of Puget Sound Slater Museum (PSM), sounds may be quieter and their feather modifica- and the University of Alaska Museum (UAM), and tions may be less extreme than adults’ (Johnston feather specimens from Featherbase (www.feather- 1960). base.info). All of these materials are listed and the Wings were clamped at the exposed humerus to a remex morphologies for each specimen are described small metal rod extending from a tripod into the

in Supplementary Table S1. For two species in the working section of the wind tunnel. The tripod Downloaded from https://academic.oup.com/icb/article/60/5/1160/5849933 by University of California, Riverside user on 23 November 2020 genus Columbina (C. picui and C. squammata), our allowed for isolated rotations relative to flow about determination of remex morphology was supple- the vertical (sweep angle; b; where b is zero when the mented with high quality photographs of live birds. leading edge of the arm-wing is perpendicular to For C. picui, these images were provided by Paul flow) and lateral (angle of attack; a; where a is Smith and are hosted at http://www.faunaparaguay. zero when the line between the wrist and S2 is par- com/columbina_picui.html. For C. squammata, these allel to flow) axes. Wings were oriented with b at images were supplemental to work by Amorim and 75 and a at 45. At this orientation, all wings Dias (2019). Material for four additional species consistently produced sounds, and sound-production (Uropelia campestris, Claravis mondetoura, Claravis diminished at angles 610 beyond these a and b geoffroyi, and Columbina cyanopis), two of which values. We did not test the effect of changing a may be extinct, could not be located or were of and b values on sound production because our sim- poor quality. The remex morphologies of these spe- plified, steady-state model is limited in its ability to cies have been described by authors in the past fully replicate the complexities of the Columbid (Goodwin 1983; Mahler and Tubaro 2001; Gibbs wingbeat, an endeavor which is beyond the scope et al. 2001), but without specimens, reliable photo- of this study. These orientations appear to match graphs, or drawings, we coded their morphologies as those observed in the upstroke of similarly-sized unknown, and following Sweet et al. (2017), we have Columbids (Crandell and Tobalske 2015; see excluded C. cyanopis entirely. Among the eight Discussion section), and wing sounds are known to remaining members of Columbina, we further cate- be produced during this phase of the wingbeat gorized morphologies into three groups based on the (Murray et al. 2017). Together, this emphasizes the size and shape of their modified regions (Fig. 1; biological relevance of these modeled orientations. Supplementary Table S1). To evaluate the evolution- Tunnel flow velocity was set to 10 ms1 to corre- ary history of the P7 morphology and its three spond to the average peak wingtip velocity of the forms, we inferred its ancestral state using an ultra- third wingbeat cycle after take-off in a similarly sized metric phylogeny from Sweet et al. (2017). We per- Columbid (Diamond Dove, Geopelia cuneata; formed these analyses in Mesquite v.3.6 (Maddison 9.9 6 1.3 ms1 for 40 g birds; Crandell and and Maddison 2018) and inferred the maximum Tobalske 2015). likelihood of ancestral states using an Mk1 rate In C. inca, where modified feather morphology is model (Lewis 2001) for trait evolution. more subtle, we performed a simple manipulation to determine the role that each modified feather plays in contributing to buzzing sounds. We used acid- Spread wings in a wind tunnel neutral, removable painter’s tape (3M Scotch- We tested dried, spread-wing specimens from the BlueTM Painter’s Tape #2090, 3M Corporate UWBM in an open-jet wind tunnel designed for Headquarters, 3M Center St. Paul, MN, USA), cut aeroacoustic experiments and described by Clark to sizes that temporarily covered the middle of two and Mistick (2018). All specimens were from adult adjacent feathers (i.e., between 20% and 70% of their birds, possessed intact and fully-grown outermost lengths, covering the entire modified region in P7), primary feathers (P10-P5), and were each from a in order to eliminate flutter in both feathers while different individual (C. passerina n ¼ 4; C. talpacoti minimally impacting airflow or sounds created by n ¼ 7; C. inca n ¼ 4; Supplementary Table S2). the free feathers (Supplementary Video 1). All adja- Morphologies appeared similar between the sexes cent pairs of feathers, from P10 to P5 (i.e., P10 and (as has been reported for other Columbids; Niese P9, P9 and P8, P8 and P7, etc.), were taped, one pair and Tobalske 2016; Murray et al. 2017), thus we at a time, and video and audio recorded of each (see treated sexes alike. We additionally tested the below). Using a similar method, we taped all primar- sound-producing capabilities of four wings from ju- ies except for groups of three adjacent feathers (P10- venile C. inca (aged according to the degree of atro- 8, P8-P6, and P7-P5), preventing airflow around all phy in the bursa of Fabricius), which we analyzed of the taped feathers in order to isolate sounds 1164 R. L. Niese et al. produced by the free feathers. For all manipulations, B for a detailed discussion). In frequency-sensitive the loudness of C. inca wing sounds was measured as analyses, the rate of element repetition becomes the the difference in sound amplitude of buzzes com- fundamental frequency of the sound, which can be pared to the sound amplitude of background tunnel measured in Raven using the “peak frequency” func- noise before each wing was placed into the tunnel tion. However, for low rates of element repetition flow (dB). We performed taping experiments on (e.g., <600 Hz), other low-frequency ambient

three wings: one adult male, one adult female, and sounds such as the persistent hum of the wind tun- Downloaded from https://academic.oup.com/icb/article/60/5/1160/5849933 by University of California, Riverside user on 23 November 2020 one juvenile (UWBM48439, UWBM80050, and nel or background sounds common to audio record- UWBM48320, respectively). As in other juveniles, ings from the field (i.e., wind, vehicles on roadways, this individual lacked a modified P6 feather which motors, flowing water, etc.) often overlap with the influenced the ways we interpreted taping experi- “peak frequency” of these repeating elements, mak- ments (see Supplementary Table S4). ing frequency-sensitive analyses unreliable (Araya- High speed video was collected using a Photron Salas et al. 2019). A time-sensitive analysis allows FASTCAM SA-3 camera (Photron USA Inc., San us to visualize each broadband element as it repeats, Diego, CA, USA; using PFV v.3282 Software) record- and distinguishes tonal sounds from atonal (i.e., ing at 6000fps with a 1/15,000 s shutter speed to a broadband) sounds by the breadth (i.e., height) of laptop computer. Audio was recorded to the same their frequency bands. However, at extremely time- laptop at 24-bits and sampling at 48 kHz through an sensitive resolutions, all sounds begin to appear audio interface (Raven Pro, v.1.4, Cornell Lab of broadband due to the inherent trade-off between Ornithology Bioacoustics Research Program, Ithaca, time- and frequency-resolution. NY, USA) with an external preamplifier (Roland In an attempt to ameliorate the dramatic loss of QUAD-CAPTURE UA-55, Roland Corporation, frequency resolution in these highly time-sensitive Hamamatsu, Japan) using a 0.5” free-field micro- analyses, we utilized a spectrum of time-sensitive phone (Bru¨el & Kjaer 4190, Naerum, Denmark) parameters specific to the rates of repetition we ob- with a turbulence-reducing nose cone (B&K UA served in flapping feathers in the wind tunnel (see 0386). The microphone was placed 10 cm down- above). All spectrograms were analyzed with a dis- stream, but not within the wake of the wings (as in crete Fourier transform frequency grid size of 2048 Clark et al. 2013a). samples and a time grid overlap of 50%, but Hann window sizes (record length) varied by 20-sample Wing sounds of free-flying birds increments from 70 to 190 samples. These parameters provided a spectrum of time analysis resolution Recordings of birds in take-off were acquired from specifically aimed at resolving elements that repeat at XenoCanto.org and the Macaulay Library of Sound rates of 685 Hz (at 70 samples) or less. We identified (Supplementary Table S3). In total, we acquired elements that were clearly visible at a high time anal- three recordings of C. passerina, four recordings of ysis resolution (70 samples) and persisted at lower C. inca, and two recordings of the C. talpacoti.To resolutions approaching the limit for expected repe- characterize wing sounds consistently across multiple tition rates for each species (e.g., 130 samples for C. recordings from different recordists with different inca sounds which are expected to repeat at 350 Hz). equipment, recording conditions, etc., and to make This improved our ability to distinguish between those measurements directly comparable to those genuinely broadband elements and elements that ap- collected from wind tunnel experiments, we analyzed pear broadband because of an individual set of spec- wing sounds using a novel method that utilized re- trographic parameters with low analysis frequency peated, time-sensitive measurements. resolution. Finally, we verified the accuracy of these measurements with high speed video of wings in the Wing sound analyses wind tunnel where the 1:1 match between the mo- Sounds that are characterized as “buzzes” in nature tion of a feather and the production of individual are often a series of rapidly repeating broadband broadband elements was more obvious (see Results elements (e.g., shuttle display buzzes in Calliope section). For all recordings, we calculated the “buzz Hummingbirds, Selasphorus calliope; Clark 2011). frequency” as the rate of repetition of individual Acoustically, these broadband elements can be de- broadband elements. In field recordings, the buzz scribed from a time-sensitive perspective that frequency was calculated individually for each wing- resolves individual elements, or from a frequency- beat, then averaged across the entire recording to sensitive perspective that instead describes the rate allow for comparisons with steady-state sounds of element repetition (Charif et al. 2010, Appendix from the wind tunnel. Sonations during flight in Columbina 1165

Statistical analyses Reconstructed ancestral states of P7 shape in All statistical analyses (except ancestral state recon- Columbina suggest that an inca-like morphology is structions, above) were performed in IBM SPSS likely ancestral to the genus, while passerina-like and Statistics v.24 (IBM Corp. Released 2016. Armonk, talpacoti-like morphologies are more derived (Fig. 2). NY, USA) after data were found to not violate the Notably, C. cruziana possesses a morphology that assumptions of normalcy. Each test used is reported may be unique within Columbina, but we coded it alongside their relevant result. as inca-like due to its relatively small increase to Downloaded from https://academic.oup.com/icb/article/60/5/1160/5849933 by University of California, Riverside user on 23 November 2020 vane width and its lack of a large hooked or recurved Results region of barbs as in passerina- and talpacoti-like feathers. Among other members of this clade of the P7 morphology throughout the genus Columbina Peristerinae, P7 morphologies do not typically devi- All members of the genus Columbina (excluding C. ate from an aerodynamically stereotyped form, cyanopis, for which we have no data) possess P7 though several species are unknown (see Discussion feathers with atypical morphologies (Fig. 1A). In section). some species, these modified morphologies also occur in P6 where they appear as slightly less dramatic versions of the P7 shape (Fig. 1B). These atypical Spread wings in a wind tunnel morphologies are the result of changes to the length Columbina passerina specimens possess a single mod- and width of barbs in the midregion of the trailing ified feather (P7) with a protrusion of elongated barbs vane (e.g., between 20% and 70% of their length; (Fig. 1A, E). At an airspeed of 10 ms1 and an ap- Fig. 1C) which widens the vane as compared to a proximate orientation emulating upstroke (b ¼ 75, stereotyped form. These modified barbs are longer a ¼45), this protrusion fluttered at 260 6 10Hz, than adjacent, unmodified barbs on the same feather, whichcausedtheprotrudingregionofthetrailing and narrower at their tips, increasing marginal barb vane of P7 to collide with P6 and produced a buzz density and decreasing marginal barb angle (i.e., (Supplementary Video 1; Figs. 3A and 4). Columbina curved toward the feather tip; Fig. 1D, E, F). The talpacoti wings also have a modified P7 feather, but gross morphology of P7 feathers (i.e., feather possess a larger protrusion (Fig. 1B, F). At the same “silhouette”) varies between species, but the under- airspeed and orientation as above, these protrusions lying modifications to barb morphology are present, fluttered at 250 6 30Hz (Fig. 4), producing very sim- to varying degrees, in all members of the genus. ilar sounds to those produced by C. passerina.For Across the eight Columbina species surveyed, we both species, there was a 1:1 match between the mo- qualitatively classified P7 feathers into three groups tion of the fluttering protrusion on P7 colliding according to the degree to which these barb modifi- against P6 and the broadband acoustic signature of cations influenced overall feather shape, and subse- buzz sounds. quently quantified barb morphometrics in an In C. inca, adult birds possess modified P7 and P6 exemplar species from each group. In C. inca, C. feathers with very small protrusions compared to C. squammata, C. picui, and C. cruziana, modified passerina and C. talpacoti (Fig. 1D). At airspeeds of barbs generate a subtle change to the P7 gross mor- 10 ms1 and an orientation emulating upstroke (b phology which we classified as inca-like (Fig. 1D). ¼ 75, a ¼45) these smaller protrusions flut- Barbs in the modified region of C. inca feathers tered at 350 6 40Hz on P7 and 340 6 10Hz on P6 are 80% longer than adjacent, unmodified barbs (Fig. 4). Columbina inca wings produced buzzing and 30% more dense. In C. talpacoti and C. buckleyi, sounds in the wind tunnel as well; however, the modified barbs create a dramatic recurved region, match between feather motion and the acoustic sig- nearly doubling the width of the trailing vane at its nature of the sounds was more difficult to ascertain widest point in some individuals (Fig. 1F). We clas- because of the dual sound source (P7 and P6, as sified this shape as talpacoti-like and is characterized opposed to only P7 in C. passerina and C. talpacoti). by barbs that are 160% longer than adjacent, To further explore this link between feather flutter unmodified barbs in this species, but are only 20% and buzz sounds, we performed a series of silencing denser. In C. passerina and C. minuta, modified experiments to determine the relative contribution of barbs generate a shape of intermediate size and are individual feathers to the overall loudness (relative characterized by modified barbs of intermediate sound amplitude; dB) of buzz sounds. length which are 100% longer and 60% more Supplementary Table S4 provides a summary of dense in C. passerina. These feathers were classified manipulations and groupings, and Supplementary as passerina-like (Fig. 1E). Table S5 provides full statistical results (ANOVA 1166 R. L. Niese et al. 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Fig. 2 Ancestral state reconstructions of P7 morphology in Columbina using a maximum likelihood approach. White nodes and tips indicate a typical, aerodynamic P7 morphology such as that shown for Zenaida macroura. Hashed gray and black tips indicate an unknown or uncertain P7 morphology. Hashed gray and black nodes indicate that ancestral states are impossible to infer. All P7 feathers are drawn to scale, except Z. macroura (scale bar shown). Phylogeny by Sweet et al. (2017). and Tukey HSD post-hoc tests). The effect of each fluttered (-P7/þP6) were of intermediate loudness manipulation on the loudness of buzzes depended and only occurred in adults (Fig. 5). In spite of adult on which modified feathers were allowed to flutter birds producing significantly louder wing sounds (ANOVA; F ¼ 12.59, df ¼ 3,23, P < 0.01). Specifically, than juveniles (see below), the effects of our silencing wing sounds were loudest in treatments that allowed experiments were similar between the two age P7 to freely flutter (þP7/þP6 and þP7/-P6; Fig. 5; groups. Collectively, these results suggest that in C. Supplementary Table S5). The sounds generated by inca, P7 is the most important source of sound, but P7 and P6 fluttering together (þP7/þP6) were not P6 is also a source of sound. significantly louder than those produced by P7 alone In juvenile C. inca individuals, three of four speci- (þP7/P6; Fig. 5; P ¼ 0.76). When neither P7 nor mens lacked obvious modifications in P6, but had P6 (-P7/-P6) fluttered, buzzes were not produced, them in P7, and one individual lacked obvious mod- but airflow over the other, nonmodified feathers still ifications in either P7 or P6. In juveniles that pos- generated some sound (Fig. 5; Supplementary Table sessed a modified P7, it fluttered at a rate of S5). Wing sounds produced whenever P6 but not P7 410 6 50Hz which was not significantly different Sonations during flight in Columbina 1167 Downloaded from https://academic.oup.com/icb/article/60/5/1160/5849933 by University of California, Riverside user on 23 November 2020

Fig. 3 Spectrograms of Columbina passerina buzz sounds produced by wing specimens and live birds. (A) Buzzes produced by a specimen (UWBM90745) in the wind tunnel at 10 ms-1 over 0.2 s. B) Buzzes produced by a live bird (XC169165) during the first four wingbeats of take-off over 0.2 s. Hann window size (record length) ¼ 110 samples. from the rate of P7 flutter in adults (t ¼1.51, df ¼ may have obscured the presence of buzzes. Buzzes 5, P ¼ 0.19; mean flutter frequencies for adults and were an obvious feature of C. inca flights and, across juveniles designated as * and respectively in all recordings, we identified 20 wingbeats with an Fig. 4). Buzzes produced by juvenile birds were not average of 3.4 6 1.0 elements per wingbeat. Buzzes as loud as buzzes produced by adults (t ¼ 2.56, df ¼ in wild C. inca flights had an average buzz frequency 6, P ¼ 0.04). of 350 6 50Hz which matched those recorded in the Across all adult wings for all three species, buzz wind tunnel for adults (t ¼ 0.2, df ¼ 6, P ¼ 0.83) and sounds did not differ in loudness regardless of spe- for adults and juveniles together (t ¼1.03, df ¼ 9, cies or sex (two-way ANOVA; Fsex ¼ 0.39, df ¼ 1,15, P ¼ 0.33; Fig. 4). Aside from recordings of C. talpa- P ¼ 0.55; Fspecies ¼ 0.75, df ¼ 1,15, P ¼ 0.50; coti, wing claps were detected in one recording of C. Fsex*species ¼ 0.10, df ¼ 1,15, P ¼ 0.91). inca (XC368476) and in no recordings of C. passerina. Wing sounds of free-flying birds The recordings of free-flying C. passerina that we analyzed contained a total of 23 wingbeats with an Discussion average of 4.1 6 1.2 broadband elements per wing- The unique P7 feathers present in members of the beat that repeated at a rate of 310 6 30Hz (Fig. 3B). genus Columbina deviate from an aerodynamically This average buzz frequency was significantly higher stereotyped form instead possessing a region of elon- than the 260 Hz buzzes recorded in the wind tunnel gate barbs that creates a distinct protrusion on its (t ¼ 5.66, df ¼ 5, P ¼ 0.002; Figs. 3A and 4). trailing vane (Fig. 1). The shape of these P7 feathers Broadband elements were not detected in our anal- facilitates aeroelastic flutter in the protrusion, caus- yses of recordings of free-flying C. talpacoti, which ing it to collide with the adjacent P6 to produce a were instead characterized by loud, atonal claps that buzzing sound (Fig. 3). Buzzes produced by dried, 1168 R. L. Niese et al. Downloaded from https://academic.oup.com/icb/article/60/5/1160/5849933 by University of California, Riverside user on 23 November 2020

Fig. 5 The effect of silencing manipulations on the loudness of buzz sounds produced by Columbina inca wings. The loudness of buzzes (sound amplitude relative to background wind tunnel noise) depends on which modified feathers are fluttering Fig. 4 Buzz frequencies produced by birds from field recordings (F ¼ 12.59, df ¼ 3,23, P < 0.01). Wings produced the loudest as compared to those recorded in the wind tunnel. Buzzes buzzes whenever P7 was fluttering freely (þP7). Whenever P7 produced by Columbina inca during flight (N ¼ 4) matched those was taped (P7), buzzes were noticeably quieter. If both P7 and recorded in the wind tunnel (N ¼ 7; t ¼1.03, df ¼ 9, P ¼ 0.33). P6 were not fluttering (P7/P6), buzzes were nearly elimi- Wings from juvenile birds that possessed a modified P7 are in- nated. Statistical differences are indicated by letters above bars cluded here and did not flutter at frequencies significantly dif- and are summarized in Supplementary Table S5. ferent from adults (t ¼ 1.5, df ¼ 5, P ¼ 0.19; average buzz frequency for adults indicated by *; average buzz frequency for juveniles indicated by ). In C. passerina, buzzes produced in that are more widespread in bird flight (Clark and flight (N ¼ 3) were statistically different (t ¼ 5.66, df ¼ 5, Prum 2015), but it is similar to the buzzes produced P ¼ 0.003) to those produced in the wind tunnel (N ¼ 4). by the tail-feathers of the Calliope Hummingbird Recordings of C. talpacoti in flight did not contain buzz elements, (Selasphorus calliope; Clark 2011). In Calliope but the frequencies observed in the wind tunnel (N ¼ 7) are shown. Dots show all observed buzz frequencies. Each point is Hummingbirds, neighboring tail-feathers flutter and the averaged buzz frequency (i.e., the rate of repetition of collide with each other and these feather-feather col- broadband buzz elements) across all wingbeats across all flights in lisions produce a buzzing sound with elements that single field recording, or over 10 ms of video for an individual repeat at 250 Hz. These tail-feather buzzes are pro- specimen in the wind tunnel. duced during sexually selected display dives and their loudness and duration are functionally linked to dive spread wings placed in a wind tunnel matched the behavior. Like the buzzes in these hummingbirds, buzzes produced by free-flying C. inca. Taken to- buzzes produced by Columbina ground doves are gether, this link between a modified morphology intrinsically linked to locomotion and may be a re- and sound-production is robust evidence that these liable indicator of flight behavior such as wingbeat remiges are specialized sonation-producing struc- frequency and flight velocity. Such information can tures (Clark 2018). Much like a bell on a cat that be related to predator avoidance as has been de- jingles with its every step, these sounds are likely scribed for other Columbids (Murray et al. 2017; involuntary (i.e., the animal may not have control Amorim and Dias 2019) but also could be used in over whether this structure makes sounds during lo- sexual signaling, though this has never been tested in comotion, see Clark 2018) but also signals because Columbids. the structures are specialized for sound production In addition to producing sonations, remiges can (Clark 2018). also become modified to function as sexually selected The mechanism of sound production uncovered visual signals or specialized aerodynamic devices, here differs from the forms of aeroelastic flutter though this is less common. It is unlikely that the Sonations during flight in Columbina 1169 specialized remiges in Columbina function as visual marginal barb density (>30%). Among the signals or as specialized aerodynamic devices. Peristerinae (those species for which P7 morphology Specifically, feathers that are sexually selected visual is known), these feather modifications are exclusive signals are physically exaggerated (i.e., ornaments), to the genus Columbina. In other Columbids, similar involved in visual displays, and/or are often sexually feather shapes have been described in P8 of four dimorphic. Male Columbina ground doves do per- members of the genus Treron (T. apicauda, T. oxy-

form a variety of wing-raising sexual or agonistic ura, T. seimundi, and T. sphenura) and in P7 of one Downloaded from https://academic.oup.com/icb/article/60/5/1160/5849933 by University of California, Riverside user on 23 November 2020 displays that could display these modifications, but (T. oxyura; Gibbs et al. 2001). Similar barb modifi- these structures are never sexually dimorphic and, cations related to sound production exist in the P10 particularly in species with an inca-like protrusion feathers of Rock Pigeons (Columba livia), but instead (the most likely ancestral state), the protrusions are produce a significant narrowing of the trailing vane, not exaggerated to the degree that might be expected not a protrusion as in Columbina (Niese and for a sexually selected visual signal. In other species Tobalske 2016). with remiges that have been modified to be sexually Remex modifications are present in all members selected visual signals, these feathers are all extreme of the Peristerinae (except perhaps Uropelia campest- ornaments that are sexually dimorphic and involved ris) and ancestral state reconstructions of modified in a conspicuous sexual display. P7 feathers suggest that the most recent common It is also unlikely that these modified feathers are ancestor of Columbina possessed a small protrusion specialized to perform unique aerodynamic functions (80% elongated barbs) that was slightly recurved like those involved in generating tip vortices or lead- (30% increased marginal barb density). Small, re- ing edge vortices (Lee et al. 2015; KleinHeerenbrink curved protrusions occur on P10 and sometimes et al. 2017). Modifications to Columbina feathers are P9 in all four members of the genus Metriopelia, not at the feather tips nor at the leading edge of the and large recurved protrusions occur in P9 and P8 wing/feathers, suggesting that they likely do not play in Claravis pretiosa (Supplementary Table S1). This a role in generating tip or leading-edge vortices. In suggests that all members of Peristerinae may share other Columbids with specialized, sound-producing the underlying developmental and gene regulatory barbs in this region of the trailing vane (P10 in pathways responsible for these relatively similar Columba livia), flutter reduces aerodynamic force barb modifications. Although the regulatory path- production (Niese and Tobalske 2016), suggesting ways governing barb growth angle, bilateral feather they are not specialized aerodynamic devices. asymmetry, and rachis morphology are known and Furthermore, this reduction in aerodynamic force shared among all birds (Feo et al. 2016; Li et al. production could be interpreted as a “cost” for pro- 2017), it is yet unclear how barb length or marginal ducing sound, thus implicating an adaptive function barb density (i.e., barb tip diameter) is controlled. for such modified remiges (Niese and Tobalske Unlike an emarginated remex shape (e.g., those in 2016). However, further research is needed to deter- raptors, gallinaceous species, etc.; Klaassen van mine the biological relevance of this relatively small Oorschot et al. 2017), which results from a rapid, cost and its potentially paradoxical involvement in but gradated change in regulatory molecules (Li the evolution of an alarm signal that is produced by et al. 2017), P7 morphology in Columbina ground fleeing. doves must result from a switch-like regulatory path- All members of the genus Columbina possess way during feather growth. Such a pathway has not modified P7 feathers which vary in shape but possess been described within an individual feather, though similar modifications to underlying barb morphol- a similar switch-like pathway regulates the differen- ogy (Fig. 1). Specifically, these feathers possess a re- tiation of feather types (e.g., dorsal vs. breast plumes; gion of modified barbs on the trailing vane that are Li et al. 2017). 80–160% elongated and 20–60% denser marginally The wings of C. inca possess P7 and P6 feathers (relative to adjacent, unmodified barbs), creating a with modified regions that flutter in airflow to pro- distinct protrusion. Protrusion shape appears to vary duce buzz sounds. The loudness of these sounds was with modified barb length and marginal barb density primarily due to flutter in P7, and buzzes were si- such that the largest protrusions (talpacoti-like) pos- lenced entirely when P7 and P6 were prevented from sess barbs that are highly elongated (160%) but have fluttering (Fig. 5). In juvenile birds, feather modifi- low marginal barb density (20%), while the smallest cations were not always present, making their wing protrusions (inca-like) have less elongate barbs sounds significantly quieter or absent. In the wild, (80%), and “recurved” or “hooked” protrusions juvenile birds also lack wing sounds or produce only (passerina-like and inca-like) tend to have a higher weak sounds (Johnston 1960). This has intriguing 1170 R. L. Niese et al. implications for the function of the sonation due to sonation behaviors (e.g., intersexual, agonistic, natu- juveniles’ lower reliability as signalers. If an individ- rally selected) depending on their context. ual is unable to produce a signal until they have Unlike recordings of free-flying C. talpacoti, only moulted into their adult plumage, then they may one recording of C. inca and no recordings of C. be prevented from diluting the efficacy of the signal passerina contained clap-like elements. During slow with their unreliable responses to cues. In alarm flight, such as during take-off or landing, all birds

sonations specifically, this may prevent young birds that perform a tip-reversal upstroke, including Downloaded from https://academic.oup.com/icb/article/60/5/1160/5849933 by University of California, Riverside user on 23 November 2020 from inducing a costly predator avoidance take-off Columbids, produce above-the-body claps (at the event, or it may prevent “bird who flapped wolf” end of upstroke; Crandell and Tobalske 2015), while scenarios that degrade the value of the alarm signal below-the-body claps tend to only occur during (McLinn and Stephens 2010; Murray et al. 2017). powerful, high wingbeat amplitude escape maneuvers While recordings of buzzes produced by free- (Hingee and Magrath 2009; Niese and Tobalske flying C. inca matched those produced in the wind 2016; Murray et al. 2017). Interestingly, in C. inca, tunnel, recordings of C. passerina were not a close clap-like elements occurred after buzzes, not before match (Fig. 4). This could be due to differences be- them as would be predicted if buzzes were produced tween the wingtip velocities estimated for our wind on the downstroke following an above-the-body tunnel experiments and those that occur in vivo.In clap. This suggests that buzzes are produced on the the wind tunnel, flow velocity was approximately upstroke and corroborates our wind tunnel experi- 10 ms1 which emulated the peak wingtip velocities ments in which the wings of all three species pro- observed in casual, horizontal flights in trained duced the loudest, most consistent sounds when Diamond Doves (Geopelia cuneata), a similarly sized their orientations matched that of upstroke (e.g. (about 40 g), but distantly related ground dove Crandell and Tobalske 2015), not downstroke. (Crandell and Tobalske 2015). This velocity would be higher if birds were fleeing a predator or if C. passerina have a naturally higher wingbeat frequency than G. cuneata (see below). If flutter frequency in C. Conclusions passerina P7 feathers positively correlates with flow P7 feathers in the genus Columbina have highly velocity (which is often the case in other fluttering modified shapes that deviate from stereotypically feathers; Clark and Prum 2015; Clark et al. 2013b), aerodynamic forms to varying degrees, possessing the conservative nature of our estimate for peak morphologies that are specialized to produce buzzing wingtip velocity could explain the lower buzz fre- sonations. These feathers have been coopted as spe- quencies we observed for C. passerina wings in the cialized acoustic signaling structures similar to those wind tunnel. described in two other species of Columbids (Niese Recordings of C. talpacoti contained very promi- and Tobalske 2016; Murray et al. 2017). Like the nent wing claps and these loud, broadband sounds sonation-producing feather modifications that occur may have masked the subtler sounds of buzzes. in other Columbids, these specialized remiges are Additionally, this species may perform sexually se- sexually monomorphic and the sounds they produce lected flight displays that incorporate wing claps are likely alarm signals (Murray et al. 2017). Given (Goodwin 1983). It is the only species in the genus the diversity of P7 shape in Columbina ground doves for which such displays have been described and is and the variety of modified remiges in the also the only member of the genus with strongly Peristerinae, sonations likely play a powerful role in sexually dimorphic plumage. Our sample of C. tal- driving the diversity of both feather morphologies pacoti wing sounds suggests that, as it produces and communication behaviors in this clade. claps, it flies with a dramatically reduced wingbeat frequency (8.9 6 2.8 Hz) as compared to C. inca and C. passerina (18.2 6 1.2 Hz) and G. cuneata (15.0 6 0.6 Hz). In other species where wing sounds Data availability are communicative and involved in display flights, All photographs of UWBM and PSM spread wing individuals modulate their wingbeat frequency and/ specimens can be accessed at https://digitalcollec- or amplitude when signaling, a behavior that often tions.pugetsound.edu/digital/collection/slaterwing. coevolves with sonations (Clark 2011). It is possible Feather specimens from Featherbase can be accessed that a reduced wingbeat frequency, prominent wing at http://www.featherbase.info/en/home. Audio claps, and specialized buzz-producing P7 morpholo- recordings can be accessed via the reference links gies in C. talpacoti may be related to one or multiple listed in Supplementary Table S3. Sonations during flight in Columbina 1171

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