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Compound-V Formations in Shorebird Flocks

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Compound-V Formations in Shorebird Flocks bioRxiv preprint doi: https://doi.org/10.1101/545301; this version posted February 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Compound-V formations in shorebird flocks Aaron J. Corcoran1, Tyson L. Hedrick1* 1 University of North Carolina at Chapel Hill, Chapel Hill NC USA 27599 *author for correspondence Dr. Tyson Hedrick UNC Dept. of Biology Coker Hall CB #3280 120 South Road Chapel Hill, NC 27599-3280 Email: [email protected] Phone: (919) 962-0757 Keywords: bird, flocking, collective behavior, flight, biomechanics, migration 1 bioRxiv preprint doi: https://doi.org/10.1101/545301; this version posted February 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Abstract 2 Animal groups have emergent properties that result from simple interactions among individuals. However, we 3 know little about why animals adopt different interaction rules because of sparse sampling among species. Here, 4 we identify an interaction rule that holds across single and mixed-species flocks of four migratory shorebird 5 species spanning a seven-fold range of body masses. The rule, aligning with a 1-wingspan lateral distance to 6 nearest neighbors in the same horizontal plane, scales linearly with wingspan but is independent of nearest 7 neighbor distance and neighbor species. This rule propagates outward to create a global flock structure that we 8 term the compound-V formation. We propose that this formation represents an intermediary between the cluster 9 flocks of starlings and the simple-V formations of geese and other large migratory birds. Analysis of individual 10 wingbeat frequencies and airspeeds indicates that the compound-V formation may be an adaptation for 11 aerodynamic flocking. 12 13 Introduction 14 The collective movements of animals—from schooling fish to swarming insects and flocking birds—have long 15 excited intrigue among observers of nature. Collective motion arises as an emergent property of interactions 16 between individuals [reviewed by (Herbert-Read, 2016; Vicsek & Zafeiris, 2012)]. Thus, much attention has been 17 placed on identifying local interaction rules (Ballerini et al., 2008; Herbert-Read et al., 2011; Katz, Tunstrøm, 18 Ioannou, Huepe, & Couzin, 2011; Lukeman, Li, & Edelstein-Keshet, 2010) and how those rules affect group 19 structure and movement (Buhl et al., 2006; Hemelrijk & Hildenbrandt, 2012). However, comparative data across 20 species are still limited, preventing us from testing hypotheses regarding the evolution and diversity of collective 21 movement patterns. 22 For example, out of hundreds of bird species that fly in groups, most research has focused on starlings (Attanasi 23 et al., 2014; Ballerini et al., 2008; Cavagna et al., 2010), homing pigeons (Nagy et al., 2013; Nagy, Ákos, Biro, & 24 Vicsek, 2010; Pettit, Ákos, Vicsek, & Biro, 2015; Pettit, Perna, Biro, & Sumpter, 2013; Usherwood, Stavrou, Lowe, 25 Roskilly, & Wilson, 2011) and birds that fly in V-formations (Badgerow & Hainsworth, 1981; Cutts & Speakman, 26 1994; Hummel, 1983; Lissaman & Shollenberger, 1970; Maeng, Park, Jang, & Han, 2013; Portugal et al., 2014; 27 Weimerskirch, Martin, Clerquin, Alexandre, & Jiraskova, 2001). These data indicate that smaller birds fly in 28 relatively dense cluster flocks that facilitate group cohesion and information transfer (Attanasi et al., 2014; 29 Ballerini et al., 2008), whereas larger migratory birds fly in highly-structured V formations (also known as line or 30 echelon formations) that provide aerodynamic and energetic benefits (Lissaman & Shollenberger, 1970; Portugal 31 et al., 2014; Weimerskirch et al., 2001). The species whose flocking behavior have been studied in detail differ in 32 many ways that could be important for flocking including body size, ecology, the frequency of aggregation and its 33 behavioral context. Therefore, it is difficult to conclude based on the available data what factors contribute to 34 birds adopting specific group formations. 35 We aimed to address this question by collecting three-dimensional (3D) trajectories of the birds in flocks of four 36 shorebird species that have similar ecologies (all forage in large groups in coastal habitats and migrate long 37 distances) but cover a seven-fold range of body mass and two-fold range of wingspan. Our study species include 38 dunlin (Calidris alpina, Linnaeus 1758; 56 g, 0.34 m wingspan), short-billed dowitcher (Limnodromus griseus, 39 Gmelin 1789; 110 g, 0.52 m wingspan), American avocet (Recurvirostra Americana, Gmelin 1789; 312 g, 0.72 m 40 wingspan), and marbled godwit (Limosa fedoa, Linnaeus, 1758; 370 g, 0.78 m). Molecular dating indicates that 41 these species diverged from their nearest common ancestor by approximately 50 Mya (Baker, Pereira, & Paton, 42 2007), providing time for evolutionary diversification of flocking behavior. By comparing group structure of birds 2 bioRxiv preprint doi: https://doi.org/10.1101/545301; this version posted February 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 43 across a range of body sizes and comparing our data from that in the literature, we aimed to determine the extent 44 to which flock structure varies across species with different body sizes and ecologies. We employ three 45 approaches: 1) identify local interaction rules by quantifying the relative positions of birds and their nearest 46 neighbors; 2) quantify the degree of spatial structure within flocks; and 3) use measurements of individual speeds 47 and wingbeat frequencies to test whether local or global 48 position within the flock affects flight performance. a 49 Based on existing flock data, we hypothesized that flocks Humboldt bay 50 of larger shorebird species would be more structured High-tide roost 51 than smaller species (recapitulating the trend of larger Coastal habitat 52 birds flying in highly-structured V formations) and that 120 m Flock path 53 larger species would also more frequently exhibit Camera Camera view 54 aerodynamic formations. Because a previous study 270,000 m3 55 showed that flying in a cluster flock is energetically 56 costly in pigeons (Usherwood et al., 2011), we 57 hypothesized that birds flying in the middle and rear of b 58 flocks and birds flying closer to their nearest neighbor 40 59 would have reduced flight performance (lower speed 60 relative to their wingbeat frequency). Surprisingly, we 61 found that all four species studied here fly in a 30 62 previously-undescribed flock structure that we term the 63 compound-V formation. We propose that this structure Y (m) 20 64 is an adaptation for aerodynamic flocking in migratory 65 species, and that ecology is an underappreciated driver 66 of the evolution of avian flocking behavior. 10 67 Results 0 c 68 We reconstructed the 3D trajectories from 18 bird flocks 10 69 that ranged in size from 189 to 961 individuals and were 5 Z (m) 70 recorded for 2.4 – 13.2 s at 29.97 frames per second 0 0 10 20 30 40 50 71 (Figure 1, Table 1). This resulted in 1,598,169 3D position X (m) 72 measurements that were used for examining flock 73 structure. Sixteen of the 18 flocks were comprised Figure 1. Shorebird flock recording 74 entirely of a single species. The remaining two flocks (a) Multi-camera videography was used to reconstruct 75 were mixed-species flocks of marbled godwits and 3D trajectories of shorebirds flying near high-tide roosts 76 short-billed dowitchers. Computer vision techniques in Humboldt Bay, California. (b) Overhead and (c) profile 77 allowed species identification of individuals in mixed- views of an example flock. Symbol sizes reflect actual 78 species flocks based on differences in body size (See scales for birds with outstretched wings. 79 Materials and Methods). 3 bioRxiv preprint doi: https://doi.org/10.1101/545301; this version posted February 8, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 80 Nearest neighbor alignment 81 We examined flock 82 structure by quantifying the Flock Species N N n.n. dist n.n. Ground Airspeed Wind Wind Z-speed Turn rate birds Frame s (m) (WS) power speed (m·s-1) speed direction (m·s-1) (° s-1) 83 position of each bird with (m·s-1) (m·s-1) (deg.) 1.30 1.67 5.43 9.36 1.12 42.6 84 respect to its nearest 0417-2 Godwit 286 147 0.361 5.73 5.9 0.79, 2.15 3.64, 8.66 8.04, 10.55 0.09, 1.97 18.5, 91.8 1.17 2.25 5.30 9.25 1.29 45.8 85 neighbor. We used modal 0417-2 Dowitcher 309 147 0.385 5.73 5.9 0.73, 1.89 3.56, 8.56 7.95, 10.48 0.23, 2.08 20.1, 97.7 1.81 2.32 3.33 7.94 -0.18 35.9 86 values to characterize 0417-3 Godwit 474 278 0.428 5.73 3.9 1.01, 2.94 1.72, 6.56 6.21, 9.78 -1.27, 0.76 0.04, 121.2 1.71 2.19 6.67 8.84 0.22 16.4 87 typical neighbor positions 0417-4 Godwit 802 397 0.391 5.73 -312.1 1.02, 2.57 3.29, 9.57 7.69, 10.06 -0.78, 1.09 5.2, 50.5 88 because position 1.57 2.25 4.49 8.69 0.41 22.5 0417-4 Dowitcher 74 397 0.382 5.73 -312.1 0.94, 2.37 2.76, 7.61 7.63, 9.75 -0.60, 1.26 7.2, 59.3 89 distributions were skewed 1.19 1.53 7.05 10.62 -0.26 24.5 0420-1 Godwit 628 177 0.409 4.06 5.5 0.60, 1.94 5.14, 9.85 8.57, 13.42 -1.83, 1.02 8.1, 95.4 90 as a result of values being 1.54 1.97 8.92 10.55 -0.07 13.1 0420-2 Godwit 304 147 0.431 4.06 54.8 91 cropped at zero.
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