bioRxiv preprint doi: https://doi.org/10.1101/2020.10.31.354605; this version posted November 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 2 Soaring styles of extinct giant birds and pterosaurs 3 4 5 Authors: 6 Yusuke Goto1*, Ken Yoda2, Henri Weimerskirch1, Katsufumi Sato3 7 8 Author Affiliation: 9 1Centre d’Etudes Biologiques Chizé, CNRS – Université de la Rochelle, 79360 Villiers 10 En Bois, France. 11 2Graduate School of Environmental Studies, Nagoya University, Furo, Chikusa, 12 Nagoya, Japan. 13 3Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan. 14 15 16 Corresponding Author: 17 Yusuke Goto 18 Centre d’Etudes Biologiques Chizé, CNRS – Université de la Rochelle, 79360 Villiers 19 En Bois, France. 20 e-mail: [email protected] 21 TEL: +814-7136-6220 22 23 24 Keywords: 25 birds, pterosaurs, soaring performance, wind, dynamic soaring, thermal soaring 26 27 28 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.31.354605; this version posted November 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 29 Summary 30 The largest extinct volant birds (Pelagornis sandersi and Argentavis magnificens) and pterosaurs 31 (Pteranodon and Quetzalcoatlus) are thought to have used wind-dependent soaring flight, similar to 32 modern large birds. There are two types of soaring: thermal soaring, used by condors and frigatebirds, 33 which involves the use of updrafts over the land or the sea to ascend and then glide horizontally; and 34 dynamic soaring, used by albatrosses, which involves the use of wind speed differences with height above 35 the sea surface. Previous studies have suggested that Pelagornis sandersi used dynamic soaring, while 36 Argenthavis magnificens, Pteranodon, and Quetzalcoatlus used thermal soaring. However, the 37 performance and wind speed requirements of dynamic and thermal soaring for these species have not yet 38 been quantified comprehensively. We quantified these values using aerodynamic models and compared 39 them with that of extant birds. For dynamic soaring, we quantified maximum flight speeds and maximum 40 upwind flight speeds. For thermal soaring, we quantified the animal’s sinking speed circling at a given 41 radius and how far it could glide losing a given height. Our results confirmed those from previous studies 42 that Pteranodon and Argentavis magnificens used thermal soaring. Conversely, the results for Pelagornis 43 sandersi and Quetzalcoatlus were contrary to those from previous studies. Pelagornis sandersi used 44 thermal soaring, and Quetzalcoatlus had a poor ability both in dynamic and thermal soaring. Our results 45 demonstrate the need for comprehensive assessments of performance and required wind conditions when 46 estimating soaring styles of extinct flying species. 47 48 49 Introduction 50 Flying animals have evolved a wide range of body sizes. Among them, there have been incredibly large 51 species of birds and pterosaurs (Fig. 1). Pelagornis sandersi and Argentavis magnificens are the largest 52 extinct volant birds. Their estimated wingspans reached 6–7 m (1–4), twice as large as that of the 53 wandering albatross, the extant bird with the longest wingspan (Table 1). Several large species of 54 pterosaurs appeared in the Cretaceous period. Pteranodon, presumably the most famous pterosaur, is 55 estimated to have had a wingspan of 6 m (Table 1) (5). The azhdarchids are one of the most successful 56 Cretaceous pterosaur groups and include many large species with wingspans of approximately 10 m 57 (Table 1) (6–9). Quetzalcoatlus northorpi, one of the azhdarchid species, is regarded as one of the largest 58 flying animals in history. 59 Discoveries of these giant winged animals have fascinated paleontologists and biologists for 60 over a century. Their flight ability has been of great interest because their huge size must significantly 61 affect their flight. With increasing size, the power required to fly increases faster than the power muscles 62 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.31.354605; this version posted November 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 63 64 65 Fig. 1. A size comparison and soaring styles of extinct giant birds (Pelagornis 66 sandersi and Argentavis magnificens), pterosaurs (Pteranodon and 67 Quetzalcoatlus), the largest extant dynamic soaring bird (wandering albatross), 68 the largest extant thermal soaring terrestrial bird (California condor), the largest 69 extant thermal soaring seabird (magnificent frigatebird), and the heaviest extant 70 volant bird (kori bustard). The icons indicate dynamic soarer, thermal soarer, 71 and poor soarer and summarize the main results of this study. The red arrows 72 indicate the transition from a previous expectation or hypothesis to 73 the knowledge updated in this study. 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.31.354605; this version posted November 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 74 Species Mass Wingspan Wing Aspect Wing loading Ref (kg) (m) area (m2) ratio Pelagornis sandersi 21.8, 6.06, 6.13, 2.45 13.0, 51.0 ~ 87.4 (1) and 6.40 and ~ 14.0, (with 21.8 kg Mass) 40.1 7.38 4.19 and 15.0 93.9 ~ 161 (with 40.1 kg Mass) Argentavis magnificens 70.0 7.00 8.11 6.04 84.7 (4) Extinct Pteranodon 36.7 5.96 1.99 17.9 181 (5) Quetzalcoatlus 259 9.64 11.4 8.18 224 (5) wandering albatross 8.64 3.05 0.606 15.4 140 (47)* (Diomedea exulans) black-browed albatross 3.55 2.25 0.376 13.4 87.5 (48)* (Thalassarche melanophris) white-chinned petrel 1.37 1.40 0.169 11.6 79.5 (49) Dynamicsoaring (Procellaria aequinoctialis) magnificent frigatebird 1.52 2.29 0.408 12.8 36.5 (18) (Fregata magnificens) California condor 9.50 2.74 1.32 5.70 70.6 (4) (Gymnogyps californianus) brown pelican 2.65 2.10 0.450 9.80 57.8 (18) (Pelecanus occidentalis) Thermalsoaring black vulture 1.82 1.38 0.327 5.82 54.6 (18) (Coragyps atratus) white stork 3.40 2.18 0.540 7.42 61.8 (4) (Ciconia ciconia) kori bustard 11.9 2.47 1.06 5.76 110 (17) - (Ardeotis kori) Non Soaring 75 76 77 Table 1. Morphological values of examined species. *For the wandering 78 albatross and the black-browed albatross, we used the averages calculated 79 from the morphological values of males and females in the cited references (47, 80 48). For the kori bustard, we used the morphology data available in the Flight 81 program (17). 82 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.31.354605; this version posted November 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 83 are able to produce by flapping of wings. Hence, this physical constraint resulted in two 84 heated arguments about the flight of extinct giants. The first is about whether and how they were able to 85 take off (4, 10–12). The present study focused on the second debate. Due to the high costs of flapping that 86 stems from their large body size, large extant birds prefer to fly utilizing wind energy or convection, that 87 is, they prefer to soar (10, 13). Hence, it is presumed that extinct large animals also employed soaring 88 flight as their primary mode of transportation (1, 4, 14). The second debate is about what kind of soaring 89 flight style they employed (1, 4, 14–16). 90 There are two main soaring flight styles among extant birds: dynamic soaring and thermal 91 soaring (17). In dynamic soaring, birds extract flight energy from wind shear—the vertical gradient in 92 horizontal wind speed over the ocean (Fig. 2A). Extant seabirds (e.g., albatrosses, shearwaters, and 93 petrels) employ this soaring style and can routinely travel hundreds of kilometers per day over the sea. In 94 thermal soaring, birds first fly circling in warm rising-air columns (thermals). They climb to a substantial 95 height and then glide off in the desired direction while losing their height (Fig. 2C-E). By repeating this 96 up-down process, birds travel over vast distances. Various terrestrial bird species (e.g., vultures, eagles, 97 and storks) and seabirds (e.g., frigatebirds and pelicans) employ thermal soaring. 98 This study investigated which soaring styles were employed by four large extinct species, that 99 is, Pelagornis sandersi, Argentavis magnificens, Pteranodon, and Quetzalcoatlus. Their soaring 100 capabilities were quantified using two factors. The first is performance, as the available speed and 101 efficiency of soaring. The second is the minimum wind speed required for sustainable soaring flight. 102 For thermal soaring, performance was evaluated during the gliding and soaring up phases. In 103 the gliding phase, a bird’s performance is its glide ratio, which is the ratio of distance a bird traverses to 104 the height the bird loses to cover that distance, i.e., (glide ratio) = (horizontal speed)/(sinking speed) (Fig. 105 2E). A bird with a higher glide ratio is more efficient as it can traverse a longer distance for the same 106 amount of height lost as a bird with a lower glide ratio.