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Physical Limits of Flight Performance in the Heaviest Soaring Bird

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Physical Limits of Flight Performance in the Heaviest Soaring Bird View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Cronfa at Swansea University Physical limits of flight performance in the heaviest soaring bird H. J. Williamsa,b,1, E. L. C. Sheparda,1,2, Mark D. Holtonc, P. A. E. Alarcónd, R. P. Wilsona, and S. A. Lambertuccid aDepartment of Biosciences, Swansea University, SA2 8PP Swansea, United Kingdom; bDepartment of Migration, Max Planck Institute of Animal Behaviour, 78315 Radolfzell, Germany; cDepartment of Computing Science, Bay Campus, Swansea University, SA1 8EN Swansea, United Kingdom; and dGrupo de Investigaciones en Biología de la Conservación, Universidad Nacional del Comahue-CONICET, Quintral 1250, R8400FRF Bariloche, Argentina Edited by Robert E. Ricklefs, University of Missouri–St. Louis, St. Louis, MO, and approved June 8, 2020 (received for review May 3, 2019) Flight costs are predicted to vary with environmental conditions, absolutely necessary. Large soaring birds are most likely to flap and this should ultimately determine the movement capacity and to remain airborne or increase speed at times when they are distributions of large soaring birds. Despite this, little is known unable to soar. Knowing the extent to which aerial conditions about how flight effort varies with environmental parameters. We force large birds to use powered flight is key to understanding deployed bio-logging devices on the world’s heaviest soaring bird, how their movements and space-use are constrained by the the Andean condor (Vultur gryphus), to assess the extent to which physical environment (12). these birds can operate without resorting to powered flight. Our Examining when and where obligate soarers resort to flapping records of individual wingbeats in >216 h of flight show that should also provide insight into the particular conditions that condors can sustain soaring across a wide range of wind and ther- might have supported the flight of the largest birds ever to have mal conditions, flapping for only 1% of their flight time. This is flown (24). The largest extant soaring birds weigh up to almost among the very lowest estimated movement costs in vertebrates. 16 kg (25), but extinct terrestrial birds were much larger, with One bird even flew for >5 h without flapping, covering ∼172 km. the largest, Argentavis magnificens, estimated to have weighed Overall, > 75% of flapping flight was associated with takeoffs. ∼72 kg or more (24). It has always been assumed that Argentavis Movement between weak thermal updrafts at the start of would have been incapable of sustained flapping flight and the day also imposed a metabolic cost, with birds flapping toward thus entirely dependent on soaring. Nonetheless, almost noth- the end of glides to reach ephemeral thermal updrafts. Nonethe- ing is known about the amount of flapping flight required for less, the investment required was still remarkably low, and even in daily foraging movements even in large extant soaring birds ECOLOGY winter conditions with weak thermals, condors are only predicted (26–28). to flap for ∼2 s per kilometer. Therefore, the overall flight effort in In the present study, we assessed whether, and if so, how, flight the largest soaring birds appears to be constrained by the require- effort varies with environmental conditions in the world’s heaviest ments for takeoff. extant soaring bird, the Andean condor (Vultur gryphus). Given that flapping was likely to be relatively infrequent, we developed aeroecology | energy landscape | biologging | flight constraints | custom logging and tag-release systems to obtain uninterrupted, movement ecology high-frequency data on the flight behavior of these birds. These radients in energy have been invoked to explain macroecological Significance Gpatterns including species distribution and abundance (1, 2). While the main forms of available energy are typically identified Flapping flight is extremely costly for large birds, yet little is as photosynthetically active radiation and chemical energy (reviewed known about the conditions that force them to flap. We at- in ref. 3), flying animals extract kinetic and potential energy from the tached custom-made “flight recorders” to Andean condors, the environment by soaring, and use this energy to subsidize the meta- world’s heaviest soaring birds, documenting every single bolic costs of flapping flight. Therefore, flight costs and capacities in wingbeat and when and how individuals gained altitude. Re- animals are fundamentally linked to the characteristics of air currents markably, condors flapped for only 1% of their flight time, – (4 6), and this affects large-scale patterns of space use. For instance, specifically during takeoff and when close to the ground. This passerine birds tune their migration decisions in relation to the wind is particularly striking as the birds were immature. Thus, our (7) and use particular migration flyways that are not necessarily as- results demonstrate that even inexperienced birds can cover sociated with the shortest route (8–10). Outside of migration, it is the vast distances over land without flapping. Overall, this can help ecology of soaring flight specialists that should be most closely linked explain how extinct birds with twice the wingspan of condors to environmental conditions (11–14). Indeed, for the very largest could have flown. flying birds, the dependence on soaring is such that their distributions appear to be linked to, and potentially constrained by, the availability Author contributions: E.L.C.S. and S.A.L. designed research; H.J.W., E.L.C.S., P.A.E.A., and of updrafts or wind shear (5). S.A.L. performed research; M.D.H. contributed new reagents/analytic tools; H.J.W. and Soaring specialists tend to be large birds (but see refs. 15 and R.P.W. analyzed data; and E.L.C.S. wrote the paper. 16), as the selective pressure to extract energy from the aerial The authors declare no competing interest. environment is related to the costs of powered flight, which in- This article is a PNAS Direct Submission. crease more or less proportionately with body size (Mass1.17) This open access article is distributed under Creative Commons Attribution-NonCommercial- (17). In contrast, the costs of soaring appear to be approximately NoDerivatives License 4.0 (CC BY-NC-ND). – Data deposition: GPS and Daily Diary data for the eight condors have been uploaded to twice the resting requirement (18 20), which itself decreases with “ 0.67 the Movebank database under the study Andean Condor (Vultur gryphus), Bariloche, Argentina, increasing mass (being proportional to Mass ) (21). Therefore, 2013–2018” (https://www.movebank.org/cms/webapp?gwt_fragment=page=studies, the disparity between the metabolic costs of soaring and flapping path=study1109284853). increases with animal mass, so that for large birds, the cost of 1H.J.W. and E.L.C.S. contributed equally to this work. flapping flight is predicted to be some 30 times greater than 2To whom correspondence may be addressed. Email: [email protected]. resting metabolic costs (22). This puts flapping flight in the same This article contains supporting information online at https://www.pnas.org/lookup/suppl/ bracket as other high-performance activities, such as sprinting in doi:10.1073/pnas.1907360117/-/DCSupplemental. mammals (23), which individuals should undertake only when www.pnas.org/cgi/doi/10.1073/pnas.1907360117 PNAS Latest Articles | 1of7 Downloaded by guest on July 23, 2020 continuous data enable us to identify each and every wingbeat, flapping flight at two different scales: across all flight time and in from which we assess the precise conditions that elicit flapping. the specific phases when condors were moving between sources of We hypothesized that flight costs would be linked to the prevailing rising air (categorized as thermal updrafts or orographic updrafts conditions, decreasing with increased availability in updrafts in the case of slope soaring). Overall, our results reveal the ca- stemming from wind speed and thermal convection (26, 27, 29). pacity of these birds to soar and the environmental factors that We thus expected to see a space-linked pattern of effort, with may constrain the movements of large soaring fliers. flapping flight less likely in more mountainous areas, which are associated with updrafts in a wide range of weather conditions. Methods However, even in regions where updrafts tend to be strong, such Eight immature condors (9.5 to 13.9 kg) were each equipped with an archival as over mountainous terrain, soaring birds must contend with “Daily Diary” (DD) unit (Wildbyte Technologies) (31), a GPS unit (Mobile temporal and fine-scale spatial variation in the availability of rising Action Technology, model GT-120), and a miniature VHF in Bariloche, Argentina (a region of mountainous Andes and flatter steppe) from 2013 to air. In fact, mountains are characterized by particularly complex 2018 (32) (SI Appendix). The DD loggers included a triaxial accelerometer airflow regimes (30). Therefore, operating in these areas is in (sampling at 20/40 Hz, enabling identification of wingbeats), a triaxial itself, a strategy that will ensure low movement costs. As a result, magnetometer (sampling at 40 Hz, enabling distinguishing circling in ther- we examined the physical determinants of the investment in mals from soaring in slope lift) (Fig. 1) (33, 34), and a barometric pressure Fig. 1. The classification of passive flight types and their distribution in space. (A) Ethogram of flight types within a single flight, classified according to the rate of change in altitude (from pressure data, in Pa) and heading (from triaxial magnetometry; Mag, G), and the absence of flapping (dynamic movement in triaxial acceleration; Acc, g). (B) GPS points (60-s frequency) within the local region, color-coded by flight type. (C) The track of a single flight from the mountainous Andes to the steppe, resolved by dead-reckoning between GPS fixes (black circles) using the heading (from the magnetometer) and a constant speed.
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