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High Altitude Fl Ights by Ruddy Shelduck Tadorna Ferruginea During Trans

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High Altitude Fl Ights by Ruddy Shelduck Tadorna Ferruginea During Trans Journal of Avian Biology 48: 001–006, 2017 doi: 10.1111/jav.01443 © 2017 Th e Authors. Journal of Avian Biology © 2017 Nordic Society Oikos Subject Editor: Th omas Alerstam. Editor-in-Chief: Jan- Å ke Nilsson. Accepted 31 May 2017 High altitude fl ights by ruddy shelduck Tadorna ferruginea during trans-Himalayan migrations N. Parr , S. Bearhop , D. C. Douglas , J. Y. Takekawa , D. J. Prosser , S. H. Newman , W. M. Perry , S. Balachandran , M. J. Witt , Y. Hou , Z. Luo and L. A. Hawkes N. Parr (http://orcid.org/0000-0001-6115-6816), S. Bearhop and L. A. Hawkes ([email protected]), College of Life and Environmental Sciences, Univ. of Exeter, Penryn, Cornwall, UK. – D. C. Douglas, US Geological Survey Alaska Science Centre, Juneau, AK, USA. – J. Y. Takekawa, Audubon California, Tiburon, CA, USA. – D. J. Prosser, US Geological Survey Patuxent Wildlife Research Centre, Beltsville, MD, USA. – S. H. Newman, Foods and Agriculture Organization of the United Nations (FAO), Italy, and CMC Road next to ILRI, Gurd Shola, Bole Sub City, Kebele, Addis Ababa, Ethiopia. – W. M. Perry, Dixon Field Station, Dixon, CA, USA. – S. Balachandran, Bombay Natural History Society, Mumbai, India. – M. J. Witt, Environment and Sustainability Inst., Univ. of Exeter, Penryn, Cornwall, UK. – Y. Hou, Qinghai Lake National Nature Reserve, Xining, China. – Z. Luo, Computer Network Information Center (CNIC), Chinese Academy of Sciences, Beijing, China. Birds that migrate across high altitude mountain ranges are faced with the challenge of maintaining vigorous exercise in environments with limited oxygen. Ruddy shelducks are known to use wintering grounds south of the Tibetan Plateau at sea level and breeding grounds north of Himalayan mountain range. Th erefore, it is likely these shelducks are preforming high altitude migrations. In this study we analyse satellite telemetry data collected from 15 ruddy shelduck from two populations wintering south of the Tibetan Plateau from 2007 to 2011. During north and south migrations ruddy shelduck travelled 1481 km (range 548 – 2671 km) and 1238 km (range 548 – 2689 km) respectively. We fi nd mean maximum altitudes of birds in fl ight reached 5590 m (range of means 4755 – 6800 m) and mean maximum climb rates of 0.45 m s – 1 (range 0.23 – 0.74 m s – 1 ). Th e ruddy shelduck is therefore an extreme high altitude migrant that has likely evolved a range of physiological adaptations in order to complete their migrations. Amongst the most impressive animal migrations are those tolerance and there is growing evidence that high altitude made by birds, which make the furthest and fastest migra- fl ights are undertaken by a variety of species (Liechti and tions of any animal (Gill et al. 2009, Egevang et al. 2010, Schaller 1999, Dolbeer 2006, Schmaljohann et al. 2009). Klaassen et al. 2011). Migrants that fl y across mountain Bar-headed geese Anser indicus are one such example, fl ying ranges experience changes in altitude, barometric pressure, across the Himalayas during their biannual migration, variable wind speeds and directions, decreasing air tempera- making vertical climbs up to 0.6 m s – 1 in excess of 5000 m ture and reduced humidity (Altshuler and Dudley 2006). In altitude (Hawkes et al. 2011, 2012). hypobaric air, the reduced air density leads to a reduction In order to sustain fl ights at high altitude, bar-headed in lift and increases the energetic cost of fl ying (although geese have evolved a number of physiological (Scott and there is a reduction in drag (Pennycuick 2008)). Th ere is Milsom 2007), morphological (Scott 2011) and biochemi- also a reduction in oxygen available (hypoxia) to fuel aero- cal adaptions (Jessen et al. 1991, Liang et al. 2001, Weber bic metabolism. During fl apping fl ight in a wind tunnel, 2007). Other avian species resident at high altitude have birds have been found to consume up to 10 – 12 times more adaptations such as haemoglobin conferring a higher affi nity oxygen than at rest (Ward et al. 2002) thus birds that fl y to oxygen than their low altitude counterparts (McCracken over mountain ranges must meet the challenge of maintain- et al. 2009, Galen et al. 2015) or greater muscle aerobic ing adequate oxygen supply to sustain long-distance fl ights capacity (Dawson et al. 2016). (Butler 2016). Birds have also been shown to use behavioural strate- Due to a number of pre-adaptations, birds have been gies to minimise energy expenditure during high altitude shown to have an inherently higher tolerance to hypoxia migrations. For example, bar-headed geese take a less ener- than mammals (Faraci 1991). For example, a house sparrow getically costly route across the Himalayas by tracking the Passer domesticus was able to maintain fl ight at a simulated terrain beneath them, rather than fl ying at higher altitudes altitude of 6100 m, whilst the same lack of oxygen avail- (Hawkes et al. 2012, Bishop et al. 2015). In addition bird ability rendered a mouse comatose (Tucker 1968). However, fl ight has often been found to be supported by favourable amongst avifauna there is a breadth in the extent of hypoxia wind conditions. For example, frigate birds Fregata minor EV-1 rise in thermals and then glide to minimise energy expendi- with a mean maximum altitude of 5590 m (range of means ture (Weimerskirch et al. 2016), and wandering albatrosses 4755 – 6800 m; Fig. 2). On average, ducks fl ew 547 m above Diomedea exulans maintain fl ight with heart rates little higher the ground during migration (grand mean value, range of than resting, when fl ying in tail winds (Weimerskirch et al. means 158 – 947 m). Shelducks travelled at a median speed 2000). Other birds optimise departure times to maximise of 13.7 m s – 1 (range 0.2 – 28.0 m s – 1 ), fl ying signifi cantly tail wind support (Hedenstrom et al. 2002, Gr ö nroos et al. faster at higher altitudes (12.44 m s – 1 below 4500 m, 14.55 2012, Gill et al. 2014, Kogure et al. 2016). m s – 1 above 4500 m, Wilcoxon W ϭ 7599, p ϭ 0.001, Fig. Given the presence of other species of waterfowl sharing 3). Climb rates decreased with altitude (0.24 m s – 1 below wintering and breeding grounds with bar-headed geese 4500 m, 0.18 m s – 1 above 4500 m Wilcoxon W ϭ 1229.5, (Prins and Namgail 2017) it seems reasonable to predict p ϭ 0.03). that there may be other Himalayan birds that have similar During the climb onto the Tibetan Plateau, movement capacities for fl ight at high altitude (Prosser et al. 2011). paths narrowed into a ‘ corridor ’ approximately 250 km Th is may include cranes and ducks, which satellite tracking wide where previously they had been more dispersed (up and ringing data suggest are likely to migrate in this area, to 450 km apart). Ruddy shelduck climbed from India however maximum fl ight altitudes have not been reported and Myanmar onto the Tibetan Plateau at mean maximum (Walkinshaw 1973, Hoyo et al. 1992, Higuchi et al. 1998, ascent rate of 0.45 m s – 1 (range 0.23 – 0.74 m s – 1 ). Th ere 2004, Qian et al. 2009). was no signifi cant diel pattern in the timing of climbing Th e ruddy shelduck Tadorna ferruginea ranges from east- fl ights (Rayleigh R ϭ 0.104, p ϭ 0.35); however, level ern Asia to south-eastern Europe and into northern Africa in (non-climbing) fl ight was more likely to take place ear- lower numbers (Birdlife International 2016 < www.birdlife. lier in the day (Rayleigh R ϭ 0.23, p Ͻ 0.01) and timings org/ > ). Within the larger Asian population, sub populations for fl ights signifi cantly diff ered to stationary locations; ϭ ϭ winter in lowlands in southern China, India and Myanmar t17 – 3.8, p 0.001 (Supplementary material Appendix and use breeding grounds on the Tibetan Plateau, thus cross- 1 Fig. A4). ing the Himalayas en route (Gaidet et al. 2010, Namgail et al. 2011, Nouidjem et al. 2015). Th ese subpopulations Ground elevation might therefore be predicted to potentially display relatively advanced adaptions for high altitude fl ight. Th e ground elevation under each shelduck location was In this study we describe the maximum altitudes and determined by overlaying GPS locations on a Digital climb rates of ruddy shelducks as they crossed the Himalayas and Tibetan Plateau. We hypothesise that ruddy shelduck: 1) are able to support climb rates in excess of 0.3 m s – 1 and sustain fl ight in hypoxic conditions at altitudes Ͼ 5000 m; and 2) employ a fl ight strategy to minimise energy, fl ying at optimal times of day, gaining support from wind condi- tions and selecting routes of the lowest fl ight altitudes. Th is study presents the fi rst data on the fl ight performance of any species other than bar-headed geese at altitudes above the Tibetan Plateau, and the fi rst evidence of extreme high alti- tude fl ight in a bird of this size. Methods and results General tracking Ruddy shelduck were captured in China (n ϭ 26), and India (n ϭ 4), sexed, aged, weighed, and GPS tracked with a Microwave Telemetry (Columbia, MD, USA) PTT-100 solar-powered Argos/GPS platform transmitter terminal (PTT) attached using a tefl on backpack harness. Tracking data were obtained from the Argos System ( < www.argos- system.org/en > ). More details of tracking and analysis can be found in the Supplementary material Appendix 1. Ducks migrating northwards from India or Myanmar travelled 1418 km (median value, range 548 – 2671 km) in 24 d (range 2 – 65 d) (Fig.
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