High Altitude Fl Ights by Ruddy Shelduck Tadorna Ferruginea During Trans

Home , Ruddy shelduck

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 t 17 – 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 conditions 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 altitude 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. 1). When moving southwards ducks travelled 1238 km from breeding grounds in China and Mongolia (range 548– 2689 km) in six days (range Figure 1. Map showing the routes of north bound migrations of 15 2 – 98 d, Supplementary material Appendix 1 Table A1). ruddy shelduck recorded in 2009; tracks are indicated by dashed During migrations, ruddy shelduck ﬂ ew at 3349 m alti- lines. White circles indicate the deployment locations in China and tude (grand mean value, range of means 1943– 4686 m), India. Black circles indicate the start and termination of each track.

EV-2 their corresponding ground elevations used as a null model. Ruddy shelduck fl ew over signifi cantly lower ground elevations than the null models throughout their fl ight path ϭ Ͻ (paired t-test, t14 – 5.115, p 0.001). For example, 19% of shelduck locations were over ground higher than 4500 m compared with 33% in the null model (Fig. 4).

Wind conditions

Weather data (global ECMWF Interim Reanalysis pack- age ‘ ERA, interim ’ (Dee et al. 2011)) were extracted for each duck location to calculate wind speed and direction. Th ere was no signifi cant diff erence in wind speed between the time of migratory departure from the breeding area and ϭ ϭ the two week average (t6 0.86, p 0.4) but winds were signifi cantly calmer (lower) when departing the wintering ϭ ϭ area (t 8 – 4.36, p 0.0025) (Supplementary material Appendix 1 Fig. A5). Likewise, wind direction (south westerly (r ϭ 0.72, p ϭ 0.01)) was not signifi cantly diff erent at departure from the two week averages for the breed- ϭ ϭ ing (t6 – 0.83, p 0.43) or wintering grounds (Rayleigh ϭ ϭ ϭ ϭ R 0.29, p 4.7, t9 – 0.3, p 0.76). Th ree of the seven ducks departed breeding areas into a head wind, whereas wintering ducks took off into cross winds or calmer head winds. Figure 2. (a) Plot showing ground elevation (smoothed with spline) Ducks experienced assisting winds 41% of the time across the latitudes crossed by the north bound ruddy shelduck Ͻ whose positions are shown in black. Black vertical lines indicate the (the air-distance to ground-distance ratio (AGR) was 1 ; boundaries of the Tibetan Plateau. (b) Histogram showing fre- Gill et al. 2014) with 20% of locations during tailwinds quency of altitudes (above sea level) for migrating ruddy shelduck. and 25% in headwinds. Ducks generally did not appear to Dotted line indicates mean maximum altitude. align their fl ights with the most profi table prevailing wind conditions. For example, in 98.9% of fl ights, the ducks Elevation Model (DEM). Following on from (Hawkes et al. could have gained better wind assistances if they had fl own 2012), random locations were generated within a polygon at a diff erent altitude. Likewise, fl ights took place during that bounded all locations from each individual duck and time periods with the most optimal tail winds only 1.6% of the time relative to a six day period centred on individual in-fl ight locations (Supplementary material Appendix 1 Fig. A2).

Data deposition

Data available from Movebank Digital Repository, Movebank data IDs: 3291880 and 3291898.

Discussion

In this study we have demonstrated that ruddy shelduck fl y up to 6800 m altitude, but more commonly remain below 5590 m (with 95% of locations at altitudes less than 5423 m). Shelduck climbed, at their steepest, faster than bar-headed geese (0.6 m s – 1 (Hawkes et al. 2011)) but more slowly above 4500 m, refl ecting the increase in fl ight power required with increasing altitude (Hedenströ m and Alerstam 1992). Level fl ight was faster at higher altitudes, consistent with predictions from fl ight biomechanical theory, given the reduction in both drag and lift with increasing altitude (Schmaljohann and Liechti 2009). Figure 3. Boxplots showing fl ight speeds of ruddy shelduck (median speed shown as horizontal black line, interquartile range shown by It is perhaps surprising that ruddy shelduck did not fl y in the grey box, range of fl ight speeds indicated by the extent of the specifi c wind speeds or directions during migratory fl ights dotted grey lines) migrating (a) north and (b) south across the or climbs (Supplementary material Appendix 1 Fig. A3). It Tibetan Plateau, in 500 m elevation bins. is possible that the wind speeds in the area were too low

EV-3 Figure 4. Ruddy shelduck in-fl ight GPS locations (white circles) (a) across the Tibetan Plateau and (b) zoomed into the area where most northbound climbs occurred (mean ground elevation in bounding box is 4055 m). Background grey shading shows ground elevation (from SRTM Digital Elevation Model) with red highlighting terrain over 4500 m. to infl uence the bird ’ s behaviour with birds preferring to In order to carry out sustained climbs at the speeds fl y in weaker cross or head winds in order to avoid strong described here suggests that ruddy shelduck may have physi- winds and increased turbulence (Erni et al. 2002, Prins and ological adaptations for high altitude fl ight that remains to Namgail 2017). Indeed our evidence suggests that shelduck be investigated. It is not yet known if other high altitude take off most often into weak head winds at the wintering migrant species share the same cardiorespiratory adapta- grounds. However, these fi ndings should be interpreted with tions to hypoxia as the bar-headed goose (Lague et al. 2016). caution as we note that the resolution of the meteorologi- Understanding what adaptations to hypoxia have been cal data was relatively coarse (six hour intervals on a 0.75 conserved across species will allow us to identify physiologi- degree resolution spatial grid) in comparison to shelduck cal changes that are most adaptive for high altitude fl ight. movements (i.e. ∼ 18.6 m s – 1 ), and can only be selected as one of 17 altitudinal bands. In addition, the confounding infl uences of the region’ s high topographic diversity, and the Acknowledgements – We thank Graham Scott and Eli Bridge, for comments to early drafts, and Th omas Alerstam and two anony- two-hour temporal resolution of the ruddy shelduck track- mous reviewers for comments that signifi cantly improved the man- ing data, meant we were not able to explore the role of winds uscript. For logistics and fi eldwork, we are grateful to the following to the level of detail on which they may be experienced by groups and individuals: China – the Qinghai Lake National Nature the ducks. Reserve staff (Zhi Xing, Dehai Zhang), Qinghai Forestry Bureau Our results suggest that ruddy shelduck select an opti- (San Dan Li), Chinese Academy of Sciences (Baoping Yan), and mum fl yway, lower (mean ground elevation 2710 m) on U.S. Geological Survey (Bridget Collins, Eric Palm, Shane Heath, average than the Tibetan Plateau (4800 m) and take a more Sabir Bin Muzaff ar). Th e use of trade, fi rm, or product names in circuitous route to avoid peaks, thus traveling further than this publication is for descriptive purposes only and does not imply endorsement by the U.S. Government. For advice and guidance the great circle distance. Th ey may also use formation fl ight using R, NP is grateful to James Phillip Duff y and Bethany Clark (Portugal et al. 2014) but we were not able to demonstrate (Univ. of Exeter). Th e views expressed in this publication are those this behaviour with a small sample size. of the author(s) and do not necessarily refl ect the views or policies Ruddy shelduck wintering further east in India may fl y of the Food and Agriculture Organization of the United Nations. even higher or climb even faster than the ducks from Myan- mar in the present study, given the higher terrain that lies north of India, along with Eurasian wigeon Anas penelope , References gadwall Anas strepera, northern pintail Anas acuta and northern shoveler Anas clypeata that winter and breed either side Altshuler, D. and Dudley, R. 2006. Th e physiology and biome- chanics of avian fl ight at high altitude. – Integr. Comp. Biol. of the Himalayas (Prins and Namgail 2017). Future studies 46: 62 – 71. should aim to collect empirical data on the altitudes reached Bishop, C. M., Hawkes, L. A., Chua, B., Frappell, P. B., Milsom, by these birds to greater understand the breadth of altitude W. K., Natsagdorj, T., Newman, S. H., Scott, G. R., Takekawa, adaptation. J. Y., Wikelski, M. and Butler, P. J. 2015. Th e roller coaster

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Supplementary material (Appendix JAV-01443 at < www. avianbiology.org/appendix/jav-01443 > ). Appendix 1.

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