Ornithol Sci 16: 17 – 22 (2017)

SPECIAL FEATURE The effects of weather conditions on avian movements Effect of wind on the ight of Brown edglings

Takashi YAMAMOTO1,#, Hiroyoshi KOHNO2, Akira MIZUTANI2, Hanako SATO3, Hiroki YAMAGISHI3, Yutaka FUJII3, Miku MURAKOSHI4 and Ken YODA1

1 Graduate School of Environmental Studies, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464–8601, Japan 2 Okinawa Regional Research Center, Tokai University, Uehara, Taketomi, Okinawa 907–1541, Japan 3 School of Marine Science and Technology, Tokai University, Orido, Shimizu-ku, Shizuoka 424–8610, Japan 4 Nagasaki Penguin Aquarium, Shuku-machi, Nagasaki 851–0121, Japan

ORNITHOLOGICAL Abstract There is increasing evidence showing that wind velocity affects the flight and foraging behavior of ; however, few studies have examined these effects SCIENCE on seabirds inhabiting tropical oceans where lighter wind conditions usually prevail. © The Ornithological Society The Brown Booby Sula leucogaster is an example of a tropical with relatively of Japan 2017 low wing loading; strong wind conditions may be expected to impede the stability of their flight. We examined how different wind conditions affected the duration and flying behavior of Brown Booby fledglings during foraging trips by means of direct observation of nest attendance and by attaching video loggers to . The duration of foraging trips by fledglings decreased with increasing wind speed, and during flight, the body rotation of fledglings became greater with increasing wind speed. As expected, fledglings were buffeted by strong winds due to their relative inexperience in flight combined with their low wing loading. Fledglings were probably forced to flap against strong winds in to adjust the stability of their bodies, offsetting the efficient use of wind for gliding. Furthermore, the height at which fledglings flew fluctuated more at higher wind velocities, which may have constrained their detection and capture of prey. In conclusion, our results indicate that the aerodynamic perfor- mance of Brown Booby fledglings is impaired by strong wind conditions, leading to poor flight stability and potentially reduced prey detection.

Key words Fledgling, Flight, Tropical seabird, Video logger, Wind

Seabirds are able to fly freely over barrier-free Previous studies into the effects of wind on the oceans; however, there is increasing evidence indi- flight of seabirds have mostly focused on cating that wind conditions (e.g., speed and direc- inhabiting relatively windy areas at high latitudes tion) influence their flight and foraging behavior at (e.g., albatrosses). Most of these species have high sea (Finney et al. 1999; González-Solís et al. 2009; wing loading (i.e., a small wing area relative to mass), Dehnhard et al. 2013; Elliott et al. 2014; Tarroux et and often perform a special flight maneuver called al. 2016). Prevalent wind patterns have been found “dynamic soaring” (i.e., using wind shears in the to determine the timing and direction of foraging boundary layer above the ocean surface; Sachs 2005) excursions by a range of different seabirds including to utilize strong winds. Thus, such species actually , petrels, shearwaters and albatrosses (Adams need higher wind velocities to remain aloft without & Navarro 2005; Garthe et al. 2007; Navarro & flapping (Weimerskirch et al. 2000; Amélineau et al. González-Solís 2009; Weimerskirch et al. 2012), with 2014). However, the flight style of birds is thought individuals taking advantage of favorable winds to to be adaptive, matching the effectiveness of their minimize their energetic expenditure during flight morphological characteristics to the wind regimes (Furness & Bryant 1996; Weimerskirch et al. 2000; of the regions they inhabit (Spear & Ainley 1997; Amélineau et al. 2014). Weimerskirch et al. 2005; Cairns et al. 2008). Winds over tropical oceans are typically much lighter (i.e., (Received 7 July 2016; Accepted 27 September 2016) less wind speed) than winds at higher latitudes # Corresponding author, E-mail: [email protected] (Suryan et al. 2008); furthermore, species inhabiting

17 T. YAMAMOTO et al. tropical regions appear to have relatively lower wing gate siblicide: Nelson 1978; Drummond et al. 2003). loadings (Spear & Ainley 1997), which is considered As part of a restoration program (Mizutani & Kohno to be an adaptation to exploit lighter winds (Hertel 2011), we transferred a total of 17 chicks of unknown & Ballance 1999; Brewer & Hertel 2007). Therefore, sexes that were abandoned by their parents to the tropical seabirds should be better adapted to weak ORRC during the study period, and raised them until wind conditions, which might determine their distri- they reached independence (see Yoda et al. 2004 butions (Cairns et al. 2008; Suryan et al. 2008). for more detailed information on our hand-raising The Brown Booby Sula leucogaster breeds in methods). This project has provided us with a unique subtropical and tropical oceans between 25°S and opportunity to understand the fledgling behavior and 25°N latitude (often termed the “pantropical” region) ecology of this species (Yoda et al. 2004; Kohno & (Harrison 1985; Nelson 2005). The species also Yoda 2011; Yoda et al. 2011). In the years follow- breeds in Japan. The colony breeding on Nakanoka- ing fledgling independence, one juvenile has been mishima Island, Japan, is close to the northern limit observed to return to the area where it was reared. of the species’ breeding range, located to the north After the chicks had fledged (i.e., the post-fledging of the Tropic of Cancer. This region is characterized dependence period), their cages were opened at sun- by seasonal changes in wind speed. Calm weather rise and closed at sunset, allowing them to make trips conditions prevail from spring to summer, but strong to and from the sea throughout the daytime. During northeasterly winds caused by the East Asian winter the period between fledging and independence, we Monsoon prevail from November to February (Zhang observed fledglings and recorded the attendance of et al. 1997; Ikema et al. 2013). migrate to their nest in 2005, 2006, 2008, 2009, and 2010 (N=13 the south of the Philippine Islands, located 1,000– birds) to quantify the time spent at sea (i.e., forag- 2,000 km away from their natal colony, usually by ing trip duration). In 2009, 2010, and 2011, we also November. This migratory behavior is assumed to attached video loggers (LY30, 1.9 cm×6.8 cm×1.9 be triggered by an increase in wind speed (Kohno cm in diameter, Benco, Taiwan) to 10 birds. In brief, 2000). However, the effects of wind conditions on the we first attached small plastic bases to the back feath- behavior of this species at sea remain poorly under- ers of fledglings with adhesive tape (Tesa, Hamburg, stood. Germany) and glue (Loctite 401). We then attached In this study, we examined how different wind the video loggers to the bases using cable ties. This conditions affected the duration and flying behav- technique allowed us to collect video footage repeat- ior of Brown Booby fledglings during foraging trips edly throughout the study period (Fig. 1a). The video through the direct observation of nest attendance and lens faced forward to provide a ’s eye view of the attachment of video loggers to birds. the environment. Each video logger had a 280 mAh Li-polymer battery and 4 GB of memory, and could record for up to three hours. We deployed the loggers MATERIALS AND METHODS once or twice each day, and retrieved them on the 1) Fieldwork same day. We then downloaded the video footage to This study was carried out on Nakanokamishima a computer. The total weight of each logger including Island, Japan (24°11′N, 123°34′E), and at the Okinawa the cable ties (27 g) corresponded to less than 2% Regional Research Center (ORRC), Tokai Univer- of the mean mass of the equipped birds (mean±SD: sity, Iriomote Island (24°19′N, 123°41′E) from May 1,361±163 g). Previous studies have recommended to December in 2005, 2006, 2008, 2009, 2010, and that loads exceeding >5% of body mass should be 2011. Birds on Nakanokamishima Island have been avoided for flying seabirds (e.g., Phillips et al. 2003). disturbed since 1906 by human activities, including commercial hunting for feathers, specimens, and oil 2) Data analysis (Mizutani & Kohno 2011). These actions led to a The video footage was used to extract scenes dur- major decline in population size to ca. <200 breeding ing which the fledglings flew linearly and the sea pairs (Hiroyoshi Kohno unpublished). Each Brown horizon was visible (Fig. 1b, also see Appendix for Booby lays two eggs, both of which hatch. However, an example). We then measured the roll angles of the one of the chicks (usually the first one to hatch) rou- body axis (i.e., transversely crossing the body from tinely kills its sibling by pushing it out of the nest right to left) for each second in relation to the horizon within a few days of the second chick hatching (obli- using protractor software (available at http://www.

18 Eff ect of wind on the fl ight of Brown Booby fl edglings

was examined in relation to 10-min means of wind (a) Photo by H Yamagishi direction and speed data corresponding to the time when each fl ight scene was recorded. Wind direction, relative to the bird’s heading, was separated into two categories: head wind and tail wind. These criteria were selected because, although the broad direction in which the birds were heading was detectable using the geomorphic characteristics of Iriomote Island, the exact direction that birds headed was not clear. Data were analyzed using R version 2.15.1 (R Development Core Team 2012). As fledglings increased the time spent at sea and developed their fl ight skills gradually towards independence (Yoda et al. 2004; Kohno & Yoda 2011), we calculated (b) anomalies in trip durations (i.e., each trip duration was subtracted from the mean trip duration for the corresponding age). The eff ects of daily wind speed on trip duration were examined using generalized lin- ear mixed models (GLMM) using Gaussian distribu- tion and bird identity as a random factor. The eff ects of wind direction and speed on the body rotation and gliding ratio were examined using GLMM with Gaussian distribution, including the days since fl edg- ing and bird identity as random factors. The model fi t (R2) for GLMM was calculated following the method Fig. 1. A fl edgling Brown Booby fi tted with a video logger described by Nakagawa and Schielzeth (2013). We (a), and an example of video footage and the measurement of used R packages lme4 and arm. Values are presented the roll angle of the body axis during fl ight using the protrac- as mean±SD and the statistical signifi cance was set tor software (b). In this scene, the fl edgling rolled its body as P<0.05. axis 25° towards the right. RESULTS vector.co.jp/soft/winnt/util/se345469.html, accessed The fl edglings raised in this study became indepen- on 28 November 2016; Fig. 1b), and calculated the dent and successfully left the ORRC at 80±14 days standard deviation (SD) during each fl ight scene. (range 54–96 days) after fl edging (mean±SD date of In addition, we determined whether fl edglings were independence: 5 November±19 days; range: 8 Octo- fl apping (large camera shakes occurred) or gliding ber–20 December). During the post-fl edging depen- (stable footage or small shakes) (Yoda et al. 2011, dence period, the duration of foraging trips decreased also see Appendix), and calculated the proportion of as wind speed increased (GLMM, R2=0.22, P<0.01; glide during each fl ight. We determined the direction Fig. 2). of the bird’s heading using geomorphic characteris- Video cameras were attached multiple times to tics of Iriomote Island or the position of the sun in fl edglings from 12–75 days after fl edging (4–21 relation to the time of day. times per bird). We obtained 194 samples of video Wind data for the study region were obtained from footage (ca. 18 hours of data in total), from which we the Japan Metrological Agency (at the meteorologi- extracted 46 fl ight scenes to determine body rotation cal station of Iriomote: http://www.jma.go.jp/jma/, (mean recording duration of each scene was 3.7±2.5 accessed on 28 November 2016). Nest-based obser- min, 170 min total) and 81 scenes to determine the vations of trip durations were compared with daily gliding ratio (2.7±1.6 min, 253 min total). The birds mean wind speeds. The SD in the roll angle of the rolled more when experiencing high wind speeds in body axis (i.e., body rotation) and the proportion of both head winds (GLMM, R2=0.27, P<0.01) and tail time spent gliding during each fl ight (i.e., glide ratio) winds (R2=0.70, P<0.05) (Fig. 3; also see Appendix).

19 T. YAMAMOTO et al.

(a) 5 0 SD in roll angle (°) 5 01 51 02 52 Anomaly in trip duration (hour) 5 − 0 2 4 6 8 10 Wind speed (m/s) 2 4 6 8 10 12 Wind speed (m/s) (b) Fig. 2. Relationship between anomalies in trip durations (i.e., each trip duration was subtracted from the mean trip duration for the corresponding age) and daily mean wind speeds.

The gliding ratio was 36.8±8.7% (range 19–59%), and was not related to either wind direction or wind speed (GLMM, R2=0.33, P=0.64 for head wind and SD in roll angle (°) R2=0.33, P=0.44 for tailwind). 5 01 51 02 52

DISCUSSION 0 2 4 6 8 10 In this study, Brown Booby fledglings reduced Wind speed (m/s) the duration of their foraging trips as wind speed Fig. 3. Standard deviation (SD) in the roll angle of the body increased, probably to avoid encountering strong axis in relation to (a) head winds and (b) tail winds. Linear winds. Similar results have been obtained by previ- regressions estimated by generalized linear mixed models are ous studies on adult European Shags Phalacrocorax shown. aristotelis (Daunt et al. 2006; Lewis et al. 2015). During flight, the body rotation of Brown Booby tain body stability (Warrick & Dial 1998; Ainley et fledglings became greater as wind speed increased. al. 2015), offsetting any possible efficient use of wind Species with high wing loadings generally fly faster for gliding. Dynamic body acceleration is correlated to remain aloft (Alerstam 2007), reducing the effect with energy expenditure (Wilson et al. 2006; Elliott of turbulence by strong winds. In contrast, species et al. 2013); thus, flying in turbulence might incur inhabiting tropical oceans, including Brown Boo- extra energetic costs. Fledglings also exhibited fluc- bies, appear to have comparatively lower wing load- tuations in flight height when encountering higher ings (Spear & Ainley 1997; Hertel & Ballance 1999; wind velocities (see Appendix). The flight height Brewer & Hertel 2007; Suryan et al. 2008). This mor- of seabirds often increases with increasing wind phological characteristic is considered to be an adap- speed (Ainley et al. 2015). Pulses of strong winds tation for exploiting lighter winds, and so might not occur between wave crests, which allow seabirds be functionally stable under strong wind conditions. to climb high enough to extract wind energy and Fledglings might have also been buffeted by strong maintain flight speeds attained during down-swoops winds due to their lack of flight experience (Thorup (Pennycuick 2002). Although fast flight speeds are et al. 2003). As such, fledglings probably needed to preferable for commuting between a breeding colony flap frequently against strong winds in order to main- and the surrounding foraging areas, increased flight

20 Effect of wind on the flight of Brown Booby fledglings speed is expected to reduce a bird’s ability to detect seabird: flight patterns and movements of breeding prey (Spear & Ainley 1997; Ainley et al. 2015). Cape gannets Morus capensis. African J Mar Sci 27: This research showed that the aerodynamic per- 239–248. formance of juvenile Brown Boobies is potentially Ainley DG, Porzig E, Zajanc D & Spear LB (2015) Sea- impaired by strong wind conditions in terms of bird flight behavior and height in response to altered flight stability and prey detectability. These- nega wind strength and direction. Mar Ornithol 43: 25–36. tive impacts may explain why fledglings reduced the Alerstam T, Rosén M, Bäckman J, Ericson PGP & duration of their foraging trips on windy days. Alter- Hellgren O (2007) Flight speeds among bird species: natively, fledglings might reduce the trip duration Allometric and phylogenetic effects. PLOS Biol 5: on such days to reduce the risk of being drifted or e197. Amélineau F, Péron C, Lescroël A, Authier M, Provost becoming disoriented (Thorup et al. 2003). Further- P & Grémillet D (2014) Windscape and tortuosity more, strong winds and associated increased wave shape the flight costs of northern gannets. J Exp Biol action might reduce the ability of birds to see below 217: 876–885. the sea surface while flying above (Finney et al. 1999; Brewer ML & Hertel F (2007) Wing morphology and Dehnhard et al. 2013). Data on the flight dynamics of flight behavior of Pelecaniform seabirds. J Morphol adult Brown Boobies is required to allow comparison 268: 866–877. between experienced and inexperienced individuals. Cairns DK, Gaston AJ & Huettmann F (2008) Endo- For example, in contrast to fledglings, the foraging thermy, ectothermy and the global structure of marine trip duration of adults might become longer under vertebrate communities. Mar Ecol Prog Ser 356: strong wind conditions to capture sufficient prey to 239–250. meet greater energy demands due to the possible Daunt F, Afanasyev V, Silk JRD & Wanless S (2006) reduction in their foraging efficiency. Future studies Extrinsic and intrinsic determinants of winter forag- should focus therefore on how wind conditions affect ing and breeding phenology in a temperate seabird. the flight performance and foraging behavior of adult Behav Ecol Sociobiol 59: 381–388. Brown Boobies. Such research might improve our Dehnhard N, Ludynia K, Poisbleau M, Demongin L & understanding of how seasonal wind conditions (i.e., Quillfeldt P (2013) Good days, bad days: wind as a seasonality) influence the breeding phenology of this driver of foraging success in a flightless seabird, the tropical species. southern rockhopper penguin. PLOS ONE 8: e79487. Drummond H, Torres R & Krishnan VV (2003) Buff- ered development: resilience after aggressive subor- ACKNOWLEDGMENTS dination in infancy. Am Nat 161: 794–807. We thank K Sakihara (the staff of the ORRC, Elliott KH, Le Vaillant M, Kato A, Speakman JR & Tokai University) and Y Ikeda for providing logis- Ropert-Coudert Y (2013) Accelerometry predicts tic support in the field. We are also grateful for the daily energy expenditure in a bird with high activity levels. Biol Lett 9: 20120919. assistance of students who were undertaking research Elliott KH, Chivers LS, Bessey L, Gaston AJ, Hatch for their dissertations. NM Yamaguchi, K Shiomi, SA, Kato A et al. (2014) Windscapes shape seabird DM Kikuchi, and one anonymous reviewer provided instantaneous energy costs but adult behavior buffers valuable comments on the manuscript. This work impact on offspring. Mov Ecol 2: 17. was financially supported by grants from ORRC, the Finney SK, Wanless S & Harris MP (1999) The effect Japan Society for the Promotion of Science (JSPS) of weather conditions on the feeding behaviour of a Research Fellowship for Young Scientists (15J07507 diving bird, the Common Guillemot Uria aalge. J to T Yamamoto), and JSPS Grant-in-Aid for Scien- Avian Biol 30: 23–30. tific Research (20519002, 24681006 to K Yoda and Furness RW & Bryant DM (1996) Effect of wind on 18310153, 25281056 to H Kohno). This study was field metabolic rates of breeding northern fulmars. conducted with permits from the Ministry of the Ecology 77: 1181–1188. Environment, the Agency for Cultural Affairs, and Garthe S, Montevecchi WA & Davoren GK (2007) the Nature Conservation Division, Okinawa, Japan. Flight destinations and foraging behaviour of north- ern gannets (Sula bassana) preying on a small forage in a low-Arctic ecosystem. Deep-Sea Res II 54: REFERENCES 311–320. Adams NJ & Navarro RA (2005) Foraging of a coastal González-Solís J, Felicísimo A, Fox JW, Afanasyev V,

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Appendix. Examples of video footage that show a Brown Booby flying under different wind conditions (0.3 m/s in a head wind, 9.5 m/s in a head wind, and 8.6 m/s in a tail wind). Available at http://www.momo-p.com/index. php?movieid=momo161003sl01a&embed=on.

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