Abstract
In comparison to other behaviours, large predators expend relatively large amounts of energy foraging for prey, based on expected high return. Documenting how they manage costs and benefits of feeding is difficult, particularly for marine predators. In July and August of 2004 and 2005, we combined animal-borne video, accelerometry and depth sensors to examine the underwater behaviour during white shark (Carcharodon carcharias) breaching at Seal Island, South Africa (34.1373°S, 18.5825°E)—where sharks launch from the water while attacking Cape fur seals (Arctocephalus pusillus pusillus). We show that breaching begins at depths up to 20 m, is characterised by a brief (~ 7 to 16 s) ascent to the surface during which pitch angle increases by ~ 30° and both tail-beat frequency and swim speed (determined using biomechanical principles) increase by a maximum of 6.5-fold (0.39–2.50 Hz and 1.0–6.5 m s−1, respectively). Sharks also demonstrated the ability to rapidly adjust their approach to the seal during ascent. Dominant tail-beat frequency during breaching was 2.1–4.2 times higher (0.83–1.67 Hz) than during non-predatory ascents (0.4 Hz), suggestive of the large increase in power required to breach. Examination of foraging behaviour through biologger deployments may play an increasingly important role in predicting the resource requirements of large predators and developing appropriate conservation measures, as their populations are generally under threat world-wide.


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References
Aguilar Soto N, Johnson MP, Madsen PT, Díaz F, Domínguez I, Brito A, Tyack P (2008) Cheetahs of the deep sea: deep foraging sprints in short-finned pilot whales off Tenerife (Canary Islands). J Anim Ecol 77:936–947
Beutler FJ (1966) Error-free recovery of signals from irregularly spaced samples. SIAM Rev 8:328–335
Bruce BD (2008) White sharks: the biology and ecology of Carcharodon carcharias. In: Pikitch E, Babcock EA, Camhi MD (eds) Sharks of the open ocean. Blackwell, Oxford, pp 69–81
Brunnschweiler JM (2005) Water-escape velocities in jumping blacktip sharks. J R Soc Interface 2:389–391
Carey FG, Kanwisher JW, Brazier O, Gabrielson G, Casey JG, Pratt HL (1982) Temperature and activities of a white shark Carcharodon carcharias. Copeia 1982:254–260
Castro JI (2012) A summary of observations on the maximum size attained by the white shark, Carcharodon carcharias. In: Domeier ML (ed) Global perspectives on the biology and life history of the white shark. CRC Press, Boca Raton, pp 85–90
Chapple TK, Gleiss AC, Jewell OJ, Wikelski M, Block BA (2015) Tracking sharks without teeth: a non-invasive rigid tag attachment for large predatory sharks. Anim Biotelem 3:14. https://doi.org/10.1186/s40317-015-0044-9
Cooke SJ, Brownscombe JW, Raby GD, Broell F, Hinch SG, Clark TD, Semmens JM (2016) Remote bioenergetics measurements in wild fish: opportunities and challenges. Comp Biochem Physiol A Physiol 202:23–37
Dickson KA (1995) Unique adaptations of the metabolic biochemistry of tunas and billfishes for life in the pelagic environment. Environ Biol Fishes 42:65–97
Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair ARE, Soule ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet earth. Science 333:301–306
Graham JB, Dewar H, Lai NC, Lowell WR, Arce SM (1990) Aspects of shark swimming performance determined using a large water tunnel. J Exp Biol 151:175–192
Gruber SH, Cohen JL (1985) Visual system of the white shark, Carcharodon carcharias, with emphasis on retinal structure. Mem South Calif Acad Sci 9:61–72
Huveneers C, Watanabe YY, Payne NL, Semmens JM (2018) Interacting with wildlife tourism increases activity levels of white sharks. Conserv Physiol. https://doi.org/10.1093/conphys/coy019
Johnston EM, Halsey LG, Payne NL, Kock AA, Iosilevskii G, Whelan B, Houghton JDR (2019) Latent power of basking sharks revealed by exceptional breaching events. Biol Lett. https://doi.org/10.1098/rsbl.2018.0537
Kawatsu S, Sato K, Watanabe Y, Hyodo S, Breves JP, Fox BK, Grau EG, Miyazaki N (2010) A new method to calibrate attachment angles of data loggers in swimming sharks. EURASIP J Adv Signal Process 2010:12
Klimley AP, Le Boeuf BJ, Cantara KM, Richert JE, Davis SF, Van Sommeran S, Kelly JT (2001) The hunting strategy of white sharks (Carcharodon carcharias) near a seal colony. Mar Biol 138:617–636
Laroche RK, Kock AA, Dill LM, Oosthuizen WH (2008) Running the gauntlet: a predator–prey game between sharks and two age classes of seals. Anim Behav 76:1901–1917
Lowe CG, Goldman KJ (2001) Thermal and bioenergetics of elasmobranchs: bridging the gap. In: Tricas TC, Gruber SH (eds) The behavior and sensory biology of elasmobranch fishes: an anthology in memory of Donald Richard Nelson. Springer, Dordrecht, pp 251–266
Martin RA, Hammerschlag N (2012) Marine predator–prey contests: ambush and speed versus vigilance and agility. Mar Biol Res 8:90–94
Martin RA, Hammerschlag N, Collier RS, Fallows C (2005) Predatory behaviour of white sharks (Carcharodon carcharias) at Seal Island, South Africa. J Mar Biol Assoc UK 85:1121–1135
Martin RA, Rossmo DK, Hammerschlag N (2009) Hunting patterns and geographic profiling of white shark predation. J Zool 279:111–118
Moll RJ, Millspaugh JJ, Beringer J, Sartwell J, He Z (2007) A new ‘view’ of ecology and conservation through animal–borne video systems. Trends Ecol Evolut 22:660–668
Mollet HF, Cailliet GM (1996) Using allometry to predict body mass from linear measurements of the white shark. In: Klimley AP, Ainley DG (eds) Great white sharks the biology of Carcharodon carcharias. Academic Press, New York, pp 81–89
Mori T, Miyata N, Aoyama J, Niizuma Y, Sato K (2015) Estimation of metabolic rate from activity measured by recorders deployed on Japanese sea bass Lateolabrax japonicus. Fish Sci 81:871–882
Nakamura I, Watanabe YY, Papastamatiou YP, Sato K, Meyer CG (2011) Yo-yo vertical movements suggest a foraging strategy for tiger sharks Galeocerdo cuvier. Mar Ecol Prog Ser 424:237–246
Nakamura I, Goto Y, Sato K (2015) Ocean sunfish rewarm at the surface after deep excursions to forage for siphonophores. J Anim Ecol 84:590–603
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Roever C (2015) bspec: Bayesian spectral inference. R package version 1:5
Rutz C, Hays GC (2009) New frontiers in biologging science. Biol Lett 5:289–292. https://doi.org/10.1098/rsbl.2009.0089
Sakamoto KQ, Sato K, Ishizuka M, Watanuki Y, Takahashi A, Daunt F, Wanless S (2009) Can ethograms be automatically generated using body acceleration data from free-ranging birds? PLoS One 4:e5379. https://doi.org/10.1371/journal.pone.0005379
Sato K, Mitani Y, Cameron MF, Siniff DB, Naito Y (2003) Factors affecting stroking patterns and body angle in diving Weddell seals under natural conditions. J Exp Biol 206:1461–1470
Sato K, Watanuki Y, Takahashi A, Miller PJO, Tanaka H, Kawabe R, Ponganis PJ, Handrich Y, Akamatsu T, Watanabe Y, Mitani Y, Costa DP, Bost C-A, Aoki K, Amano M, Trathan P, Shapiro A, Naito Y (2007) Stroke frequency, but not swimming speed, is related to body size in free-ranging seabirds, pinnipeds and cetaceans. Proc R Soc Lond B Biol Sci 274:471–477
Steinhausen MF, Steffensen JF, Andersen NG (2005) Tail beat frequency as a predictor of swimming speed and oxygen consumption of saithe (Pollachius virens) and whiting (Merlangius merlangus) during forced swimming. Mar Biol 148:197–204
Strong WR Jr (1996) Shape discrimination and visual predatory tactics in white sharks. In: Klimley AP, Ainley DG (eds) Great white sharks the biology of Carcharodon carcharias. Academic Press, New York, pp 229–240
Tanaka H, Takagi Y, Naito Y (2001) Swimming speeds and buoyancy compensation of migrating adult chum salmon Oncorhynchus keta revealed by speed/depth/acceleration data logger. J Exp Biol 204:3895–3904
Thomson KS, Dan ES (1977) Body form and locomotion in sharks. Am Zool 17:343–354
Towner AV, Leos-Barajas V, Langrock R, Schick RS, Smale MJ, Kaschke T, Jewell OJD, Papastamatiou YP (2016) Sex-specific and individual preferences for hunting strategies in white sharks. Funct Ecol 30:1397–1407
Wardle CS (1975) Limit of fish swimming speed. Nature 255:725–727
Wardle CS, Videler JJ (1980) How do fish break the speed limit? Nature 284:445–447
Watanabe YY, Takahashi A (2013) Linking animal-borne video to accelerometers reveals prey capture variability. Proc Natl Acad Sci USA 110:2199–2204
Watanabe YY, Payne NL, Semmens JM, Fox A, Huveneers C (2019a) Hunting behaviour of white sharks recorded by animal-borne accelerometers and cameras. Mar Ecol Prog Ser. https://doi.org/10.3354/meps12981
Watanabe YY, Payne NL, Semmens JM, Fox A, Huveneers C (2019b) Swimming strategies and energetics of endothermic white sharks during foraging. J Exp Biol. https://doi.org/10.1242/jeb.185603
Webb PW, Keyes RS (1982) Swimming kinematics of sharks. Fish Bull 80:803–812
Welch PD (1967) The use of fast Fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms. IEEE Trans Audio Electroacoust 15:70–73
Williams TM, Wolfe L, Davis T, Kendall T, Richter B, Wang Y, Bryce C, Elkaim GH, Wilmers CC (2014) Instantaneous energetics of puma kills reveal advantage of felid sneak attacks. Science 346:81–85
Yoda K, Naito Y, Sato K, Takahashi A, Nishikawa J, Ropert-Coudert Y, Kurita M, Le Maho Y (2001) A new technique for monitoring the behaviour of free-ranging Adelie penguins. J Exp Biol 204:685–690
Acknowledgements
We thank G. Wilhelm (National Geographic) for clamp design, G. Marshall, K. Abernathy, P. Greene and M. Thorpe (National Geographic) for logistical support, L. Best for logging the footage and the South African Navy (Simonstown) for providing free harbour facilities for the research vessel. The following people are thanked for their help during fieldwork: K. Laroche, M. Hardenberg, A. de Vos, A. Casagrande, T. Lodge and numerous volunteers. We also thank Pete Klimley and an anonymous reviewer for improving this manuscript. This work was supported by a South African National Research Foundation Bursary (to A.A.K.); SEAChange Programme funding (to A.A.K.); Save Our Seas Foundation funding (to A.A.K.); Japan Society for Promotion of Science Invitational Fellowships for Research in Japan (S13196 & L15560 to J.M.S.) and a National Institute of Polar Research (Japan) Visiting Professorship (to J.M.S.).
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Crittercam attachment and biologging methodology was approved by the South African Department of Environmental Affairs, Oceans and Coasts permitting authority and carried out in accordance with the approved guidelines described in permits V1/1/5/1 and V1/8/5/1.
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Supplementary video 1. Animal-borne video of a white shark Carcharodon carcharias preparing to breach on a Cape fur seal Arctocephalus pusillus pusillus at Seal Island, South Africa. (MOV 13135 kb)
227_2019_3542_MOESM2_ESM.mov (download MOV )
Supplementary video 2. Animal-borne video of a white shark Carcharodon carcharias chasing a Cape fur seal Arctocephalus pusillus pusillus horizontally near the surface at Seal Island, South Africa. (MOV 4852 kb)
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Semmens, J.M., Kock, A.A., Watanabe, Y.Y. et al. Preparing to launch: biologging reveals the dynamics of white shark breaching behaviour. Mar Biol 166, 95 (2019). https://doi.org/10.1007/s00227-019-3542-0
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DOI: https://doi.org/10.1007/s00227-019-3542-0


