Abstract
Movements and habitat preferences of sharks relative to a central location are widely documented for many species; however, the reasons for such behaviors are currently unknown. Do movements vary spatially or temporally or between individuals? Do sharks have seasonal habitat and environmental preferences or simply perform movements at random at any time of the year? To help understand requirements for the designation of critical habitats for an endangered top predator and to develop zoning and management plans for key habitats, we examined vertical and horizontal movements, and determined habitat and environmental preferences of scalloped hammerhead sharks (Sphyrna lewini). We tracked seven hammerheads for 19–96 h at Wolf Island (1.38ºN, 91.82ºW) between 2007 and 2009 using ultrasonic transmitters with depth and temperature sensors, and we profiled temperature through the water column. Movements of individual hammerheads fell in two classes: constrained (remaining near the island) and dispersive (moving offshore to pelagic environments). The central activity space or kernel off the southeast side of Wolf Island was small and common to most, but the area varied among individuals (mean ± SE 0.25 ± 0.2 km2), not exceeding 0.6 km2 for any of the sharks, and not changing significantly between seasons. In general, hammerheads showed preference for the up-current habitat on the eastern side of Wolf Island in both the warm and cold seasons. However, the depth of sharks varied with season, apparently in response to seasonal changes in the vertical structure of temperature. Hammerheads performed frequent vertical excursions above the thermocline during offshore movements and, in general, were observed to prefer temperatures of 23–26 °C found above the thermocline. At times, though individuals moved into the thermocline and made brief dives below it. Our results provided evidence that hammerheads (1) are highly selective of location (i.e., habitat on up-current side of island) and depth (i.e., top of the thermocline) while refuging, where they may carry out essential activities such as cleaning and thermoregulation, and (2) perform exploratory vertical movements by diving the width of the mixed layer and occasionally diving below the thermocline while moving offshore, most likely for foraging.
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References
Arthur SM, Manly BFJ, McDonald LL, Garner GW (1996) Assessing habitat selection when availability changes. Ecology 77:215–227
Barton ED (2001) Turbulence and diffusion: island wakes. In: Steele J, Thorpe S, Turekian K (eds) Encyclopedia of ocean sciences I. Academic Press, London, pp 1397–1403
Bates D, Maechler M (2009): linear mixed-effects models using S4 classes. R Package Version 0.999375-32 http://cran.r-project.org/web/packages/lme4/
Bessudo S, Soler G, Klimley AP, Ketchum JT, Arauz R, Hearn A (2011) Residency of the scalloped hammerhead shark (Sphyrna lewini) at Malpelo Island and evidence of migration to other islands in the Eastern Tropical Pacific. Environ Biol Fishes 91:165–176
Beyer HL (2009) Geospatial modelling environment (version 0.3.3 Beta)
Block BA, Keen JE, Castillo B, Dewar H, Freund EV, Marcinek DJ, Brill RW, Farwell C (1997) Environmental preferences of yellowfin tuna (Thunnus albacares) at the northern extent of its range. Mar Biol 130:119–132
Boehlert GW, Watson W, Charles Sun L (1992) Horizontal and vertical distributions of larval fishes around an isolated oceanic island in the tropical Pacific. Deep-Sea Res 39:439–466
Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:2–28
Cartamil DP, Vaudo JJ, Lowe CG, Wetherbee BM, Holland KN (2003) Diel movement patterns of the Hawaiian stingray, Dasyatis lata: implications for ecological interactions between sympatric elasmobranch species. Mar Biol 142:841–847
Casey JG, Kohler NE (1990) Long distance movements of Atlantic sharks from the NMFS cooperative shark tagging program. In: Gruber SH (ed) Discovering sharks. Underwater Naturalist, Highlands, pp 87–91
Castañeda-Suárez JD, Sandoval-Londoño LJ (2007) Hábitos alimentarios del tiburón martillo, Sphyrna lewini (Griffith & Smith, 1834) en el Pacífico Ecuatoriano. In: Martínez-Ortiz J, Galvan-Magana F (eds) Tiburones en el Ecuador: casos de estudio. EPESPO-PMRC, Manta, pp 66–76
Chadwick B (2007) Galapagos bathymetry. http://www.pmel.noaa.gov/eoi/staff/chadwick/galapagos.html
Dawson CL, Starr RM (2009) Movements of subadult prickly sharks Echinorhinus cookei in the monterey canyon. Mar Ecol Prog Ser 386:253–262
Di Santo V, Bennett WA (2011) Is post-feeding thermotaxis advantageous in elasmobranch fishes? J Fish Biol 78:195–207
Economakis AE, Lobel PS (1998) Aggregation behavior of the grey reef shark, Carcharodon amblyrhynchos, at Johnston Atoll, Central Pacific Ocean. Environ Biol Fishes 51:129–139
Furukawa S, Kawabe R, Ohshimo S, Fujioka K, Nishihara GN, Tsuda Y, Aoshima T, Kanehara H, Nakata H (2011) Vertical movement of dolphinfish Coryphaena hippurus as recorded by acceleration data-loggers in the northern East China Sea. Environ Biol Fishes 92:89–99
Grubbs RD (2010) Ontogenetic shifts in movements and habitat use. In: Carrier J, Musick JA, Heithaus MR (eds) Sharks and their relatives II: biodiversity, adaptive physiology, and conservation. CRC Press, Boca Raton, pp 319–350
Hamilton WJ, Watt KE (1970) Refuging. In: Johnston RF, Frank PW, Michener CD (eds) Annu Rev Ecol Syst 1:263–287
Hearn A, Ketchum JT, Klimley AP, Espinoza E, Peñaherrera C (2010) Hotspots within hotspots? Hammerhead shark movements around Wolf Island, Galapagos Marine Reserve. Mar Biol 157:1899–1915
Heupel MR, Simpfendorfer CA, Hueter RE (2004) Estimation of shark home ranges using passive monitoring techniques. Environ Biol Fishes 71:135–142
Holland KN, Wetherbee BW, Peterson JD, Lowe CG (1993) Movements and distribution of hammerhead pups on their natal grounds. Copeia 1993:495–502
Hooge PN, Eichenlaub W, Solomon E (1999a) The animal movement program. USGS, Alaska Biological Science Center
Hooge PN, Eichenlaub WM, Solomon EK (1999b) Using GIS to analyze movements in the marine environment. Unpublished Report
Hopkins TE, Cech JJ (1994) Effect of temperature on oxygen consumption of the bat ray, Myliobatis californica (Chondrichthyes, Myliobatidae). Copeia 1994:529–532
Houvenaghel GT (1984) Oceanographic setting of the Galápagos Islands. In: Perry R (ed) Galapagos (key environments). Pergamont Press, Oxford, pp 43–54
Howey-Jordan LA, Brooks EJ, Abercrombie DL, Jordan LK, Brooks A, Williams S, Gospodarczyk E, Chapman DD (2013) Complex movements, philopatry and expanded depth range of a severely threatened pelagic shark, the oceanic whitetip (Carcharhinus longimanus) in the Western North Atlantic. PLoS ONE 8:e56588
Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource reference. Ecology 61:65–71
Jorgensen SJ, Klimley AP, Muhlia-Melo AF (2009) Scalloped hammerhead shark Sphyrna lewini, utilizes deep-water, hypoxic zone in the Gulf of California. J Fish Biol 74:1682–1687
Klimley AP (1987) The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environ Biol Fishes 18:27–40
Klimley AP (1993) Highly directional swimming by scalloped hammerhead sharks, Sphyrna lewini, and subsurface irradiance, temperature, bathymetry, and geomagnetic field. Mar Biol 117:1–22
Klimley AP, Butler SB (1988) Immigration and emigration of a pelagic fish assemblage to seamounts in the Gulf of California related to water mass movements using satellite imagery. Mar Ecol Prog Ser 49:11–20
Klimley AP, Nelson DR (1981) Schooling of the scalloped hammerhead shark, Sphyrna lewini, in the Gulf of California. Fish Bull 79:356–360
Klimley AP, Nelson DR (1984) Diel movement patterns of the scalloped hammerhead shark (Sphyrna lewini) in relation to El Bajo Espiritu Santo: a refuging central position social system. Behav Ecol Sociobiol 15:45–54
Klimley AP, Beavers SC, Curtis TH, Jorgensen SJ (2002) Movements and swimming behavior of three species of sharks in La Jolla Canyon, California. Environ Biol Fishes 63:117–135
Klimley AP, Kihslinger RL, Kelly JT (2005) Directional and non-directional movements of bat rays, Myliobatis californica, in Tomales Bay, California. Environ Biol Fishes 74:79–88
Lande R, Wood AM (1987) Suspension times of particles in the upper ocean. Deep-Sea Res Pt I 34:61–72
Marschner I (2009) glm2: fitting generalized linear models. R Package Version 1.1.1. http://cran.r-project.org/web/packages/glm2/
Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305
Morrissey JF, Gruber SH (1993) Home range of juvenile lemon sharks, Negaprion brevirostris. Copeia 1993:425–434
Nelson DR, Johnson RH (1980) Behavior of the reef sharks of Rangiroa, French Polynesia. National Geographic Research Report 12:479–499
Pak H, Zaneveld RV (1974) Equatorial front in the eastern Pacific Ocean. J Phys Oceanogr 4:570–578
Palacios DM (2004) Seasonal patterns of sea-surface temperature and ocean color around the Galapagos: regional and local influences. Deep-Sea Res Pt II 51:43–57
Palacios DM, Bograd SJ, Foley DG, Schwing FB (2006) Oceanographic characteristics of biological hotspots in the North Pacific: a remote sensing perspective. Deep-Sea Res Pt II 53:250–269
Peñaherrera C, Harpp K, Banks S (2013) Rapid seafloor mapping of the Northern Galapagos Islands. Darwin and Wolf, Galapagos Research 68
Queiroz N, Humphries NE, Noble LR, Santos AM, Sims DW (2012) Spatial dynamics and expanded vertical niche of blue sharks in oceanographic fronts reveal habitat targets for conservation. PLoS ONE 7:e32374
Sepulveda C, Kohin S, Chan C, Vetter R, Graham J (2004) Movement patterns, depth preferences, and stomach temperatures of free-swimming juvenile mako sharks, Isurus oxyrhinchus, in the Southern California Bight. Mar Biol 145:191–199
Silverman BW (1986) Density estimation for statistics and data analysis. Chapman & Hall, Boca Raton
Simpfendorfer CA, Heupel MR (2012) Assessing habitat use and movement. In: Carrier J, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 579–601
Sims DW, Nash JP, Morritt D (2001) Movements and activity of male and female dogfish in a tidal sea lough: alternative behavioural strategies and apparent sexual segregation. Mar Biol 139:1165–1175
Sims DW, Southall EJ, Wearmouth VJ, Hutchinson N, Budd GC, Morritt D (2005) Refuging behaviour in the nursehound Scyliorhinus stellaris (Chondrichthyes:elasmobranchii): preliminary evidence from acoustic telemetry. J Mar Biol Assoc UK 85:1137–1140
Snell HL, Stone PA, Snell HL (1996) A summary of the geographic characteristics of the Galapagos Islands. J Biogeogr 23:619–624
Speed CW, Meekan MG, Field IC, McMahon CR, Bradshaw CJA (2012) Heat-seeking sharks: support for behavioural thermoregulation in reef sharks. Mar Ecol Prog Ser 463:231–245
Standora EA, Nelson DR (1977) A telemetric study of the behavior of free-swimming Pacific angel sharks, Squatina californica. Bull South Calif Acad Sci 76:193–201
Sundstrom LF, Gruber SH, Clermont SM, Correia JPS, de Marignac JRC, Morrissey JF, Lowrance CR, Thomassen L, Oliveira MT (2001) Review of elasmobranch behavioral studies using ultrasonic telemetry with special reference to the lemon shark, Negaprion brevirostris, around Bimini Islands, Bahamas. Environ Biol Fishes 60:225–250
Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802
Sweet WV, Morrison JM, Kamykowski D, Schaeffer BA, Banks S, McCulloch A (2007) Water mass seasonal variability in the Galapagos Archipelago. Deep Sea Res Part 1 Oceanogr Res Pap 54:2023–2035
Sweet WV, Morrison JM, Liu KM, Kamykowski D, Schaeffer BA, Xie L, Banks S (2009) Tropical instability wave interactions within the Galapagos Archipelago. Deep-Sea Res Pt I 56:1217–1229
Thums M, Meekan M, Stevens J, Wilson S, Polovina J (2013) Evidence for behavioural thermoregulation by the world’s largest fish. J R Soc Interface 10:20120477
Venables WN, Ripley BD (2002) Modern applied statistics with S. Statistics and computing, 4th edn. Springer, New York
Vianna GMS, Meekan MG, Meeuwig JJ, Speed CW (2013) Environmental influences on patterns of vertical movement and site fidelity of grey reef sharks (Carcharhinus amblyrhynchos) at aggregation sites. PLoS ONE 8:e60331
Weihs D (1973) Mechanically efficient swimming techniques for fish with negative buoyancy. J Mar Res 31:194–209
Weng KC, Castillo PC, Morrissette JM, Landeira-Fernandez AM, Holts DB, Schallert RJ, Goldman KJ, Block BA (2005) Satellite tagging and cardiac physiology reveal niche expansion in salmon sharks. Science 310:104–106
Weng KC, O’Sullivan JB, Lowe CG, Winkler CE, Dewar H, Block BA (2007) Movements, behavior and habitat preferences of juvenile white sharks Carcharodon carcharias in the eastern Pacific. Mar Ecol Prog Ser 338:211–224
Westerberg H (1982) Ultrasonic tracking of Atlantic salmon (Salmo salar). II. Swimming depth and temperature stratification. Inst Freshw Res Drottningholm 60:102–120
Winter B (2013) Linear models and linear mixed effects models in R with linguistic applications. arXiv:1308.5499. http://arxiv.org/pdf/1308.5499.pdf
Worton BJ (1989) Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70:164–168
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgments
We thank the Galapagos National Park Service and the crews of the M/N Sierra Negra and B/I Tiburón Martillo for providing crucial logistical support for tracking sharks near Wolf Island and in the open ocean. Thanks to the Charles Darwin Research Station and staff of Biomar, especially Matthias Wolff, Roberto Pépolas, and Julio Delgado. Many thanks to Cap. Tito Franco for his dedication, long hours at the helm, and appreciation of our study. Many thanks to Cap. Peter Castillo of the F/M Arrecife, Cap. Andy Angermeyer of the Sea Ranger, and to all tracking volunteers: J. Delgado, R. Pépolas, G. Soler, R. Nebot, M. Calvopiña, P. Martínez, G. Vázquez, N. Trivedi, P. Acosta, Y. Mascarell, V. Linares, Y. Llerena, and T. Chapple. Thanks are due to Hawthorne Beyer (geospatial modeling) for his assistance in the use of the kernel density tool and to E. Melcon for her help on statistical analyses. We would also like to thank the Associate Editor and two anonymous reviewers for their constructive comments and suggestions that greatly improved earlier versions of this manuscript. This work was funded by WWF-Galapagos, Conservation International, Galapagos Conservation Trust, Galapagos Conservancy, Lindblad Expeditions, AeroGal, and Shark Diver. JTK was awarded a UC MEXUS-CONACYT fellowship that supported part of his work. Special thanks to Karina Busto for her help in the final edition of this manuscript.
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Communicated by J. D. R. Houghton.
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Ketchum, J.T., Hearn, A., Klimley, A.P. et al. Seasonal changes in movements and habitat preferences of the scalloped hammerhead shark (Sphyrna lewini) while refuging near an oceanic island. Mar Biol 161, 755–767 (2014). https://doi.org/10.1007/s00227-013-2375-5
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DOI: https://doi.org/10.1007/s00227-013-2375-5