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Residency patterns and movements of grey reef sharks (Carcharhinus amblyrhynchos) in semi-isolated coral reef habitats

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Abstract

The degree of reef isolation may limit the frequency of long-range dispersals in reef-associated sharks. Therefore, understanding how the behaviour and spatial ecology of a species differs across reef habitats is essential for developing sound conservation approaches. The present study examined the residency, movement and activity space of grey reef sharks (Carcharhinus amblyrhynchos) in the central Great Barrier Reef (GBR). An array of 56 acoustic receivers covering 17 semi-isolated coral reefs across 150 km was used to monitor shark movements. Forty C. amblyrhynchos were tagged with acoustic transmitters and monitored from 251 to 821 days. Most sharks were detected on a single reef; however, some individuals (4 females; 10 males) moved to up to five reefs. Residency index ranged from 0.02 to 1.0, with a mean ± SD of 0.78 ± 0.26. Mixed-effect models showed that weekly and monthly residency was mainly influenced by shark size, with little or no effect of environmental parameters. Although C. amblyrhynchos were present year-round, juvenile sharks had lower residency to their tagging reef than adults. In addition, mature females were detected less between November and mid-February, which coincides with reported parturition in the central GBR. Long-term monitoring data revealed that C. amblyrhynchos exhibited high residency to their tagging reef, and therefore, even in systems with semi-isolated reefs such as the GBR, this species may benefit from spatial management approaches at the reef level. However, behavioural differences between sexes and life-stages of C. amblyrhynchos reported in this study suggest marine reserves may provide lower protection relative to more remote and isolated coral reefs.

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References

  • Baayen RH, Davidson DJ, Bates DM (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412. doi:10.1016/j.jml.2007.12.005

    Article  Google Scholar 

  • Barnett A, Abrantes KG, Seymour J, Fitzpatrick R (2012) Residency and spatial use by reef sharks of an isolated seamount and its implications for conservation. PLoS ONE 7:e36574. doi:10.1371/journal.pone.0036574

    Article  CAS  Google Scholar 

  • Bates D, Maechler M, Bolker BM, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.0-6. http://cran.r-project.org/package=lme4

  • Bond ME, Babcock E, Pikitch EK et al (2012) Reef sharks exhibit site-fidelity and higher relative abundance in marine reserves on the Mesoamerican Barrier Reef. PLoS ONE 7:e32983. doi:10.1371/journal.pone.0032983

    Article  CAS  Google Scholar 

  • Bush A, Holland KN (2002) Food limitation in a nursery area: estimates of daily ration in juvenile scalloped hammerheads, Sphyrna lewini (Griffith and Smith, 1834) in Ka¯ne’ ohe Bay, ahu, Hawai’i. J Exp Mar Bio Ecol 278:157–178

    Article  Google Scholar 

  • Chapman DD, Pikitch EK, Babcock E, Shivji MS (2005) Marine reserve design and evaluation using automated acoustic telemetry: a case-study involving coral reef-associated sharks in the Mesoamerican Caribbean. Mar Technol Soc J 39:42–55

    Article  Google Scholar 

  • Chin A, Heupel MR, Simpfendorfer CA, Tobin AJ (2013a) Ontogenetic movements of juvenile blacktip reef sharks: evidence of dispersal and connectivity between coastal habitats and coral reefs. Aquat Conserv Mar Freshw Ecosyst 23:468–474. doi:10.1002/aqc.2349

    Article  Google Scholar 

  • Chin A, Tobin AJ, Heupel MR, Simpfendorfer CA (2013b) Population structure and residency patterns of the blacktip reef shark Carcharhinus melanopterus in turbid coastal environments. J Fish Biol 82:1192–1210. doi:10.1111/jfb.12057

    Article  CAS  Google Scholar 

  • Done TJ (1982) Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1:95–107

    Article  Google Scholar 

  • Duong T (2007) ks: kernel density estimation and kernel discriminant analysis for multivariate data in R. J Stat Softw 21:1–16

    Google Scholar 

  • Economakis AE, Lobel PS (1998) Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean. Environ Biol Fishes 51:129–139

    Article  Google Scholar 

  • Espinoza M, Farrugia TJ, Lowe CG (2011) Habitat use, movements and site fidelity of the gray smooth-hound shark (Mustelus californicus Gill 1863) in a newly restored southern California estuary. J Exp Mar Biol Ecol 401:63–74. doi:10.1016/j.jembe.2011.03.001

    Article  Google Scholar 

  • Espinoza M, Cappo M, Heupel MR et al (2014) Quantifying shark distribution patterns and species-habitat associations: implications of Marine Park Zoning. PLoS ONE 9:e106885. doi:10.1371/journal.pone.0106885

    Article  Google Scholar 

  • Field IC, Meekan MG, Speed CW et al (2011) Quantifying movement patterns for shark conservation at remote coral atolls in the Indian Ocean. Coral Reefs 30:61–71. doi:10.1007/s00338-010-0699-x

    Article  Google Scholar 

  • Garla RC, Chapman DD, Wetherbee BM, Shivji MS (2006) Movement patterns of young Caribbean reef sharks, Carcharhinus perezi, at Fernando de Noronha Archipelago, Brazil: the potential of marine protected areas for conservation of a nursery ground. Mar Biol 149:189–199. doi:10.1007/s00227-005-0201-4

    Article  Google Scholar 

  • Graham NAJ, Spalding MD, Sheppard CRC (2010) Reef shark declines in remote atolls highlight the need for multi-faceted conservation action. Aquat Conserv Mar Freshw Ecosyst 20:543–548. doi:10.1002/aqc.1116

    Article  Google Scholar 

  • Graham NAJ, Chong-Seng KM, Huchery C et al (2014) Coral reef community composition in the context of disturbance history on the great barrier reef, australia. PLoS ONE 9:e101204. doi:10.1371/journal.pone.0101204

    Article  Google Scholar 

  • Grubbs RD (2010) Ontogenetic shifts in movement and habitat use. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks their relat. II. CRC Press, Boca Raton, pp 317–350

    Google Scholar 

  • Hearn A, Ketchum J, Klimley AP et al (2010) Hotspots within hotspots? Hammerhead shark movements around Wolf Island, Galapagos Marine Reserve. Mar Biol 157:1899–1915. doi:10.1007/s00227-010-1460-2

    Article  Google Scholar 

  • Heupel MR, Simpfendorfer CA (2002) Estimation of mortality of juvenile blacktip sharks, Carcharhinus limbatus, within a nursery area using telemetry data. Can J Fish Aquat Sci 59:624–632. doi:10.1139/F02-036

    Article  Google Scholar 

  • Heupel MR, Simpfendorfer CA (2014) Importance of environmental and biological drivers in the presence and space use of a reef-associated shark. Mar Ecol Prog Ser 496:47–57. doi:10.3354/meps10529

    Article  Google Scholar 

  • Heupel MR, Simpfendorfer CA, Hueter RE (2004) Estimation of shark home ranges using passive monitoring techniques. Environ Biol Fishes 71:135–142

    Article  Google Scholar 

  • Heupel MR, Simpfendorfer CA, Fitzpatrick R (2010) Large-scale movement and reef fidelity of grey reef sharks. PLoS ONE 5:e9650. doi:10.1371/journal.pone.0009650

    Article  Google Scholar 

  • Hopley D, Parnell K, Isdale P (1989) The Great Barrier Reef Marine Park: dimensions and regional patterns. Aust Geogr Stud 27:47–66

    Article  Google Scholar 

  • Hussey NE, Dudley SFJ, McCarthy ID et al (2011) Stable isotope profiles of large marine predators: viable indicators of trophic position, diet, and movement in sharks? Can J Fish Aquat Sci 2045:2029–2045. doi:10.1139/F2011-115

    Article  Google Scholar 

  • Keeney DB, Heupel MR, Hueter RE, Heist EJ (2003) Genetic heterogeneity among blacktip shark, Carcharhinus limbatus, continental nurseries along the U.S. Atlantic and Gulf of Mexico. Mar Biol 143:1039–1046. doi:10.1007/s00227-003-1166-9

    Article  Google Scholar 

  • Keeney DB, Heupel MR, Hueter RE, Heist EJ (2005) Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Mol Ecol 14:1911–1923. doi:10.1111/j.1365-294X.2005.02549.x

    Article  CAS  Google Scholar 

  • Knip DM, Heupel MR, Simpfendorfer CA (2012a) Habitat use and spatial segregation of adult spottail sharks Carcharhinus sorrah in tropical nearshore waters. J Fish Biol 80:767–784. doi:10.1111/j.1095-8649.2012.03223.x

    Article  CAS  Google Scholar 

  • Knip DM, Heupel MR, Simpfendorfer CA (2012b) To roam or to home: site fidelity in a tropical coastal shark. Mar Biol 159:1647–1657. doi:10.1007/s00227-012-1950-5

    Article  Google Scholar 

  • Lowe CG (2002) Bioenergetics of free-ranging juvenile scalloped hammerhead sharks (Sphyrna lewini) in Kane’ohe Bay, Oahu, HI. J Exp Mar Bio Ecol 278:141–156

    Article  Google Scholar 

  • Lowe CG, Bray RN (2006) Movement and activity patterns. In: Allen LG, Pondella DJ (eds) The ecology of marine fishes: California and adjacent waters. University of California Press, pp 524–553

  • McKibben JN, Nelson DR (1986) Patterns of movement and grouping of grey reef sharks, Carcharhinus amblyrhynchos, at Enewetak, Marshall Islands. Bull Mar Sci 38:89–110

    Google Scholar 

  • Meyer CG, Papastamatiou YP, Holland KN (2010) A multiple instrument approach to quantifying the movement patterns and habitat use of tiger (Galeocerdo cuvier) and Galapagos sharks (Carcharhinus galapagensis) at French Frigate Shoals, Hawaii. Mar Biol 157:1857–1868. doi:10.1007/s00227-010-1457-x

    Article  Google Scholar 

  • Morrissey JF, Gruber SH (1993) Home range of juvenile lemon sharks, Negaprion brevirostris. Copeia 1993:425–434

    Article  Google Scholar 

  • Mourier J, Planes S (2013) Direct genetic evidence for reproductive philopatry and associated fine-scale migrations in female blacktip reef sharks (Carcharhinus melanopterus) in French Polynesia. Mol Ecol 22:201–214

    Article  Google Scholar 

  • Papastamatiou YP, Lowe CG, Caselle JE, Friedlander AM (2009) Scale-dependent effects of habitat on movements and path structure of reef sharks at a predator-dominated atoll. Ecology 90:996–1008

    Article  Google Scholar 

  • Papastamatiou YP, Friedlander AM, Caselle JE, Lowe CG (2010) Long-term movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus melanopterus) at Palmyra Atoll. J Exp Mar Bio Ecol 386:94–102. doi:10.1016/j.jembe.2010.02.009

    Article  Google Scholar 

  • Papastamatiou YP, Cartamil DP, Lowe CG et al (2011) Scales of orientation, directed walks and movement path structure in sharks. J Anim Ecol 80:864–874. doi:10.1111/j.1365-2656.2011.01815.x

    Article  Google Scholar 

  • Papastamatiou YP, Meyer CG, Carvalho F et al (2013) Telemetry and random-walk models reveal complex patterns of partial migration in a large marine predator. Ecology 94:2595–2606

    Article  Google Scholar 

  • Pardini AT, Jones CS, Noble LR et al (2001) Sex-biased dispersal of great white sharks. Nature 412:139–140. doi:10.1038/35084125

    Article  CAS  Google Scholar 

  • Pratchett M, Baird A, McCowan D, et al. (2008) Protracted declines in coral cover and fish abundance following climate-induced coral bleaching on the Great Barrier Reef. In: Proceedings of 11th international coral reef symposium 2008, 7–11 July

  • Quattro JM, Stoner DS, Driggers WB et al (2005) Genetic evidence of cryptic speciation within hammerhead sharks (Genus Sphyrna). Mar Biol 148:1143–1155. doi:10.1007/s00227-005-0151-x

    Article  Google Scholar 

  • Rechisky EL, Wetherbee BM (2003) Short-term movements of juvenile and neonate sandbar sharks, Carcharhinus plumbeus, on their nursery grounds in Delaware Bay. Environ Biol Fishes 68:113–128

    Article  Google Scholar 

  • Robbins WD (2006) Abundance, demography and population structure of the grey reef shark (Carcharhinus amblyrhynchos) and the whitetip reef shark (Triaenodon obesus) (Fam. Carcharhinidae). PhD thesis, James Cook University

  • Ruppert JLW, Travers MJ, Smith LL et al (2013) Caught in the middle: combined impacts of shark removal and coral loss on the fish communities of coral reefs. PLoS ONE 8:e74648. doi:10.1371/journal.pone.0074648

    Article  CAS  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Sandin SA, Smith JE, Demartini EE et al (2008) Baselines and degradation of coral reefs in the Northern Line Islands. PLoS ONE 3:1–11. doi:10.1371/journal.pone.0001548

    Article  Google Scholar 

  • Simpfendorfer CA, Heupel MR, Hueter RE (2002) Estimation of short-term centers of activity from an array of omnidirectional hydrophones and its use in studying animal movements. Can J Fish Aquat Sci 59:23–32. doi:10.1139/F01-191

    Article  Google Scholar 

  • Speed C, Field I, Meekan M, Bradshaw C (2010) Complexities of coastal shark movements and their implications for management. Mar Ecol Prog Ser 408:275–293. doi:10.3354/meps08581

    Article  Google Scholar 

  • Speed CW, Meekan MG, Field IC et al (2011) Spatial and temporal movement patterns of a multi-species coastal reef shark aggregation. Mar Ecol Prog Ser 429:261–275

    Article  Google Scholar 

  • Speed CW, Meekan MG, Field IC et al (2012) Heat-seeking sharks: support for behavioural thermoregulation in reef sharks. Mar Ecol Prog Ser 463:231–245. doi:10.3354/meps09864

    Article  Google Scholar 

  • Vianna GM, 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. doi:10.1371/journal.pone.0060331

    Article  CAS  Google Scholar 

  • Ward-Paige CA, Mora C, Lotze HK et al (2010) Large-scale absence of sharks on reefs in the greater-Caribbean: a footprint of human pressures. PLoS ONE 5:e11968. doi:10.1371/journal.pone.0011968

    Article  Google Scholar 

  • Werry JM, Planes S, Berumen ML et al (2014) Reef-fidelity and migration of tiger sharks, Galeocerdo cuvier, across the Coral Sea. PLoS ONE 9:e83249. doi:10.1371/journal.pone.0083249

    Article  Google Scholar 

  • Wetherbee BM, Crow GL, Lowe CG (1997) Distribution, reproduction and diet of the gray reef shark Carcharhinus amblyrhynchos in Hawaii. Mar Ecol Prog Ser 151:181–189

    Article  Google Scholar 

  • Whitney NM, Pyle RL, Holland KN, Barcz JT (2012) Movements, reproductive seasonality, and fisheries interactions in the whitetip reef shark (Triaenodon obesus) from community-contributed photographs. Environ Biol Fishes 93:121–136. doi:10.1007/s10641-011-9897-9

    Article  Google Scholar 

  • Williams DM (1982) Patterns in the distribution of fish communities across the Central Great Barrier Reef. Coral Reefs 1:35–43. doi:10.1007/BF00286538

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, p 574

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Acknowledgments

We would like to thank students and staff from the Centre for Sustainable Tropical Fisheries and Aquaculture for field support, especially J. Matley, E. Lédée, F. Faria and S. Moore. We would also like to thank Dr. Rhondda Jones for statistical advice and the crew from the RV James Kirby for their time and support during fieldwork. We are grateful to José Fabricio Vargas for the scientific drawing used in the manuscript and helpful comments from three anonymous reviewers. This project was funded by the Australian Government’s National Environmental Research Program (Tropical Ecosystems Hub Project 6.1). MRH was supported by a Future Fellowship (#FT100101004) from the Australian Research Council, and ME was supported by the PADI Foundation, Australian Endeavour and AIMS@JCU Scholarships.

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Authors and Affiliations

  1. Centre for Sustainable Tropical Fisheries and Aquaculture and College of Marine and Environmental Sciences, James Cook University, Townsville, QLD, 48113, Australia

    Mario Espinoza, Michelle. R. Heupel, Andrew J. Tobin & Colin A. Simpfendorfer

  2. AIMS@JCU, Australian Institute of Marine Science, College of Marine and Environmental Sciences, James Cook University, Townsville, QLD, 4811, Australia

    Mario Espinoza

  3. Australian Institute of Marine Science, PMB No 3, Townsville, QLD, 4810, Australia

    Michelle. R. Heupel

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  1. Mario Espinoza
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  2. Michelle. R. Heupel
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Correspondence to Mario Espinoza.

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Communicated by J. Carlson.

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Espinoza, M., Heupel, M.R., Tobin, A.J. et al. Residency patterns and movements of grey reef sharks (Carcharhinus amblyrhynchos) in semi-isolated coral reef habitats. Mar Biol 162, 343–358 (2015). https://doi.org/10.1007/s00227-014-2572-x

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