Contrasting movements and connectivity of reef-associated sharks using acoustic telemetry: Implications for management

Ecological Applications

Volumn 25, Issue 8, 2015, Pages 2101-2118

  Espinoza, Mario ^a   Ledee, Elodie J I ^a   Simpfendorfer, Colin A ^a   Tobin, Andrew J ^a   Heupel, Michelle R ^a,b  

^a JAMES COOK UNIVERSITY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

Acoustic telemetry; Acoustic telemetry in fisheries management; Carcharhinus albimarginatus; Carcharhinus amblyrhynchos; Carcharhinus leucas; Conservation; Coral reefs; Great Barrier Reef; Management; Marine protected areas; Networks; Wide ranging predators.

Indexed keywords

BIOMONITORING; BIOTELEMETRY; CONNECTIVITY; CONSERVATION MANAGEMENT; CORAL REEF; DISPERSAL; FISHERY MANAGEMENT; MARINE PARK; MOVEMENT; NETWORK ANALYSIS; PREDATOR; REEF; SHARK; SPATIAL PLANNING; TAGGING;

AUSTRALIA; CORAL SEA; GREAT BARRIER REEF; QUEENSLAND;

ANTHOZOA; CARCHARHINUS ALBIMARGINATUS; CARCHARHINUS AMBLYRHYNCHOS; CARCHARHINUS LEUCAS; CHONDRICHTHYES;

ANIMAL; ANIMAL DISPERSAL; AUSTRALIA; CLASSIFICATION; CORAL REEF; FEMALE; MALE; PHYSIOLOGY; POPULATION DENSITY; PROCEDURES; SHARK; SPECIES DIFFERENCE; TELEMETRY; VETERINARY;

ANIMAL DISTRIBUTION; ANIMALS; AUSTRALIA; CORAL REEFS; FEMALE; MALE; POPULATION DENSITY; SHARKS; SPECIES SPECIFICITY; TELEMETRY;

EID: 84940536027     PISSN: None     EISSN: 19395582     Source Type: Journal    
DOI: 10.1890/14-2293.1     Document Type: Article

References (82)

1. Barnett, A., K. G. Abrantes, J. Seymour, and R. Fitzpatrick. 2012. Residency and spatial use by reef sharks of an isolated seamount and its implications for conservation. PLoS ONE 7:e36574.
2. Barrat, A., M. Barthelemy, R. Pastor-Satorras, and A. Vespignani. 2004. The architecture of complex weighted networks. Proceedings of the National Academy of Sciences USA 101:3747-3752.
3. Bodin, O., H. Ramirez-Sanchez, S. Ernstson, and C. Prell. 2011. Some basic structural characteristics of networks. Pages 29-43 in O. Bodin and C. Prell, editors. Social networks and natural resource management: uncovering the social fabric of environmental governance. Cambridge University Press, UK.
4. Bond, M. E., E. Babcock, E. K. Pikitch, D. L. Abercrombie, N. F. Lamb, and D. D. Chapman. 2012. Reef sharks exhibit site-fidelity and higher relative abundance in marine reserves on the Mesoamerican Barrier Reef. PLoS ONE 7:e32983.
5. Brunnschweiler, J. M., and A. Barnett. 2013. Opportunistic visitors: long-term behavioural response of bull sharks to food provisioning in Fiji. PLoS ONE 8:e58522.
6. Butts, C. T. 2013. SNA: tools for social network analysis. Version 2.3-1. www.cran.r-project.org/package=sna
7. Chapman, D. D., E. K. Pikitch, E. Babcock, and M. S. Shivji. 2005. Marine reserve design and evaluation using automated acoustic telemetry: a case-study involving coral reef-associated sharks in the Mesoamerican Caribbean. Marine Technology Society Journal 39:42-55.
8. Chetkiewicz, C. L. B., C. C. St. Clair, and M. S. Boyce. 2006. Corridors for conservation: integrating pattern and process. Annual Review of Ecology, Evolution, and Systematics 37:317-342.
9. Chin, A., M. R. Heupel, C. A. Simpfendorfer, and A. J. Tobin. 2013. Ontogenetic movements of juvenile blacktip reef sharks: evidence of dispersal and connectivity between coastal habitats and coral reefs. Aquatic Conservation: Marine and Freshwater Ecosystems 23:468-474.
10. Chin, A., P. M. Kyne, T. I. Walker, and R. B. McAauley. 2010. An integrated risk assessment for climate change: analysing the vulnerability of sharks and rays on Australia's Great Barrier Reef. Global Change Biology 16:1936-1953.
11. Croft, D. P., J. R. Madden, D. W. Franks, and R. James. 2011. Hypothesis testing in animal social networks. Trends in Ecology & Evolution 26:502-507.
12. Csardi, G., and T. Nepusz. 2006. The igraph software package for complex network research. R package version 0.6.6. http://cran.r-project.org/web/packages/igraph
13. Dale, J. J., A. M. Stankus, M. S. Burns, and C. G. Meyer. 2011. The shark assemblage at French Frigate Shoals atoll, Hawai'i: species composition, abundance and habitat use. PLoS ONE 6:e16962.
14. Daly, R., M. J. Smale, P. D. Cowley, and P. W. Froneman. 2014. Residency patterns and migration dynamics of adult bull sharks (Carcharhinus leucas) on the east coast of southern Africa. PLoS ONE 9:e109357.
15. Davidson, L. N. 2012. Shark sanctuaries: substance or spin? Science 338:1538.
16. De'ath, G., K. E. Fabricius, H. Sweatman, and M. Puotinen. 2012. The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences USA 109:17995-17999.
17. Done, T. J. 1982. Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1:95-107.
18. Dulvy, N. K. 2013. Super-sized MPAs and the marginalization of species conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 362:357-362.
19. Dulvy, N. K., et al. 2014. Extinction risk and conservation of the world's sharks and rays. eLife 3:e00590.
20. Espinoza, M., M. Cappo, M. R. Heupel, A. J. Tobin, and C. A. Simpfendorfer. 2014. Quantifying shark distribution patterns and species-habitat associations: implications of Marine Park Zoning. PLoS ONE 9:e106885.
21. Espinoza, M., T. J. Farrugia, D. M. Webber, F. Smith, and C. G. Lowe. 2011. Testing a new acoustic telemetry technique to quantify long-term, fine-scale movements of aquatic animals. Fisheries Research 108:364-371.
22. Espinoza, M., M. R. Heupel, A. J. Tobin, and C. A. Simpfendorfer. 2015a. Movement patterns of silvertip sharks (Carcharhinus albimarginatus) on coral reefs. Coral Reefs. http://dx.doi.org/10.1007/s00338-015-1312-0
23. Espinoza, M., M. R. Heupel, A. J. Tobin, and C. A. Simpfendorfer. 2015b. Residency patterns and movements of grey reef sharks (Carcharhinus amblyrhynchos) in semi-isolated coral reef habitats. Marine Biology 162:343-358.
24. Fernandes, L., et al. 2005. Establishing representative no-take areas in Great Barrier Reef: large scale implementation of theory on marine protected areas. Conservation Biology 19:1733-1744.
25. Fletcher, R. J., M. A. Acevedo, B. E. Reichert, K. E. Pias, and W. M. Kitchens. 2011. Social network models predict movement and connectivity in ecological landscapes. Proceedings of the National Academy of Sciences USA 108:19282-19287.
26. Gaines, S. D., C. White, M. H. Carr, and S. R. Palumbi. 2010. Designing marine reserve networks for both conservation and fisheries management. Proceedings of the National Academy of Sciences USA 107:18286-18293.
27. Graham, N. A. J., M. D. Spalding, and C. R. C. Sheppard. 2010. Reef shark declines in remote atolls highlight the need for multi-faceted conservation action. Aquatic Conservation: Marine and Freshwater Ecosystems 20:543-548.
28. Grubbs, R. D. 2010. Ontogenetic shifts in movement and habitat use. Pages 317-350 in J. C. Carrier, J. A. Musick, and M. R. Heithaus, editors. Sharks and their relatives II. CRC Press, Boca Raton, Florida, USA.
29. Gu, Z., L. Gu, R. Ellis, M. Schlesner, and B. Brors. 2014. Circlize implements and enhances circular visualization in R. Bioinformatics 30(19):2811-2812.
30. Hanski, I. 1998. Metapopulation dynamics. Nature 396:41-49.
31. Hawkes, C. 2009. Linking movement behaviour, dispersal and population processes: is individual variation a key? Journal of Animal Ecology 78:894-906.
32. Hearn, A., J. Ketchum, A. P. Klimley, E. Espinoza, and C. Pen-aherrera. 2010. Hotspots within hotspots? Hammerhead shark movements around Wolf Island, Galapagos Marine Reserve. Marine Biology 157:1899-1915.
33. Hein, S., B. Pfenning, T. Hovestadt, and H. J. Poethke. 2004. Patch density, movement pattern, and realised dispersal distances in a patch-matrix landscape-a simulation study. Ecological Modelling 174:411-420.
34. Heithaus, M. R., et al. 2014. Seagrasses in the age of sea turtle conservation and shark overfishing. Frontiers in Marine Science 1:1-6.
35. Heupel, M. R., J. Semmens, and A. Hobday. 2006. Automated acoustic tracking of aquatic animals: scales, design and deployment of listening station arrays. Marine and Freshwater Research 57:1-13.
36. Heupel, M. R., and C. A. Simpfendorfer. 2014. Importance of environmental and biological drivers in the presence and space use of a reef-associated shark. Marine Ecology Progress Series 496:47-57.
37. Heupel, M. R., C. A. Simpfendorfer, M. Espinoza, A. F. Smoothy, A. J. Tobin, and V. M. Peddemors. 2015. Conservation challenges of sharks with continental scale migrations. Frontiers in Marine Science 2:12.
38. Heupel, M. R., C. A. Simpfendorfer, and R. Fitzpatrick. 2010. Large-scale movement and reef fidelity of grey reef sharks. PLoS ONE 5:e9650.
39. Heupel, M. R., A. Williams, D. Welch, A. Ballagh, B. Mapstone, G. Carlos, C. Davies, and C. A. Simpfendorfer. 2009. Effects of fishing on tropical reef associated shark populations on the Great Barrier Reef. Fisheries Research 95:350-361.
40. IMOS (Integrated Marine Observing System). 2009. Australian Animal Tagging and Monitoring System (AATAMS). Sydney, Australia. http://imos.org.au/aatams.html
41. Jacoby, D. M. P., D. P. Croft, and D. W. Sims. 2012. Social behaviour in sharks and rays: analysis, patterns and implications for conservation. Fish and Fisheries 13:399-417.
42. Jones, G. P., G. R. Almany, G. R. Russ, P. F. Sale, R. S. Steneck, M. J. H. Oppen, and B. L. Willis. 2009. Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307-325.
43. Jordan, F., A. Baldi, K. M. Orci, I. Racz, and Z. Varga. 2003. Characterizing the importance of habitat patches and corridors in maintaining the landscape connectivity of a Pholidoptera transsylvanica (Orthoptera) metapopulation. Landscape Ecology 18:83-92.
44. Ketchum, J. T., A. Hearn, A. P. Klimley, C. Pen-aherrera, E. Espinoza, S. Bessudo, G. Soler, and R. Arauz. 2014. Inter-island movements of scalloped hammerhead sharks (Sphyrna lewini) and seasonal connectivity in a marine protected area of the eastern tropical Pacific. Marine Biology 161:939-951.
45. Kininmonth, S. J., G. De'ath, and H. P. Possingham. 2009. Graph theoretic topology of the Great but small Barrier Reef world. Theoretical Ecology 3:75-88.
46. Knip, D. M., M. R. Heupel, and C. A. Simpfendorfer. 2012. Evaluating marine protected areas for the conservation of tropical coastal sharks. Biological Conservation 148:200-209.
47. Ledee, E., M. R. Heupel, A. J. Tobin, D. M. Knip, and C. A. Simpfendorfer. 2015. A comparison between traditional kernel-based methods and network analysis: an example from two nearshore shark species. Animal Behaviour 103:17-28.
48. McCauley, D. J., P. A. DeSalles, H. S. Young, Y. P. Papastamatiou, J. E. Caselle, M. H. Deakos, J. P. A. Gardner D. W. Garton, J. D. Collen, and F. Micheli. 2014. Reliance of mobile species on sensitive habitats: a case study of manta rays (Manta alfredi) and lagoons. Marine Biology 161:1987-1998.
49. McCauley, D. J., H. S. Young, R. B. Dunbar, J. A. Estes, B. X. Semmens, and F. Micheli. 2012. Assessing the effects of large mobile predators on ecosystem connectivity. Ecological Applications 22:1711-1717.
50. McCook, L. J., et al. 2010. Adaptive management of the Great Barrier Reef: a globally significant demonstration of the benefits of networks of marine reserves. Proceedings of the National Academy of Sciences USA 107:18278-18285.
51. Meyer, C. G., K. N. Holland, and Y. P. Papastamatiou. 2005. Sharks can detect changes in the geomagnetic field. Journal of the Royal Society Interface 2:129-130.
52. Minor, E. S., and D. L. Urban. 2008. A graph-theory framework for evaluating landscape connectivity and conservation planning. Conservation Biology 22:297-307.
53. Montgomery, J. C., and M. M. Walker. 2001. Orientation and navigation in elasmobranchs: which way forward? Environmental Biology of Fishes 60:109-116.
54. Mourier, J., J. Vercelloni, and S. Planes. 2012. Evidence of social communities in a spatially structured network of a free-ranging shark species. Animal Behaviour 83:389-401.
55. Nadon, M. O., J. K. Baum, I. D. Williams, J. M. McPherson, B. J. Zgliczynski, B. L. Richards, R. E. Schroeder, and R. E. Brainard. 2012. Re-creating missing population baselines for Pacific reef sharks. Conservation Biology 26:493-503.
56. Olds, A. D., R. M. Connolly, K. A. Pitt, and P. S. Maxwell. 2012. Habitat connectivity improves reserve performance. Conservation Letters 5:56-63.
57. Papastamatiou, Y. P., D. P. Cartamil, C. G. Lowe, C. G. Meyer, B. M. Wetherbee, and K. N. Holland. 2011. Scales of orientation, directed walks and movement path structure in sharks. Journal of Animal Ecology 80:864-874.
58. Papastamatiou, Y. P., P. A. DeSalles, and D. J. McCauley. 2012. Area-restricted searching by manta rays and their response to spatial scale in lagoon habitats. Marine Ecology Progress Series 456:233-244.
59. Papastamatiou, Y. P., A. M. Friedlander, J. E. Caselle, and C. G. Lowe. 2010. Long-term movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus melanopterus) at Palmyra Atoll. Journal of Experimental Marine Biology and Ecology 386:94-102.
60. Papastamatiou, Y. P., C. G. Lowe, J. E. Caselle, and A. M. Friedlander. 2009. Scale-dependent effects of habitat on movements and path structure of reef sharks at a predator-dominated atoll. Ecology 90:996-1008.
61. Papastamatiou, Y. P., C. G. Meyer, F. Carvalho, J. J. Dale, M. R. Hutchinson, and K. N. Holland. 2013. Telemetry and random-walk models reveal complex patterns of partial migration in a large marine predator. Ecology 94:2595-2606.
62. Pascual-Hortal, L., and S. Saura. 2006. Comparison and development of new graph-based landscape connectivity indices: towards the priorization of habitat patches and corridors for conservation. Landscape Ecology 21:959-967.
63. Pittman, S. J., M. E. Monaco, A. M. Friedlander, B. Legare, R. S. Nemeth, M. S. Kendall, M. Poti, R. D. Clark, L. M. Wedding, and C. Caldow. 2014. Fish with chips: tracking reef fish movements to evaluate size and connectivity of Caribbean marine protected areas. PLoS ONE 9:e96028.
64. R Development Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.r-project.org
65. Rizkalla, C. E., J. E. Moore, and R. K. Swihart. 2008. Modeling patch occupancy: relative performance of ecologically scaled landscape indices. Landscape Ecology 24:77-88.
66. Rizzari, J. R., A. J. Frisch, and K. A. Magnenat. 2014. Diversity, abundance, and distribution of reef sharks on outer-shelf reefs of the Great Barrier Reef, Australia. Marine Biology 161:2847-2855.
67. Ruppert, J. L. W., M. J. Travers, L. L. Smith, M. J. Fortin, and M. G. Meekan. 2013. Caught in the middle: combined impacts of shark removal and coral loss on the fish communities of coral reefs. PLoS ONE 8:e74648.
68. Sandin, S. A., et al. 2008. Baselines and degradation of coral reefs in the Northern Line Islands. PLoS ONE 3:1-11.
69. Saura, S., and L. Pascual-Hortal. 2007. A new habitat availability index to integrate connectivity in landscape conservation planning: comparison with existing indices and application to a case study. Landscape and Urban Planning 83:91-103.
70. Saura, S., and J. Torne. 2009. Conefor Sensinode 2.2: a software package for quantifying the importance of habitat patches for landscape connectivity. Environmental Modelling & Software 24:135-139.
71. Simpfendorfer, C. A., M. R. Heupel, and R. E. Hueter. 2002. Estimation of short-term centers of activity from an array of omnidirectional hydrophones and its use in studying animal movements. Canadian Journal of Fisheries and Aquatic Sciences 59:23-32.
72. Speed, C., I. Field, M. Meekan, and C. Bradshaw. 2010. Complexities of coastal shark movements and their implications for management. Marine Ecology Progress Series 408:275-293.
73. Stehfest, K. M., T. A. Patterson, L. Dagorn, K. N. Holland, D. Itano, and J. M. Semmens. 2013. Network analysis of acoustic tracking data reveals the structure and stability of fish aggregations in the ocean. Animal Behaviour 85:839-848.
74. Treml, E. A., P. N. Halpin, D. L. Urban, and L. F. Pratson. 2008. Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landscape Ecology 23:19-36.
75. Urban, D. L., and T. Keitt. 2001. Landscape connectivity: a graph-theoretic perspective. Ecology 85:1205-1218.
76. Vianna, G. M., M. G. Meekan, J. J. Meeuwig, and C. W. Speed. 2013. Environmental influences on patterns of vertical movement and site fidelity of grey reef sharks (Carcharhinus amblyrhynchos) at aggregation sites. PLoS ONE 8:e60331.
77. Ward-Paige, C. A., C. Mora, H. K. Lotze, C. Pattengill-Semmens, L. McClenachan, E. Arias-Castro, and R. A. Myers. 2010. Large-scale absence of sharks on reefs in the greater-Caribbean: a footprint of human pressures. PLoS ONE 5:e11968.
78. Werry, J. M., S. Planes, M. L. Berumen, K. A. Lee, C. D. Braun, and E. Clua. 2014. Reef-fidelity and migration of tiger sharks, Galeocerdo cuvier, across the Coral Sea. PLoS ONE 9:e83249.
79. West, D. B. 2001. Introduction to graph theory. Prentice Hall, London, UK.
80. Whitney, N. M., W. D. Robbins, J. K. Schultz, B. W. Bowen, and K. N. Holland. 2012. Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): genetic evidence for extensive connectivity without a pelagic larval stage. Journal of Biogeography 39:1144-1156.
81. Wilson, S. K., N. A. J. Graham, M. S. Pratchett, G. P. Jones, and N. V. C. Polunin. 2006. Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Global Change Biology 12:2220-2234.
82. Zuur, A. F., E. N. Ieno, N. Walker, A. A. Saveliev, and G. M. Smith. 2009. Mixed effects models and extensions in ecology with R. Springer, New York, New York, USA.