Abstract
The grey reef shark, Carcharhinus amblyrhynchos, is one of the most abundant coral reef sharks throughout the Indo-Pacific. However, this species has been critically impacted across its range, with well-documented population declines of > 90% attributed to human activities. A key knowledge gap in the successful implementation of grey reef shark conservation plans is the understanding of large-scale movement patterns, along with the associated biological and ecological drivers. To address this shortfall, we acoustically monitored 147 adult and juvenile grey reef sharks of all sexes for more than 2 yr across the New Caledonian archipelago, West Pacific. Here, we document multiple adult males undertaking return journeys of up to nearly 700 km in consecutive years. This constitutes the first evidence of repeated long-range migrations for this species. Although only a limited number of adult males were definitively tracked undertaking migrations, similar timing in changes in the detection patterns of a further 13 animals, mostly adult males, suggests this behavior may be more common than previously thought. The paucity of evidence for juvenile migrations and timing of adult movements suggest that mating is the motivation behind these migrations. Our results have important implications for management, given the potential of mature individuals to recurrently travel outside managed or protected areas. Future management of this species clearly needs to consider the importance of large-scale migratory behaviors when developing management plans.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Australian Government (2004) Great Barrier Reef Marine Park zoning plan 2003
Bansemer CS, Bennett MB (2011) Sex- and maturity-based differences in movement and migration patterns of grey nurse shark, Carcharias taurus, along the eastern coast of Australia. Mar Freshw Res 62:596
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
Bass NC, Mourier J, Knott NA, Day J, Guttridge T, Brown C (2017) Long-term migration patterns and bisexual philopatry in a benthic shark species. Mar Freshw Res 68:1414
Block BA, Teo SLH, Walli A, Boustany A, Stokesbury MJW, Farwell CJ, Weng KC, Dewar H, Williams TD (2005) Electronic tagging and population structure of Atlantic bluefin tuna. Nature 434:1121–1127
Bruce B, Bradford R (2015) Segregation or aggregation? Sex-specific patterns in the seasonal occurrence of white sharks, Carcharodon carcharias, at the Neptune Islands, South Australia. J Fish Biol 87:1355–1370
D’agata S, Mouillot D, Wantiez L, Friedlander AM, Kulbicki M, Vigliola L (2016) Marine reserves lag behind wilderness in the conservation of key functional roles. Nature Commun 7:12000
Dingle H, Drake VA (2007) What is migration? BioScience 57:113–121
Domeier ML, Nasby-Lucas N (2013) Two-year migration of adult female white sharks (Carcharodon carcharias) reveals widely separated nursery areas and conservation concerns. Anim Biotelemetry 1:2
Double MC, Andrews-Goff V, Jenner KCS, Jenner M-N, Laverick SM, Branch TA, Gales NJ (2014) Migratory movements of pygmy blue whales (Balaenoptera musculus brevicauda) between Australia and Indonesia as revealed by satellite telemetry. PLoS ONE 9:e93578
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
Espinoza M, Heupel MR, Tobin AJ, Simpfendorfer CA (2015) Residency patterns and movements of grey reef sharks (Carcharhinus amblyrhynchos) in semi-isolated coral reef habitats. Mar Biol 162:343–358
Feldheim KA, Gruber SH, DiBattista JD, Babcock EA, Kessel ST, Hendry AP, Pikitch EK, Ashley MV, Chapman DD (2014) Two decades of genetic profiling yields first evidence of natal philopatry and long-term fidelity to parturition sites in sharks. Mol Ecol 23:110–117
Field IC, Meekan MG, Speed CW, White W, Bradshaw CJA (2010) Quantifying movement patterns for shark conservation at remote coral atolls in the Indian Ocean. Coral Reefs 30:61–71
Friedlander AM, DeMartini EE (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian islands: the effects of fishing down apex predators. Mar Ecol Prog Ser 230:e264
Gilmore RG, Dodrill JW, Linley PA (1983) Reproduction and embryonic development of the sand tiger shark, Odontaspis taurus (Rafinesque). Fish Bull 81:25
Gordon I (1993) Pre-copulatory behaviour of captive sandtiger sharks, Carcharias taurus. The reproduction and development of sharks, skates, rays and ratfishes. Springer, Dordrecht, pp 159–164
Harrison A-L, Costa DP, Winship AJ, Benson SR, Bograd SJ, Antolos M, Carlisle AB, Dewar H, Dutton PH, Jorgensen SJ, Kohin S, Mate BR, Robinson PW, Schaefer KM, Shaffer SA, Shillinger GL, Simmons SE, Weng KC, Gjerde KM, Block BA (2018) The political biogeography of migratory marine predators. Nat Ecol Evol 2:1571–1578
Hays GC, Luschi P, Papi F, del Seppia C, Marsh R (1999) Changes in behaviour during the inter-nesting period and post-nesting migration for Ascension Island green turtles. Mar Ecol Prog Ser 189:263–273
Heupel MR, Reiss KL, Yeiser BG, Simpfendorfer CA (2008) Effects of biofouling on performance of moored data logging acoustic receivers. Limnol Oceanogr Methods 6:327–335
Heupel MR, Simpfendorfer CA, Fitzpatrick R (2010) Large-scale movement and reef fidelity of grey reef sharks. PLoS ONE 5:e9650
Hussey NE, McCarthy ID, Dudley SFJ, Mann BQ (2009) Nursery grounds, movement patterns and growth rates of dusky sharks, Carcharhinus obscurus: a long-term tag and release study in South African waters. Mar Freshw Res 60:571–583
Juhel J-B, Vigliola L, Mouillot D, Kulbicki M, Letessier TB, Meeuwig JJ, Wantiez L (2017) Reef accessibility impairs the protection of sharks. J Appl Ecol 55:673–683
Juhel J-B, Vigliola L, Wantiez L, Letessier TB, Meeuwig JJ, Mouillot D (2019) Isolation and no-entry marine reserves mitigate anthropogenic impacts on grey reef shark behavior. Sci Rep 9:2897
Katona SK, Beard JA (1990) Population size, migrations and feeding aggregations of the humpback whale (Megaptera novaeangliae) in the western North Atlantic Ocean. Int Whal Comn 12:295–305
Momigliano P, Harcourt R, Robbins WD, Jaiteh V, Mahardika GN, Sembiring A, Stow A (2017) Genetic structure and signatures of selection in grey reef sharks (Carcharhinus amblyrhynchos). Heredity 119(3):142
Momigliano P, Harcourt R, Robbins WD, Stow A (2015) Connectivity in grey reef sharks (Carcharhinus amblyrhynchos) determined using empirical and simulated genetic data. Sci Rep 5:13229
Mourier J, Maynard J, Parravicini V, Ballesta L, Clua E, Domeier ML, Planes S (2016) Extreme inverted trophic pyramid of reef sharks supported by spawning groupers. Curr Biol 26:2011–2016
Owen M, Gullestad N (1984) Migration routes of Svalbard barnacle geese Branta leucopsis with a preliminary report on the importance of the Bjørnöya staging area. Nor Polarinst Skr 181:67–78
Papastamatiou YP, Itano DG, Dale JJ, Meyer CG, Holland KN (2010) Site fidelity and movements of sharks associated with ocean-farming cages in Hawaii. Mar Freshw Res 61:1366
Rasher DB, Hoey AS, Hay ME (2017) Cascading predator effects in a Fijian coral reef ecosystem. Sci Rep 7:15684
Read TC, Wantiez L, Werry JM, Farman R, Petro G, Limpus CJ (2014) Migrations of green turtles (Chelonia mydas) between nesting and foraging grounds across the Coral Sea. PLoS ONE 9:e100083
Reyier EA, Franks BR, Chapman DD, Scheidt DM, Stolen ED, Gruber SH (2014) Regional-Scale migrations and habitat use of juvenile lemon sharks (Negaprion brevirostris) in the US South Atlantic. PLoS ONE 9:e88470
Rizzari JR, Frisch AJ, Hoey AS, McCormick MI (2014) Not worth the risk: apex predators suppress herbivory on coral reefs. Oikos 123:829–836
Robbins R, Enarson M, Bradford R, Robbins W, Fox A (2015) Residency and local connectivity of white sharks at Liguanea Island: a second aggregation site in South Australia? Open Fish Sci J 8:23–29
Robbins WD (2006) Abundance, demography and population structure of the grey reef shark (Carcharhinus amblyrhynchos) and the white tip reef shark (Triaenodon obesus) (Fam. Charcharhinidae). Ph.D. thesis, James Cook University
Robbins WD, Hisano M, Connolly SR, Choat JH (2006) Ongoing collapse of coral-reef shark populations. Curr Biol 16:2314–2319
Robbins WD, Renaud P (2015) Foraging mode of the grey reef shark, Carcharhinus amblyrhynchos, under two different scenarios. Coral Reefs 35:253–260
Roff G, Doropoulos C, Rogers A, Bozec Y-M, Krueck NC, Aurellado E, Priest M, Birrell C, Mumby PJ (2016) The ecological role of sharks on coral reefs. Trends Ecol Evol 31:395–407
Shiffman DS, Hammerschlag N (2016) Shark conservation and management policy: a review and primer for non-specialists. Anim Conserv 19:401–412
Thirgood S, Mosser A, Tham S, Hopcraft G, Mwangomo E, Mlengeya T, Kilewo M, Fryxell J, Sinclair ARE, Borner M (2004) Can parks protect migratory ungulates? The case of the Serengeti wildebeest. Anim Conserv Forum 7:113–120
Urquhart FA, Urquhart NR (1978) Autumnal migration routes of the eastern population of the monarch butterfly (Danaus p. plexippus L.; Danaidae; Lepidoptera) in North America to the overwintering site in the Neovolcanic Plateau of Mexico. Can J Zool 56:1759–1764
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
Werry JM, Planes S, Berumen ML, Lee KA, Braun CD, Clua E (2014) Reef-fidelity and migration of tiger sharks, Galeocerdo cuvier, across the coral sea. PLoS ONE 9:e83249
White TD, Carlisle AB, Kroodsma DA, Block BA, Casagrandi R, De Leo GA, Gatto M, Micheli F, McCauley DJ (2017) Assessing the effectiveness of a large marine protected area for reef shark conservation. Biol Conserv 207:64–71
Acknowledgements
We thank the crew of the research vessel Amborella (Government of New Caledonia). This work is an outcome of the APEX project co-funded by the Total Foundation, the Pew Charitable Trusts and the Government of New Caledonia. Animals were handled according to current legislation of the New Caledonian Government (Permit no. 2015-1351/GNC), the South Province (Permit no. 479-2016/ARR/DENV) and the North Province (Permit no. 60912-1508-2015/JJC). We thank the Millenium Coral Reef Mapping Project for providing shapefiles used for the map fonts.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, L. Bonnin states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Topic Editor Michael Lee Berumen
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bonnin, L., Robbins, W.D., Boussarie, G. et al. Repeated long-range migrations of adult males in a common Indo-Pacific reef shark. Coral Reefs 38, 1121–1132 (2019). https://doi.org/10.1007/s00338-019-01858-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-019-01858-w