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RESEARCH ARTICLE

New insights into the reproductive biology of the tiger shark Galeocerdo cuvier and no detection of polyandry in Reunion Island, western Indian Ocean

Agathe Pirog A , Hélène Magalon A B , Thomas Poirout A and Sébastien Jaquemet A C
+ Author Affiliations
- Author Affiliations

A UMR ENTROPIE (Université de La Réunion/IRD/CNRS), Université de La Réunion, 15 Avenue René Cassin, CS 92003, 97744 Saint Denis Cedex 09, La Réunion, France.

B Laboratoire d’Excellence CORAIL, 58 Avenue Paul Alduy, 66860 Perpignan Cedex, France.

C Corresponding author. Email: sebastien.jaquemet@univ-reunion.fr

Marine and Freshwater Research 71(10) 1301-1312 https://doi.org/10.1071/MF19244
Submitted: 10 December 2018  Accepted: 20 January 2020   Published: 31 March 2020

Abstract

The reproductive biology of the tiger shark Galeocerdo cuvier remains poorly documented because it is difficult to obtain data on a sufficient number of mature individuals to conduct appropriate analyses and thus to adequately investigate its population biology. In this study, the reproductive traits of 150 individuals caught during a shark control program in Reunion Island (western Indian Ocean), including five gravid females, were investigated. Specific microsatellite loci were used to investigate the occurrence of polyandry. The total length (TL) of the studied individuals was 130–415 cm for males and 175–429 cm for females. Sizes at maturity were estimated at 278.5 cm for males and 336 cm for females. Although the length–weight relationships differed between both sexes (analysis of covariance (ANCOVA): intercept, n = 49, F1,45 = 0.95, P = 0.34; slope, n = 49, F1,45 = 8.39, P = 0.01), the TL–frequency distributions did not differ significantly. Parturition likely occurs during the warm season, in December–January. No evidence of genetic polyandry was detected, and this supports recently published results. This absence of polyandry in the species likely reflects both a long reproductive cycle and a specific reproductive behaviour related to the oceanic nature of the tiger shark. These results are valuable for improving conservation and management plans for this species.

Additional keywords: Carcharhinidae, gonadosomatic index, microsatellites, monoandry, reproductive traits, size at sexual maturity.


References

Afonso, A. S., and Hazin, F. H. V. (2014). Post-release survival and behavior and exposure to fisheries in juvenile tiger sharks, Galeocerdo cuvier, from the South Atlantic. Journal of Experimental Marine Biology and Ecology 454, 55–62.
Post-release survival and behavior and exposure to fisheries in juvenile tiger sharks, Galeocerdo cuvier, from the South Atlantic.Crossref | GoogleScholarGoogle Scholar |

Bass, A. J., D’Aubrey, J. D., and Kistnasamy, N. (1975). ‘Sharks of the East Coast of Southern Africa. III. The Families Carcharhinidae (Excluding Mustelus and Carcharhinus) and Sphyrnidae.’ (The Oceanographic Research Institute, South African Association for Marine Biological Research: Durban, South Africa.)

Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J., and Doherty, P. A. (2003). Collapse and conservation of shark populations in the northwest Atlantic. Science 299, 389–392.
Collapse and conservation of shark populations in the northwest Atlantic.Crossref | GoogleScholarGoogle Scholar | 12532016PubMed |

Bernard, A. M., Feldheim, K. A., and Shivji, M. S. (2015). Isolation and characterization of polymorphic microsatellite markers from a globally distributed marine apex predator, the tiger shark (Galeocerdo cuvier). Conservation Genetics Resources 7, 509–511.
Isolation and characterization of polymorphic microsatellite markers from a globally distributed marine apex predator, the tiger shark (Galeocerdo cuvier).Crossref | GoogleScholarGoogle Scholar |

Bernard, A. M., Feldheim, K. A., Heithaus, M. R., Wintner, S. P., Wetherbee, B. M., and Shivji, M. S. (2016). Global population genetic dynamics of a highly migratory, apex predator shark. Molecular Ecology 25, 5312–5329.
Global population genetic dynamics of a highly migratory, apex predator shark.Crossref | GoogleScholarGoogle Scholar | 27662523PubMed |

Bigelow, H. B., and Schroeder, W. C. (1948). ‘Fishes of the Western North Atlantic: Lancelets, Cyclostomes, Sharks. Part 1.’ (Yale University, Sears Foundation for Marine Research: New Haven, CT, USA.)

Blaison, A., Jaquemet, S., Guyomard, D., Vangrevelynghe, G., Gazzo, T., Cliff, G., Cotel, P., and Soria, M. (2015). Seasonal variability of bull and tiger shark presence on the west coast of Reunion Island, western Indian Ocean. African Journal of Marine Science 37, 199–208.
Seasonal variability of bull and tiger shark presence on the west coast of Reunion Island, western Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Braccini, J. M., Gillanders, B. M., and Walker, T. I. (2006). Determining reproductive parameters for population assessments of chondrichthyan species with asynchronous ovulation and parturition: piked spurdog (Squalus megalops) as a case study. Marine and Freshwater Research 57, 105–119.
Determining reproductive parameters for population assessments of chondrichthyan species with asynchronous ovulation and parturition: piked spurdog (Squalus megalops) as a case study.Crossref | GoogleScholarGoogle Scholar |

Branstetter, S., Musick, J. A., and Colvocoresses, J. A. (1987). A comparison of the age and growth of the tiger shark, Galeocerdo cuvieri, from off Virginia and from the northwestern Gulf of Mexico. Fishery Bulletin 85, 269–279.

Burkholder, D. A., Heithaus, M. R., Fourqurean, J. W., Wirsing, A., and Dill, L. M. (2013). Patterns of top-down control in a seagrass ecosystem: could a roving apex predator induce a behaviour-mediated trophic cascade? Journal of Animal Ecology 82, 1192–1202.
Patterns of top-down control in a seagrass ecosystem: could a roving apex predator induce a behaviour-mediated trophic cascade?Crossref | GoogleScholarGoogle Scholar | 23730871PubMed |

Byrne, R. J., and Avise, J. C. (2012). Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species. Marine Biology 159, 749–756.
Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species.Crossref | GoogleScholarGoogle Scholar |

Campana, S. E., and Ferretti, F. (2016). Sharks and other elasmobranchs. In ‘The First Global Integrated Marine Assessment: World Ocean Assessment I’. (Ed. United Nations.) pp. 781–788. (Cambridge University Press: Cambridge, UK.)

Castro, J. I. (2011). ‘The Sharks of North America.’ (Oxford University Press: New York, NY, USA.)

Castro, J. I., Sato, K., and Bodine, A. B. (2016). A novel mode of embryonic nutrition in the tiger shark, Galeocerdo cuvier. Marine Biology Research 12, 200–205.
A novel mode of embryonic nutrition in the tiger shark, Galeocerdo cuvier.Crossref | GoogleScholarGoogle Scholar |

Chakravarti, I. M., Laha, R. G., and Roy, J. (1967). ‘Handbook of Methods of Applied Statistics.’ (John Wiley: New York, NY, USA.)

Chapman, D. D., Prodohl, P. A., Gelsleichter, J., Manire, C. A., and Shivji, M. S. (2004). Predominance of genetic monogamy by females in a hammerhead shark, Sphyrna tiburo: implications for shark conservation. Molecular Ecology 13, 1965–1974.
Predominance of genetic monogamy by females in a hammerhead shark, Sphyrna tiburo: implications for shark conservation.Crossref | GoogleScholarGoogle Scholar | 15189217PubMed |

Clark, E., and von Schmidt, K. (1965). Sharks of the central Gulf Coast of Florida. Bulletin of Marine Science 15, 13–83.

Clarke, S. C., McAllister, M. K., Milner-Gulland, E. J., Kirkwood, G. P., Michielsens, C. G. J., Agnew, D. J., Pikitch, E. K., Nakano, H., and Shivji, M. S. (2006). Global estimates of shark catches using trade records from commercial markets. Ecology Letters 9, 1115–1126.
Global estimates of shark catches using trade records from commercial markets.Crossref | GoogleScholarGoogle Scholar | 16972875PubMed |

Cliff, G., and Dudley, S. F. J. (1991). Sharks caught in the protective gill nets off Natal, South Africa. 4. The bull shark Carcharhinus leucas Valenciennes. South African Journal of Marine Science 10, 253–270.
Sharks caught in the protective gill nets off Natal, South Africa. 4. The bull shark Carcharhinus leucas Valenciennes.Crossref | GoogleScholarGoogle Scholar |

Cloern, J. E., Abreu, P. C., Carstensen, J., Chauvaud, L., Elmgren, R., Grall, J., Greening, H., Johansson, J. O. R., Kahru, M., Sherwood, E. T., Xu, J., and Yin, K. (2016). Human activities and climate variability drive fast-paced change across the world’s estuarine–coastal ecosystems. Global Change Biology 22, 513–529.
Human activities and climate variability drive fast-paced change across the world’s estuarine–coastal ecosystems.Crossref | GoogleScholarGoogle Scholar | 26242490PubMed |

Compagno, L. J. V. (1984). ‘FAO Species Catalogue: Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 2 – Carcharhiniformes.’ (FAO: Rome, Italy.)

Conrath, C. L., Musick, J. A., Carrier, J. C., and Heithaus, M. R. (2012). Reproductive biology of elasmobranchs. In ‘Biology of Sharks and their Relatives’. 2nd edn. (Eds J. C. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 291–311. (CRC Press, Taylor & Francis Group: Boca Raton, FL, USA.)

Cortés, E. (1998). Demographic analysis as an aid in shark stock assessment and management. Fisheries Research 39, 199–208.
Demographic analysis as an aid in shark stock assessment and management.Crossref | GoogleScholarGoogle Scholar |

Cortés, E. (2002). Incorporating uncertainty into demographic modeling: application to shark populations and their conservation. Conservation Biology 16, 1048–1062.
Incorporating uncertainty into demographic modeling: application to shark populations and their conservation.Crossref | GoogleScholarGoogle Scholar |

Daly-Engel, T. S., Grubbs, R. D., Holland, K. N., Toonen, R. J., and Bowen, B. W. (2006). Assessment of multiple paternity in single litters from three species of carcharhinid sharks in Hawaii. Environmental Biology of Fishes 76, 419–424.
Assessment of multiple paternity in single litters from three species of carcharhinid sharks in Hawaii.Crossref | GoogleScholarGoogle Scholar |

Daly-Engel, T. S., Grubbs, R. D., Bowen, B. W., and Toonen, R. J. (2007). Frequency of multiple paternity in an unexploited tropical population of sandbar sharks (Carcharhinus plumbeus). Canadian Journal of Fisheries and Aquatic Sciences 64, 198–204.
Frequency of multiple paternity in an unexploited tropical population of sandbar sharks (Carcharhinus plumbeus).Crossref | GoogleScholarGoogle Scholar |

De Crosta, M. A., Taylor, L. R. J., and Parrish, J. D. (1984). Age determination, growth, and energetics of three species of carcharhinid sharks in Hawaii. In ‘Proceedings of the Second Symposium on Resource Investigations of the NW Hawaiian Islands’. 25–27 May 1983. (Eds R. W. Grigg and K. Y. Tanoue.) pp. 75–95. (University of Hawaii: Honolulu, HI, USA.)

Dibattista, J. D., Feldheim, K. A., Thibert-Plante, X., Gruber, S. H., and Hendry, A. P. (2008). A genetic assessment of polyandry and breeding-site fidelity in lemon sharks. Molecular Ecology 17, 3337–3351.
A genetic assessment of polyandry and breeding-site fidelity in lemon sharks.Crossref | GoogleScholarGoogle Scholar | 18564083PubMed |

Dicken, M. L., Cliff, G., and Winker, H. (2016). Sharks caught in the KwaZulu-Natal bather protection programme, South Africa. 13. The tiger shark Galeocerdo cuvier. African Journal of Marine Science 38, 285–301.
Sharks caught in the KwaZulu-Natal bather protection programme, South Africa. 13. The tiger shark Galeocerdo cuvier.Crossref | GoogleScholarGoogle Scholar |

Dudley, S. F. J. (1997). A comparison of the shark control programs of New South Wales and Queensland (Australia) and KwaZulu-Natal (South Africa). Ocean and Coastal Management 34, 1–27.
A comparison of the shark control programs of New South Wales and Queensland (Australia) and KwaZulu-Natal (South Africa).Crossref | GoogleScholarGoogle Scholar |

Dudley, S. F. J., and Simpfendorfer, C. A. (2006). Population status of 14 shark species caught in the protective gillnets off KwaZulu-Natal beaches, South Africa, 1978–2003. Marine and Freshwater Research 57, 225–240.
Population status of 14 shark species caught in the protective gillnets off KwaZulu-Natal beaches, South Africa, 1978–2003.Crossref | GoogleScholarGoogle Scholar |

Dulvy, N. K., Fowler, S. L., Musick, J. A., Cavanagh, R. D., Kyne, P. M., Harrison, L. R., Carlson, J. K., Davidson, L. N. K., Fordham, S. V., and Francis, M. P. (2014). Extinction risk and conservation of the world’s sharks and rays. eLife 3, e00590.
Extinction risk and conservation of the world’s sharks and rays.Crossref | GoogleScholarGoogle Scholar | 24448405PubMed |

Feldheim, K. A., Gruber, S. H., and Ashley, M. V. (2004). Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris. Evolution 58, 2332–2342.
Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris.Crossref | GoogleScholarGoogle Scholar | 15562694PubMed |

Ferretti, F., Worm, B., Britten, G. L., Heithaus, M. R., and Lotze, H. K. (2010). Patterns and ecosystem consequences of shark declines in the ocean. Ecology Letters 13, 1055–1071.
Patterns and ecosystem consequences of shark declines in the ocean.Crossref | GoogleScholarGoogle Scholar | 20528897PubMed |

Fourmanoir, P. (1961). Requins de la côte ouest de Madagascar. Mémoires de l'Institut Scientifique de Madagascar. Série F: Océanographie 4, 3–81.

Green, M. E., Appleyard, S. A., White, W., Tracey, S., and Ovenden, J. (2017). Variability in multiple paternity rates for grey reef sharks (Carcharhinus amblyrhynchos) and scalloped hammerheads (Sphyrna lewini). Scientific Reports 7, 1528–1536.
Variability in multiple paternity rates for grey reef sharks (Carcharhinus amblyrhynchos) and scalloped hammerheads (Sphyrna lewini).Crossref | GoogleScholarGoogle Scholar | 28484261PubMed |

Guyomard, D., Perry, C., Tournoux, P.-H., Cliff, G., Peddemors, V., and Jaquemet, S. (2019). An innovative fishing gear to enhance the release of non-target species in coastal-shark control programs: The SMART (Shark Management Alert in Real-Time) drumline. Fisheries Research 216, 6–17.
An innovative fishing gear to enhance the release of non-target species in coastal-shark control programs: The SMART (Shark Management Alert in Real-Time) drumline.Crossref | GoogleScholarGoogle Scholar |

Heithaus, M. R., Hamilton, I. M., Wirsing, A. J., and Dill, L. M. (2006). Validation of a randomization procedure to assess animal habitat preferences: microhabitat use of tiger sharks in a seagrass ecosystem. Journal of Animal Ecology 75, 666–676.
Validation of a randomization procedure to assess animal habitat preferences: microhabitat use of tiger sharks in a seagrass ecosystem.Crossref | GoogleScholarGoogle Scholar | 16689949PubMed |

Heithaus, M. R., Wirsing, A. J., Dill, L. M., and Heithaus, L. I. (2007). Long-term movements of tiger sharks satellite-tagged in Shark Bay, Western Australia. Marine Biology 151, 1455–1461.
Long-term movements of tiger sharks satellite-tagged in Shark Bay, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Heithaus, M. R., Frid, A., Wirsing, A. J., and Worm, B. (2008). Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution 23, 202–210.
Predicting ecological consequences of marine top predator declines.Crossref | GoogleScholarGoogle Scholar |

Holland, K. N., Anderson, J. M., Coffey, D. M., Holmes, B. J., Meyer, C. G., and Royer, M. A. (2019). A perspective on future tiger shark research. Frontiers in Marine Science 6, .
A perspective on future tiger shark research.Crossref | GoogleScholarGoogle Scholar |

Holmes, B. J., Sumpton, W. D., Mayer, D. G., Tibbetts, I. R., Neil, D. T., and Bennett, M. B. (2012). Declining trends in annual catch rates of the tiger shark (Galeocerdo cuvier) in Queensland, Australia. Fisheries Research 129–130, 38–45.
Declining trends in annual catch rates of the tiger shark (Galeocerdo cuvier) in Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

Holmes, B. J., Peddemors, V. M., Gutteridge, A. N., Geraghty, P. T., Chan, R. W. K., Tibbetts, I. R., and Bennett, M. B. (2015). Age and growth of the tiger shark Galeocerdo cuvier off the East coast of Australia. Journal of Fish Biology 87, 422–448.
Age and growth of the tiger shark Galeocerdo cuvier off the East coast of Australia.Crossref | GoogleScholarGoogle Scholar | 26248806PubMed |

Holmes, B. J., Williams, S. M., Otway, N. M., Nielsen, E. E., Maher, S. L., Bennett, M. B., and Ovenden, J. R. (2017). Population structure and connectivity of tiger sharks (Galeocerdo cuvier) across the Indo-Pacific Ocean basin. Royal Society Open Science 4, 170309.
Population structure and connectivity of tiger sharks (Galeocerdo cuvier) across the Indo-Pacific Ocean basin.Crossref | GoogleScholarGoogle Scholar | 29291060PubMed |

Holmes, B. J., Pope, L. C., Williams, S. M., Tibbetts, I. R., Bennett, M. B., and Ovenden, J. R. (2018). Lack of multiple paternity in the oceanodromous tiger shark (Galeocerdo cuvier). Royal Society Open Science 5, 171385.
Lack of multiple paternity in the oceanodromous tiger shark (Galeocerdo cuvier).Crossref | GoogleScholarGoogle Scholar | 29410842PubMed |

Jaquemet, S., Smale, M. J., Blaison, A., Guyomard, D., and Soria, M. (2013). First observation of a pregnant tiger shark (Galeocerdo cuvier) in Reunion Island, Western Indian Ocean. Western Indian Ocean Journal of Marine Science 11, 205–207.

Jones, O. R., and Wang, J. L. (2010). COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources 10, 551–555.
COLONY: a program for parentage and sibship inference from multilocus genotype data.Crossref | GoogleScholarGoogle Scholar | 21565056PubMed |

Keeney, D. B., and Heist, E. J. (2003). Characterization of microsatellite loci isolated from the blacktip shark and their utility in requiem and hammerhead sharks. Molecular Ecology Notes 3, 501–504.
Characterization of microsatellite loci isolated from the blacktip shark and their utility in requiem and hammerhead sharks.Crossref | GoogleScholarGoogle Scholar |

Kneebone, J., Natanson, L. J., Andrews, A. H., and Howell, W. H. (2008). Using bomb radiocarbon analyses to validate age and growth estimates for the tiger shark, Galeocerdo cuvier, in the western North Atlantic. Marine Biology 154, 423–434.
Using bomb radiocarbon analyses to validate age and growth estimates for the tiger shark, Galeocerdo cuvier, in the western North Atlantic.Crossref | GoogleScholarGoogle Scholar |

Kohler, N. E., Casey, J. G., and Turner, P. A. (1995). Length–weight relationships for 13 species of sharks from the western North Atlantic. Fisheries Bulletin 93, 412–418.

Lowe, C. G., Wetherbee, B. M., Crow, G. L., and Tester, A. L. (1996). Ontogenetic dietary shifts and feeding behavior of the tiger shark, Galeocerdo cuvier, in Hawaiian waters. Environmental Biology of Fishes 47, 203–211.
Ontogenetic dietary shifts and feeding behavior of the tiger shark, Galeocerdo cuvier, in Hawaiian waters.Crossref | GoogleScholarGoogle Scholar |

McCauley, D. J., Pinsky, M. L., Palumbi, S. R., Estes, J. A., Joyce, F. H., and Warner, R. R. (2015). Marine defaunation: animal loss in the global ocean. Science 347, 1255641.
Marine defaunation: animal loss in the global ocean.Crossref | GoogleScholarGoogle Scholar | 25593191PubMed |

Mendes, N. J., Cruz, V. P., Ashikaga, F. Y., Camargo, S. M., Oliveira, C., Piercy, A. N., Burgess, G. H., Coelho, R., Santos, M. N., Mendonça, F. F., and Foresti, F. (2016). Microsatellite loci in the tiger shark and cross-species amplification using pyrosequencing technology. PeerJ 4, e2205.
Microsatellite loci in the tiger shark and cross-species amplification using pyrosequencing technology.Crossref | GoogleScholarGoogle Scholar | 27635306PubMed |

Meyer, C. G., O’Malley, J. M., Papastamatiou, Y. P., Dale, J. J., Hutchinson, M. R., Anderson, J. M., Royer, M. A., and Holland, K. N. (2014). Growth and maximum size of tiger sharks (Galeocerdo cuvier) in Hawaii. PLoS One 9, e84799.
Growth and maximum size of tiger sharks (Galeocerdo cuvier) in Hawaii.Crossref | GoogleScholarGoogle Scholar | 24416287PubMed |

Musick, J. A. (2010). Chondrichthyan reproduction. In ‘Reproduction and Sexuality in Marine Fishes’. (Ed. K. S. Cole.) pp. 3–20. (University of California Press: Berkeley, CA, USA.)

Musick, J. A., Burgess, G., Cailliet, G., Camhi, M., and Fordham, S. (2000). Management of sharks and their relatives (Elasmobranchii). Fisheries 25, 9–13.
Management of sharks and their relatives (Elasmobranchii).Crossref | GoogleScholarGoogle Scholar |

Myers, R. A., and Worm, B. (2003). Rapid worldwide depletion of predatory fish communities. Nature 423, 280–283.
Rapid worldwide depletion of predatory fish communities.Crossref | GoogleScholarGoogle Scholar | 12748640PubMed |

Myers, R. A., and Worm, B. (2005). Extinction, survival or recovery of large predatory fishes. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 13–20.
Extinction, survival or recovery of large predatory fishes.Crossref | GoogleScholarGoogle Scholar | 15713586PubMed |

Natanson, L. J., Casey, J. G., Kohler, N. E., and Colket, T. (1999). Growth of the tiger shark, Galeocerdo cuvier, in the Western North Atlantic based on tag returns and length frequencies; and a note on the effects of tagging. Fishery Bulletin 97, 944–953.

Neff, B. D., and Pitcher, T. E. (2002). Assessing the statistical power of genetic analyses to detect multiple mating in fishes. Journal of Fish Biology 61, 739–750.
Assessing the statistical power of genetic analyses to detect multiple mating in fishes.Crossref | GoogleScholarGoogle Scholar |

Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37, 637–669.

Parsons, G. R., Hoffmayer, E. R., Frank, J., and Bet-Sayad, W. V. (2008). A review of shark reproductive ecology: LIFE history and evolutionary implications. In ‘Fish Reproduction’. 1st edn. (Eds M. J. Rocha, A. Aruke, and B. G. Kapoor.) pp. 435–469. (CRC Press: Boca Raton, FL, USA.)

Pienaar, L. V., and Thomson, J. A. (1969). Allometric weight–length regression model. Journal of the Fisheries Research Board of Canada 26, 123–131.
Allometric weight–length regression model.Crossref | GoogleScholarGoogle Scholar |

Pirog, A. (2018). Structure génétique des populations et biologie de la reproduction chez le requin bouledogue Carcharhinus leucas et le requin tigre Galeocerdo cuvier. Ph.D. Thesis, University of La Réunion, Saint-Denis, France.

Pirog, A., Blaison, A., Jaquemet, S., Soria, M., and Magalon, H. (2015). Isolation and characterization of 20 microsatellite markers from Carcharhinus leucas (bull shark) and cross-amplification in Galeocerdo cuvier (tiger shark), Carcharhinus obscurus (dusky shark) and Carcharhinus plumbeus (sandbar shark). Conservation Genetics Resources 7, 121–124.
Isolation and characterization of 20 microsatellite markers from Carcharhinus leucas (bull shark) and cross-amplification in Galeocerdo cuvier (tiger shark), Carcharhinus obscurus (dusky shark) and Carcharhinus plumbeus (sandbar shark).Crossref | GoogleScholarGoogle Scholar |

Pirog, A., Jaquemet, S., Blaison, A., Soria, M., and Magalon, H. (2016). Isolation and characterization of eight microsatellite loci from Galeocerdo cuvier (tiger shark) and cross-amplification in Carcharhinus leucas, Carcharhinus brevipinna, Carcharhinus plumbeus and Sphyrna lewini. PeerJ 4, e2041.
Isolation and characterization of eight microsatellite loci from Galeocerdo cuvier (tiger shark) and cross-amplification in Carcharhinus leucas, Carcharhinus brevipinna, Carcharhinus plumbeus and Sphyrna lewini.Crossref | GoogleScholarGoogle Scholar | 27231661PubMed |

Pirog, A., Jaquemet, S., Soria, M., and Magalon, H. (2017). First evidence of multiple paternity in the bull shark (Carcharhinus leucas). Marine and Freshwater Research 68, 195–201.
First evidence of multiple paternity in the bull shark (Carcharhinus leucas).Crossref | GoogleScholarGoogle Scholar |

Pirog, A., Jaquemet, S., Cliff, G., Holmes, B. J., Hussey, N. E., Nevill, J. E. G., Temple, A. J., Vigliola, L., and Magalon, H. (2019a). Genetic population structure and demography of an apex predator, the tiger shark Galeocerdo cuvier. Ecology and Evolution 9, 5551–5571.
Genetic population structure and demography of an apex predator, the tiger shark Galeocerdo cuvier.Crossref | GoogleScholarGoogle Scholar | 31160982PubMed |

Pirog, A., Magalon, H., Poirout, T., and Jaquemet, S. (2019b). Reproductive biology, multiple paternity and polyandry of the bull shark Carcharhinus leucas. Journal of Fish Biology 95, 1195–1206.
Reproductive biology, multiple paternity and polyandry of the bull shark Carcharhinus leucas.Crossref | GoogleScholarGoogle Scholar | 31393599PubMed |

Polovina, J. J., and Lau, B. B. (1993). Temporal and spatial distribution of catches of tiger sharks, Galeocerdo cuvier, in the pelagic longline fishery around the Hawaiian Islands. Marine Fisheries Review 55, 1–3.

Portnoy, D. S., Piercy, A. N., Musick, J. A., Burgess, G. H., and Graves, J. E. (2007). Genetic polyandry and sexual conflict in the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic and Gulf of Mexico. Molecular Ecology 16, 187–197.
Genetic polyandry and sexual conflict in the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic and Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar | 17181730PubMed |

Pratt, H. L. (1993). The storage of spermatozoa in the oviducal glands of western North-Atlantic sharks. Environmental Biology of Fishes 38, 139–149.
The storage of spermatozoa in the oviducal glands of western North-Atlantic sharks.Crossref | GoogleScholarGoogle Scholar |

Randall, J. E. (1992). Review of the biology of the tiger shark (Galeocerdo cuvier). Australian Journal of Marine and Freshwater Research 43, 21–31.
Review of the biology of the tiger shark (Galeocerdo cuvier).Crossref | GoogleScholarGoogle Scholar |

Reid, D. D., and Krogh, M. (1992). Assessment of catches from protective shark meshing off New South Wales beaches between 1950 and 1990. Marine and Freshwater Research 43, 283–296.
Assessment of catches from protective shark meshing off New South Wales beaches between 1950 and 1990.Crossref | GoogleScholarGoogle Scholar |

Rossouw, C., Wintner, S. P., and Bester-Van Der Merwe, A. E. (2016). Assessing multiple paternity in three commercially exploited shark species: Mustelus mustelus, Carcharhinus obscurus and Sphyrna lewini. Journal of Fish Biology 89, 1125–1141.
Assessing multiple paternity in three commercially exploited shark species: Mustelus mustelus, Carcharhinus obscurus and Sphyrna lewini.Crossref | GoogleScholarGoogle Scholar | 27237109PubMed |

Simpfendorfer, C. A. (1992). Biology of tiger sharks (Galeocerdo cuvier) caught by the Queensland shark meshing program off Townsville, Australia. Australian Journal of Marine and Freshwater Research 43, 33–43.
Biology of tiger sharks (Galeocerdo cuvier) caught by the Queensland shark meshing program off Townsville, Australia.Crossref | GoogleScholarGoogle Scholar |

Simpfendorfer, C. A. (2009) Tiger shark Galeocerdo cuvier. The IUCN Red List of Threatened Species. Version 2015.1. Available at: https://www.iucnredlist.org/species/39378/2913541 [verified 24 January 2020].

Stehmann, M. F. W. (2002). Proposal of a maturity stages scale for oviparous and viviparous cartilaginous fishes (Pisces, Chondrichthyes). Arquive of Fishery and Marine Research 50, 23–48.

Stevenson, R. D., and Woods, W. A. (2006). Condition indices for conservation: new uses for evolving tools. Integrative and Comparative Biology 46, 1169–1190.
Condition indices for conservation: new uses for evolving tools.Crossref | GoogleScholarGoogle Scholar | 21672816PubMed |

Sugg, D. W., and Chesser, R. K. (1994). Effective population sizes with multiple paternity. Genetics 137, 1147–1155.
| 7982568PubMed |

Sumpton, W. D., Taylor, S. M., Gribble, N. A., McPherson, G., and Ham, T. (2011). Gear selectivity of large-mesh nets and drumlines used to catch sharks in the Queensland Shark Control Program. African Journal of Marine Science 33, 37–43.
Gear selectivity of large-mesh nets and drumlines used to catch sharks in the Queensland Shark Control Program.Crossref | GoogleScholarGoogle Scholar |

Torrejon-Magallanes, J. (2017). sizeMat: Estimate Size at Sexual Maturity. R Package Version 0.3.0.

Varghese, S. P., Unnikrishnan, N., Gulati, D. K., and Ayoob, A. E. (2017). Size, sex and reproductive biology of seven pelagic sharks in the Eastern Arabian Sea. Journal of the Marine Biological Association of the United Kingdom 97, 181–196.
Size, sex and reproductive biology of seven pelagic sharks in the Eastern Arabian Sea.Crossref | GoogleScholarGoogle Scholar |

Walker, T. I. (2005). Reproduction in fisheries science. In ‘Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Rays and Chimaeras’. (Ed. W. C. Hamlett.) pp. 81–127. (Science Publishers: Enfield, NH, USA.)

Weimerskirch, H. (2007). Are seabirds foraging for unpredictable resources? Deep-sea Research. Part II, Topical Studies in Oceanography 54, 211–223.
Are seabirds foraging for unpredictable resources?Crossref | GoogleScholarGoogle Scholar |

Wetherbee, B. M., Lowe, C. G., and Crow, G. L. (1994). A review of shark control in Hawaii with recommendations for future research. Pacific Science 48, 95–115.

Whitney, N. M., and Crow, G. L. (2007). Reproductive biology of the tiger shark (Galeocerdo cuvier) in Hawaii. Marine Biology 151, 63–70.
Reproductive biology of the tiger shark (Galeocerdo cuvier) in Hawaii.Crossref | GoogleScholarGoogle Scholar |

Wintner, S. P., and Dudley, S. F. J. (2000). Age and growth estimates for the tiger shark, Galeocerdo cuvier, from the east coast of South Africa. Marine and Freshwater Research 51, 43–53.
Age and growth estimates for the tiger shark, Galeocerdo cuvier, from the east coast of South Africa.Crossref | GoogleScholarGoogle Scholar |

Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2007). Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)? Oecologia 153, 1031–1040.
Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)?Crossref | GoogleScholarGoogle Scholar | 17636333PubMed |

Worm, B., Davis, B., Kettemer, L., Ward-Paige, C. A., Chapman, D., Heithaus, M. R., Kessel, S. T., and Gruber, S. H. (2013). Global catches, exploitation rates, and rebuilding options for sharks. Marine Policy 40, 194–204.
Global catches, exploitation rates, and rebuilding options for sharks.Crossref | GoogleScholarGoogle Scholar |

Zeh, J. A., and Zeh, D. W. (2001). Reproductive mode and the genetic benefits of polyandry. Animal Behaviour 61, 1051–1063.
Reproductive mode and the genetic benefits of polyandry.Crossref | GoogleScholarGoogle Scholar |