Significance of Sex-Specific Ecological and Life History Traits on the Sustainable Exploitation of Sharks

  • Yasuko SembaEmail author
Part of the Fisheries Science Series book series (FISHSS)


Sharks, which maintain the role of top predator in aquatic ecosystems, have a reproductive system and life history traits that are quite different from those of most teleosts, including internal fertilization, slow growth, high age at maturity, and the live birth of only a few well-formed offspring. Although shark species show diversity in many traits such as body size, morphology, diet, habitat (vertically, horizontally, and latitudinally), and reproductive system (ovoviviparous and viviparous), sexual difference in various phenotypic traits is one of their major characteristics. Sex-specific phenotypic traits such as life history parameters and sexual segregation are illustrated, focusing on shortfin mako and other species. A survey of the literature on growth suggests that slow growth and large body size in females are a major trend in sharks with significant intersexual difference in growth. Sexual segregation of sharks is reported with varying degrees of resolution, but its pattern is variable depending on the species, and the underlying mechanisms are largely unclear. The implication of intersexual difference in life history and behavioral traits is discussed from both evolutional and practical points of view. Existing studies that have evaluated the effect of sexual difference suggest the importance of including sex-specific traits in stock assessment and management, especially for species with marked sexual difference. Given its significance, both the study of sexual difference in the biological characteristics and the collection of sex-specific information on fishery statistics are important for understanding population dynamics and the sustainable exploitation of shark species.


Behavioral traits Life history traits Mating system Sharks Sexual difference Sexual segregation Sustainable use 


  1. Bansemer CS, Bennett MB (2009) Reproductive periodicity, localized movements and behavioural segregation of pregnant Carcharias taurus at Wolf Rock, southeast Queensland, Australia. Mar Ecol Prog Ser 374:215–227CrossRefGoogle Scholar
  2. Bishop SDH, Francis MP, Duffy C, Montgomery JC (2006) Age, growth, maturity, longevity and natural mortality of the shortfin mako shark (Isurus oxyrinchus) in New Zealand waters. Mar Freshw Res 57:143–154CrossRefGoogle Scholar
  3. Boomer JJ, Harcourt RG, Francis MP, Walker TI, Braccini JM, Stow AJ (2013) Frequency of multiple paternity in gummy shark, Mustelus antarcticus, and rig, Mustelus lenticulatus, and the implications of mate encounter rate, postcopulatory influences, and reproductive mode. J Hered 104(3):371–379CrossRefPubMedGoogle Scholar
  4. Byrne RJ, Avise JC (2012) Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species. Mar Biol 159(4):749–756CrossRefGoogle Scholar
  5. Cailliet GM, Goldman KJ (2004) Age determination and validation in Chondrichthyan fishes. In: Carrier J, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press LLC, Boca Raton, pp 399–447Google Scholar
  6. Carrier JC, Pratt HL Jr, Castro JI (2004) Reproductive biology of elasmobranchs. In: Carrier J, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press LLC, Boca Raton, pp 269–286CrossRefGoogle Scholar
  7. Cerna F, Licandeo R (2009) Age and growth of the shortfin mako (Isurus oxyrinchus) in the south-eastern Pacific off Chile. Mar Freshw Res 60:394–403CrossRefGoogle Scholar
  8. Chabot CL, Haggin BM (2014) Frequency of multiple paternity varies between two populations of brown smoothhound shark, Mustelus henlei. Mar Biol 161:797–804CrossRefGoogle Scholar
  9. Chapman DD, Prodöhl PA, Gelsleichter J, Manire CA, Shivji MS (2004) Predominance of genetic monogamy by females in a hammerhead shark, Sphyrna tiburo: implications for shark conservation. Mol Ecol 13(7):1965–1974CrossRefPubMedGoogle Scholar
  10. Chapman DD, Wintner SP, Abercrombie DL, Ashe J, Bernard AM, Shivji MS, Feldheim KA (2013) The behavioural and genetic mating system of the sand tiger shark, Carcharias taurus, an intrauterine cannibal. Biol Lett 9(3):20130003CrossRefPubMedPubMedCentralGoogle Scholar
  11. Compagno LJV (2001) Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Vol. 2. Bullhead, mackerel and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO Species Catalogue for Fishery Purposes. No. 1, Vol. 2. FAO, Rome, 269 ppGoogle Scholar
  12. Conradt L (2005) Definitions, hypotheses, models and measures in the study of animal segregation. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation in vertebrates. Cambridge University Press, Cambridge, pp 11–32Google Scholar
  13. Corrigan S, Kacev D, Werry J (2015) A case of genetic polyandry in the shortfin mako Isurus oxyrinchus. J Fish Biol 87:794–798CrossRefPubMedGoogle Scholar
  14. Cortés E (2000) Life history patterns and correlations in sharks. Rev Fish Sci 8(4):299–344CrossRefGoogle Scholar
  15. Cortés E, Arocha F, Beerkircher L, Carvalho F, Domingo A, Heupel M, Holtzhausen H, Santos MN, Ribera M, Simpfendorfer C (2010) Ecological risk assessment of pelagic sharks caught in Atlantic pelagic longline fisheries. Aquat Living Resour 23:25–34CrossRefGoogle Scholar
  16. Daly-Engel TS, Grubbs RD, Holland KN, Toonen RJ, Bowen BW (2006) Assessment of multiple paternity in single litters from three species of carcharhinid sharks in Hawaii. Environ Biol Fish 76:419–424CrossRefGoogle Scholar
  17. Daly-Engel TS, Grubbs RD, Bowen BW, Toonen RJ (2007) Frequency of multiple paternity in an unexploited tropical population of sandbar sharks (Carcharhinus plumbeus). Can J Fish Aquat Sci 64:198–204CrossRefGoogle Scholar
  18. Daly-Engel TS, Grubbs RD, Feldheim KA, Bowen BW, Toonen RJ (2010) Is multiple mating beneficial or unavoidable? Low multiple paternity and genetic diversity in the shortspine spurdog Squalus mitsukurii. Mar Ecol Prog Ser 403:255–267CrossRefGoogle Scholar
  19. Dell’Apa A, Cudney-Burch J, Kimmel DG, Rulifson RA (2014) Sexual segregation of spiny dogfish in fishery-dependent survey in Cape Cod, Massachusetts: potential management benefits. Trans Am Fish Soc 143(4):833–844CrossRefGoogle Scholar
  20. DiBattista JD, Feldheim KA, Thibert-Plante X, Gruber SH, Hendry AP (2008a) A genetic assessment of polyandry and breeding-site fidelity in lemon sharks. Mol Ecol 17:3337–3351CrossRefPubMedGoogle Scholar
  21. DiBattista JD, Feldheim KA, Gruber SH, Hendry AP (2008b) Are direct genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks. Mol Ecol 17:783–795CrossRefPubMedGoogle Scholar
  22. Farrell ED, O’Sullivan N, Sacchi C, Mariani S (2014) Multiple paternity in the starry smooth-hound shark Mustelus asterias (Carcharhiniformes: Triakidae). Biol J Linn Soc 111(1):119–125CrossRefGoogle Scholar
  23. Feldheim KA, Gruber SH, Ashley MV (2001a) Multiple paternity of a lemon shark litter (Chondrichthyes: Carcharhinidae). Copeia 3:781–786CrossRefGoogle Scholar
  24. Feldheim KA, Gruber SH, Ashley MV (2001b) Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite variation. Mol Ecol 10(2):295–303CrossRefPubMedGoogle Scholar
  25. Francis MP, Duffy C (2005) Length at maturity in three pelagic sharks (Lamna nasus, Isurus oxyrinchus, and Prionace glauca) from New Zealand. Fish Bull 103:489–500Google Scholar
  26. Gerber LR, White ER (2014) Two-sex matrix models in assessing population viability: when do male dynamics matter? J Appl Ecol 51:270–278CrossRefGoogle Scholar
  27. Griffiths AM, Jacoby DMP, Casane D, McHugh M, Croft DP, Genner MJ, Sims DW (2012) First analysis of multiple paternity in an oviparous shark, the small-spotted catshark (Scyliorhinus canicula L.) J Hered 103(2):166–173CrossRefPubMedGoogle Scholar
  28. Heist EJ, Carrier JC, Pratt HL Jr, Pratt TC (2011) Exact enumeration of sires in the polyandrous nurse shark (Ginglymostoma cirratum). Copeia 4:539–544CrossRefGoogle Scholar
  29. Holden MJ (1973) Are long-term sustainable fisheries for elasmobranchs possible? Rapp P-V Réun Cons Int Explor Mer 164:360–367Google Scholar
  30. Holden MJ (1977) Elasmobranchs. In: Gulland J (ed) Fish population dynamics. Wiley, London, pp 187–215Google Scholar
  31. Joung SJ, Hsu HH (2005) Reproduction and embryonic development of the shortfin mako, Isurus oxyrinchus Rafinesque, 1810, in the Northwestern Pacific. Zool Stud 44(4):487–496Google Scholar
  32. Karkach AS (2006) Trajectories and models of individual growth. Demogr Res 15:347–400CrossRefGoogle Scholar
  33. Klimley AP (1987) The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environ Biol Fish 18:27–40CrossRefGoogle Scholar
  34. Kock A, O’Riain MJ, Mauff K, Meÿer M, Kotze D, Griffiths C (2013) Residency, habitat use and sexual segregation of white sharks, Carcharodon carcharias in False Bay, South Africa. PLoS One 8(1):e55048CrossRefPubMedPubMedCentralGoogle Scholar
  35. Krebs JR, Davis NB (1993) An introduction to behavioural ecology. Blackwell Publishing, OxfordGoogle Scholar
  36. Lage CR, Petersen CW, Forest D, Barnes D, Kornfield I, Wray C (2008) Evidence of multiple paternity in spiny dogfish (Squalus acanthias) broods based on microsatellite analysis. J Fish Biol 73(8):2068–2074CrossRefGoogle Scholar
  37. Larson S, Christiansen J, Griffing D, Ashe J, Lowry D, Andrews K (2011) Relatedness and polyandry of sixgill sharks, Hexanchus griseus, in an urban estuary. Conserv Genet 12(3):679–690CrossRefGoogle Scholar
  38. Lee H-H, Piner KR, Hinton MG, Chang Y-J, Kimoto A, Kanaiwa M, Su N-J, Walsh W, Sun C-L, DiNardo G (2014) Sex-structured population dynamics of blue marlin Makaira nigricans in the Pacific Ocean. Fish Sci 80(5):869–878CrossRefGoogle Scholar
  39. Magurran AE, Garcia CM (2000) Sex differences in behaviour as an indirect consequence of mating system. J Fish Biol 57(4):839–857CrossRefGoogle Scholar
  40. Maia A, Queiroz N, Cabral HN, Santos AM, Correia JP (2007) Reproductive biology and population dynamics of shortfin mako, Isurus oxyrinchus Rafinesque, 1810, off the southwest Portuguese coast, eastern North Atlantic. J Appl Ichthyol 23:246–251CrossRefGoogle Scholar
  41. Milner JM, Nilsen EB, Andreassen HP (2007) Demographic side effects of selective hunting in ungulates and carnivores. Conserv Biol 21(1):36–47CrossRefPubMedGoogle Scholar
  42. Mollet HF, Cliff G, Pratt HL Jr, Stevens JD (2000) Reproductive biology of the female shortfin mako, Isurus oxyrinchus Rafinesque, 1810, with comments on the embryonic development of lamnoids. Fish Bull 98:299–318Google Scholar
  43. Mucientes GR, Queiroz N, Sousa LL, Tarroso P, Sims DW (2009) Sexual segregation of pelagic sharks and the potential threat from fisheries. Biol Lett 5:156–159CrossRefPubMedPubMedCentralGoogle Scholar
  44. Nakano H (1994) Age, reproduction and migration of blue shark in the North Pacific Ocean. Bull Nat Res Inst Far Seas Fish 31:141–256Google Scholar
  45. Nakano H, Nagasawa K (1996) Distribution of pelagic elasmobranchs caught by salmon research gillnets in the north Pacific. Fish Sci 62(6):860–865CrossRefGoogle Scholar
  46. Natanson LJ, Kohler NE, Ardizzone D, Cailliet GM, Wintner SP, Mollet HF (2006) Validated age and growth estimates for the shortfin mako, Isurus oxyrinchus, in the North Atlantic Ocean. Environ Biol Fish 77:367–383CrossRefGoogle Scholar
  47. Naylor GJP, Caira JN, Jensen K, Rosana KAM, White WT, Last PR (2012) A DNA sequence-based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology, Bulletin of the American Museum of Natural History, No. 367. American Museum of Natural History, New YorkGoogle Scholar
  48. Nelson JS (2006) Fishes of the world. Wiley, HobokenGoogle Scholar
  49. Nosal AP, Lewallen EA, Burton RS (2013) Multiple paternity in leopard shark (Triakis semifasciata) litters sampled from a predominantly female aggregation in La Jolla, California, USA. J Exp Mar Biol Ecol 446:110–114CrossRefGoogle Scholar
  50. Okamura H, McAllister MK, Ichinokawa M, Yamanaka L, Holt K (2014) Evaluation of the sensitivity of biological reference points to the spatio-temporal distribution of fishing effort when seasonal migrations are sex-specific. Fish Res 158:116–123CrossRefGoogle Scholar
  51. Pardini AT, Jones CS, Noble LR, Kreiser B, Malcolm H, Bruce BD, Stevens JD, Cliff G, Scholl MC, Francis M, Duffy CAJ, Martin AP (2001) Sex-biased dispersal of great white sharks. Nature 412:139–140CrossRefPubMedGoogle Scholar
  52. Portnoy DS, Piercy AN, Musick JA, Burgess GH, Graves JE (2007) Genetic polyandry and sexual conflict in the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic and Gulf of Mexico. Mol Ecol 16:187–197CrossRefPubMedGoogle Scholar
  53. Pratt HL Jr, Casey JG (1983) Age and growth of the shortfin mako, Isurus oxyrinchus, using four methods. Can J Fish Aquat Sci 40(11):1944–1957CrossRefGoogle Scholar
  54. Ramp C, Bérubé M, Palsbøll P, Hagen W, Sears R (2010) Sex-specific survival in the humpback whale Megaptera novaeangliae in the Gulf of St. Lawrence, Canada. Mar Ecol Prog Ser 400:267–276CrossRefGoogle Scholar
  55. Rice J, Kai M, Harley S (2014) Stock assessment of blue shark in the north Pacific Ocean using stock synthesis. Document presented at second shark working Group in International Scientific Committee for tuna and tuna-like species in the North Pacific Ocean, National Taiwan Ocean University, Taiwan, 3–10 June 2014Google Scholar
  56. Robbins RL (2007) Environmental variables affecting the sexual segregation of great white sharks Carcharodon carcharias at the Neptune Islands South Australia. J Fish Biol 70(5):1350–1364CrossRefGoogle Scholar
  57. Rodríguez-Cabello C, Sánchez F, Olaso I (2007) Distribution patterns and sexual segregation of Scyliorhinus canicula (L.) in the Cantabrian Sea. J Fish Biol 70(5):1568–1586CrossRefGoogle Scholar
  58. Rowe S, Hutchings JA (2003) Mating systems and the conservation of commercially exploited marine fish. Trends Ecol Evol 18(11):567–572CrossRefGoogle Scholar
  59. Sato T (2012) Impacts of large male-selective harvesting on reproduction: illustration with large decapod crustacean resources. Aqua BioSci Monogr 5(3):67–102CrossRefGoogle Scholar
  60. Saville KJ, Lindley AM, Maries EG, Carrier JC, Pratt HL Jr (2002) Multiple paternity in the nurse shark Ginglymostoma cirratum. Environ Biol Fish 63:347–351CrossRefGoogle Scholar
  61. Schmidt JV, Chen CC, Sheikh SI, Meekan MG, Norman BM, Joung SJ (2010) Paternity analysis in a litter of whale shark embryos. Endanger Species Res 12:117–124CrossRefGoogle Scholar
  62. Semba Y (2011) Ecological study on the sex-specific life history of shortfin mako, Isurus oxyrinchus. Dissertation, Tokyo UniversityGoogle Scholar
  63. Semba Y, Nakano H, Aoki I (2009) Age and growth analysis of the shortfin mako, Isurus oxyrinchus, in the western and central North Pacific Ocean. Environ Biol Fish 84:377–391CrossRefGoogle Scholar
  64. Semba Y, Aoki I, Yokawa K (2011) Size at maturity and reproductive traits of shortfin mako, Isurus oxyrinchus, in the western and central North Pacific. Mar Freshw Res 62:20–29CrossRefGoogle Scholar
  65. Sims DW (2005) Differences in habitat selection and reproductive strategies of male and female sharks. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation in vertebrates. Cambridge University Press, Cambridge, pp 127–147Google Scholar
  66. Sims DW, Nash JP, Morritt D (2001) Movements and activity of male and female dogfish in a tidal sea lough: alternative behavioral strategies and apparent sexual segregation. Mar Biol 139(6):1165–1175CrossRefGoogle Scholar
  67. Springer S (1967) Social organization of shark populations. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, skates, and rays. The Johns Hopkins Press, Baltimore, pp 149–174Google Scholar
  68. Stearns SC (1992) The evolution of life histories. Oxford University Press Inc, New YorkGoogle Scholar
  69. Stevens JD (1983) Observations on reproduction in the shortfin mako Isurus oxyrinchus. Copeia 1:126–130CrossRefGoogle Scholar
  70. Strasburg DW (1958) Distribution, abundance, and habits of pelagic sharks in the central Pacific Ocean. Fish Bull 58:335–361Google Scholar
  71. Su N-J, Sun C-L, Punt AE, Yeh S-Z, Dinardo G (2011) Evaluation of a spatially sex-specific assessment method incorporating a habitat preference model for blue marlin (Makaira nigricans) in the Pacific Ocean. Fish Oceanogr 20(5):415–433CrossRefGoogle Scholar
  72. Tsai WP, Liu KM, Punt AE, Sun CL (2014) Assessing the potential biases of ignoring sexual dimorphism and mating mechanism in using a single-sex demographic model: the shortfin mako shark as a case study. ICES J Mar Sci 72(3):793–803CrossRefGoogle Scholar
  73. Veríssimo A, Grubbs D, McDowell J, Musick J, Portnoy D (2011) Frequency of multiple paternity in the spiny dogfish Squalus acanthias in the western north Atlantic. J Hered 102(1):88–93CrossRefPubMedGoogle Scholar
  74. Wearmouth VJ, Sims DW (2008) Sexual segregation in marine fish, reptiles, birds and mammals: behaviour patterns, mechanisms and conservation implications. Adv Mar Biol 54:107–170CrossRefPubMedGoogle Scholar
  75. Wearmouth VJ, Southall EJ, Morritt D, Thompson RC, Cuthill IC, Partridge JC, Sims DW (2012) Year-round sexual harassment as a behavioral mediator of vertebrate population dynamics. Ecol Monogr 82(3):351–366CrossRefGoogle Scholar
  76. Wetherbee BM, Cortés E (2004) Food consumption and feeding habits. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 225–246CrossRefGoogle Scholar
  77. Wilderbuer TK, Turnock BJ (2009) Sex-specific natural mortality of arrowtooth flounder in Alaska: implications of a skewed sex ratio on exploitation and management. North AM J Fish Manag 29(2):306–322CrossRefGoogle Scholar
  78. Wourms JP (1977) Reproduction and development in Chondrichthyan fishes. Am Zool 17(2):379–410CrossRefGoogle Scholar
  79. Wourms JP, Demski LS (1993) The reproduction and development of sharks, skates, rays and ratfishes: introduction, history, overview, and future prospects. Environ Biol Fish 38(1):7–21CrossRefGoogle Scholar

Copyright information

© Springer Japan KK and the Japanese Society of Fisheries Science 2018

Authors and Affiliations

  1. 1.National Research Institute of Far Seas FisheriesJapan Fisheries Research and Education AgencyShizuokaJapan

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