Female receptivity, mating history, and familiarity influence the mating behavior of cuttlefish


Animals attempt to maximize their reproductive fitness by employing discrimination tactics that increase their fertilization success. Semelparous species are faced with high energy and time constraints. These constraints are predicted to affect the extent of discrimination tactics that may be employed. The semelparous giant Australian cuttlefish, Sepia apama, seek multiple mates during their single breeding season, yet the discrimination tactics used to assess mates remain ambiguous. We combined field observations and laboratory-controlled mating experiments to determine (i) the relationship between the female signal (i.e., white lateral stripe) and mating outcome and (ii) the effects of the white lateral stripe, receptive postures, mating history, and familiarity on mating behavior. Females were less likely to mate when they expressed the white lateral stripe, suggesting that this signal conveys non-receptivity. Female mating history appeared to predict their likelihood of mating because females that had not recently mated were more likely to perform receptive postures and less likely to express the white lateral stripe. Familiarity with the males did not affect female expression of the white lateral stripe nor receptive postures. In males, mating behavior was not affected by the females’ expression of the white lateral stripe nor female receptive postures; however, familiarity with the female did affect male mating behavior. Males exerted a strong preference for unfamiliar females, providing evidence for familiarity discrimination. This research suggests that distinct selection pressures may be driving different discrimination capabilities in the sexes and provides the first empirical evidence of familiarity discrimination in a cephalopod species.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5


  1. Allen GR, Simmons LW (1996) Coercive mating, fluctuating asymmetry and male mating success in a dung fly Sepsis cynipsea. Anim Behav 52:737–741

  2. Andersson M (1994) Sexual selection. Princeton University Press, Princeton

  3. Arnqvist G (1992) Pre-copulatory fighting in a water strider: inter-sexual conflict or mate assessment? Anim Behav 43:559–567

  4. ASAB/ABS (2012) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 83:301–309

  5. Baena ML, Eberhard WG (2007) Appearances deceive: female ‘resistance’ in a sepsid fly is not a test of male ability to hold on. Ethol Ecol Evol 19:27–50

  6. Beach FA, Jordan L (1956) Sexual exhaustion and recovery in the male rat. Q J Exp Psychol 8:121–133

  7. Bisazza A, Vaccari G, Pilastro A (2001) Female mate choice in a mating system dominated by male sexual coercion. Behav Ecol 12:59–64

  8. Blanckenhorn WU, Muhlhauser C, Morf C, Reusch T, Reuter M (2000) Female choice, female reluctance to mate and sexual selection on body size in the dung fly Sepsis cynipsea. Ethology 95:466–482

  9. Blumstein D, Evans CS, Daniel JC (2006) JWatcher 1.0.

  10. Boal JG (1996) Absence of social recognition in laboratory-reared cuttlefish, Sepia officinalis L. (Mollusca: Cephalopoda). Anim Behav 52:529–537

  11. Boal JG (1997) Female choice of males in cuttlefish (Mollusca: Cephalopoda). Behaviour 134:975–988

  12. Boal JG (2006) Social recognition: a top down view of cephalopod behaviour. Vie Milieu 56:69–79

  13. Braithwaite RW, Lee AK (1979) A mammalian example of semelparity. Am Nat 113:151–155

  14. Cameron E, Day T, Rowe L (2003) Sexual conflict and indirect benefits. J Evol Biol 16:1055–1060

  15. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595

  16. Cole LC (1954) The population consequences of life history phenomena. Q Rev Biol 29:103–137

  17. Cordero A, Andrés JA (2002) Male coercion and convenience polyandry in a calopterygid damselfly. J Insect Sci 2:7

  18. Cordero C, Eberhard WG (2003) Female choice of sexually antagonistic male adaptations: a critical review of some current research. J Evol Biol 16:1–6

  19. Dewsbury DA (1981) The Coolidge effect in the northern grasshopper mice (Onychomys leucogaster). Southwest Nat 26:193–197

  20. Dutto MS, Calbacho-Rosa L, Peretti AV (2011) Signalling and sexual conflict: female spiders use stridulations to inform males of sexual receptivity. Ethology 117:1040–1049

  21. Farr JA (1980) Social behavior patterns as determinants of reproductive success in the guppy, Poecilia reticulata Peters (Pisces: Poeciliidae): an experimental study of the effects of intermale competition, female choice and sexual selection. Behaviour 74:38–91

  22. Fincke OM (1997) Conflict resolution in the Odonata: implications for understanding female mating patterns and female choice. Biol J Linn Soc 60:201–220

  23. Fox CW, Hickman DL (1994) Influence of oviposition on female receptivity to multiple mating in Callosobruchus maculatus (Coleoptera: Bruchidae). Ann Entomol Soc Am 87:395–398

  24. Gershman SN, Sakaluk SK (2009) No Coolidge effect in decorated crickets. Ethology 115:774–780

  25. González M, Costa F (2008) Persistence of sexual reluctance in mated females and the importance of regular copulation in a wolf spider. Ethol Ecol Evol 20:11–124

  26. Grant CA, Fowler K, Chapman T (2002) No reduction of female sexual receptivity following mating in a stalk-eye fly, Cyrtodiopsis dalmanni (Diptera: Diopsidae). J Evol Biol 15:210–215

  27. Gross MR (1985) Disruptive selection for alternative life histories in salmon. Nature 313:47–48

  28. Guevara-Fiore P, Stapley J, Watt PJ (2010) Mating effort and female receptivity: how do male guppies decide when to invest in sex? Behav Ecol Sociobiol 64:1665–1672

  29. Hall KC, Hanlon RT (2002) Principal features of the mating system of a large aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Mar Biol 140:533–545

  30. Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, Cambridge

  31. Hanlon RT, Ament SA, Gabr H (1999) Behavioral aspects of sperm competition in cuttlefish, Sepia officinalis (Sepepioidea: Cephalopoda). Mar Biol 134:719–728

  32. Hanlon RT, Naud MJ, Shaw PW, Havenhand JN (2005) Transient sexual mimicry leads to fertilization. Nature 433:212

  33. Harari AR, Landolt PJ, O’Brien CW, Brockmann HJ (2003) Prolonged mate guarding and sperm competition in the weevil Diaprepes abbreviatus (L.). Behav Ecol 14:89–96

  34. Harshman LG, Hoffmann AA, Prout T (1988) Environmental effects on remating in Drosophila melanogaster. Evolution 42:312–321

  35. Hosken DJ, Martin OY, Born J, Huber F (2003) Sexual conflict in Sepsis cynipsea: female reluctance, fertility and mate choice. J Evol Biol 16:485–490

  36. Hughes KA, Du L, Rodd FH, Reznick DN (1999) Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata. Anim Behav 58:907–916

  37. Hughes L, Siew-Woon B, Wagner D, Pierce NE (2000) Effects of mating history on ejaculate size, fecundity, longevity, and copulation duration in the ant-tended lycaenid butterfly, Jalmenus evagoras. Behav Ecol Sociobiol 47:119–128

  38. Ivy TM, Weddle CB, Sakaluk SK (2005) Females use self-referent cues to avoid mating with previous mates. Proc R Soc Lond B 272:2475–2478

  39. Jennions MD, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev Camb Philos Soc 72:283–327

  40. Koderic-Brown A (1993) Female choice of multiple male criteria in guppies: interacting effects of dominance, coloration, and courtship. Behav Ecol Sociobiol 32:415–420

  41. Koderic-Brown A, Nicoletto PF (2001) Female choice in the guppy (Poecilia reticulata): the interaction between male color and display. Behav Ecol Sociobiol 50:346–351

  42. Langmore NE, Davies NB, Hatchwell BJ, Hartley IR (1996) Female song attracts males in the alpine accentor Prunella collaris. Proc R Soc Lond B 263:141–146

  43. Liley NR, Wishlow W (1974) Interactions of endocrine and experiential factors in regulation of sexual behaviour in female guppy Poecilia reticulata. Behaviour 48:185–214

  44. Linley JR, Hinds MJ (1975) Quantity of the male ejaculate influenced by female unreceptivity in the fly, Culicoides melleus. J Insect Physiol 21:281–285

  45. Lisk RD, Baron G (1982) Female regulation of mating location and acceptance of new mating partners following mating to sexual satiety: the Coolidge effect demonstrated in the female golden hamster. Behav Neural Biol 36:416–421

  46. Malin M (1983) The Coolidge effect. Nature 305:570

  47. Martin P, Bateson P (1993) Measuring behaviour: an introductory guide, 2nd edn. Cambridge University Press, Cambridge

  48. McLaughlin ME, Bruce KE (2001) The effect of male familiarity on proximity time in female eastern mosquitofish (Gambusia holbrooks). Psychol Rec 51:237–250

  49. Mossinson S, Yuval B (2003) Regulation of sexual receptivity of female Mediterranean fruit flies: old hypotheses revisited and a new synthesis proposed. J Insect Physiol 49:561–567

  50. Moynihan M, Rodaniche AF (1982) The behavior and natural history of the Caribbean reef squid Sepioteuthis sepioidea. Vergal Paul Parey, Germany

  51. NHMRC (National Health and Medical Research Council) (2004) Australian code of practice for the care and use of animals for scientific purposes. 7th edition.

  52. Naud MJ, Hanlon RT, Hall KC, Shaw PW, Havenhand JN (2004) Behavioural and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. Anim Behav 67:1043–1050

  53. Naud MJ, Shaw PW, Hanlon RT, Havenhand JN (2005) Evidence of biased use of sperm sources in wild female giant cuttlefish. Proc R Soc Lond B 272:1047–1051

  54. Norman MD, Finn J, Tregenza T (1999) Female impersonation as an alternative reproductive strategy in giant cuttlefish. Proc R Soc Lond B 266:1347–1349

  55. Orteiza N, Linder JE, Rice WR (2005) Sexy sons from re-mating do not recoup the direct costs of harmful male interactions in the Drosphila melanogaster laboratory model system. J Evol Biol 18:1315–1323

  56. Ortigosa A, Rowe L (2003) The role of mating history and male size in determining mating behaviours and sexual conflict in a water strider. Anim Behav 65:851–858

  57. Parker GA (1974) Courtship persistence and female-guarding as male time investment strategies. Behaviour 48:157–184

  58. Parker GA, Ball MA, Stockley P, Gage MJG (1997) Sperm competition games: a prospective analysis of risk assessment. Proc R Soc Lond B 264:1793–1802

  59. Payne NL, Semmens JM, Gillanders BM (2010) Examination of giant Australian cuttlefish ′Sepia apama′ breeding behaviour through acoustic telemetry. S Aust Nat 84:38–41

  60. Peretti AV, Cordoba-Aguilar A (2007) Sexual conflict over mating: on the value of fine-scaled behavioral observations for studies on sexual coercion. Ethol Ecol Evol 19:77–86

  61. Peretti AV, Willemart RH (2007) Sexual coercion does not exclude luring behavior in the climbing camel-spider Oltacola chacoensis (Arachnida, Solifugae, Ammotrechidae). J Ethol 25:29–39

  62. Pizzari T (2002) Sperm allocation, the Coolidge effect and female polyandry. Trends Ecol Evol 17:456

  63. Rocha F, Guerra A, Gonzalez AF (2001) A review of reproductive strategies in cephalopods. Rev Biol 76:291–304

  64. Rosenthal GG, Evans CS, Miller WL (1996) Female reference for dynamic traits in the green swordtail, Xiphophorus helleri. Anim Behav 51:811–820

  65. Rowe L (1992) Convenience polyandry in a water strider: foraging conflicts and female control of copulation frequency and guarding duration. Anim Behav 44:189–202

  66. Rudnick D, Veldhuizen T, Tullis R, Culver C, Hieb K, Tskuimura B (2005) A life history model for the San Francisco estuary population of the Chinese mitten crab, Eriocheir sinensis (Decapoda: Grapsoidea). Biol Invasions 7:333–350

  67. Shine R, Olsson MM, Mason RT (2000) Chastity belts in gartersnakes: the functional significance of mating plugs. Biol J Linn Soc 70:377–390

  68. Sievers C, Magurran AE (2011) Context dependent acquisition of familiarity in Trinidadian guppies. Behaviour 148:843–858

  69. Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton

  70. Smith RL (1984) Sperm competition and the evolution of animal mating systems. Academic, London

  71. Smith PH, Gillott C, Barton Browne L, van Gerwen ACM (2008) The mating-induced refractoriness of Lucilia cuprina females: manipulating the male contribution. Physiol Entomol 15:469–481

  72. Sparkes TC, Keogh DP, Haskins KE (2000) Female resistance and male preference in a stream-dwelling isopod: effects of female molt characteristics. Behav Ecol Sociobiol 47:145–155

  73. Steiger S, Franz R, Eggert AK, Müller JK (2008) The Coolidge effect, individual recognition and selection for distinctive cuticular signatures in a burying beetle. Proc R Soc Lond B 275:1831–1838

  74. Stumpf RM, Boesch C (2010) Male aggression and sexual coercion in wild west African chimpanzees, Pan troglodytes verus. Anim Behav 79:333–342

  75. Svard L, Wiklund C (1989) Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 24:395–402

  76. Tan CKW, Løvlie H, Greenway E, Goodwin SF, Pizzari T, Wigby S (2013) Sex-specific responses to sexual familiarity, and the role of olfaction in Drosophila. Proc R Soc Lond B 280:20131691

  77. Thomas ML (2011) Detection of female mating status using chemical signals and cues. Biol Rev 86:1–13

  78. Thornhill R (1980) Rape in Panorpa scorpionflies and a general rape hypothesis. Anim Behav 28:52–59

  79. Tuni C, Berger-Tal R (2012) Male preference and female cues: males assess female sexual maturity and mating status in a web-building spider. Behav Ecol 23:582–587

  80. Wada T, Takegaki T, Mori T, Natsukari Y (2010) Sperm removal, ejaculation and their behavioural interaction in male cuttlefish in response to female mating history. Anim Behav 79:613–619

  81. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320

Download references

Author information

Correspondence to Alexandra K. Schnell.

Additional information

Communicated by T. Breithaupt

Electronic supplementary material

Below is the link to the electronic supplementary material.

(MOV 8946 kb)


(MOV 8946 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schnell, A.K., Smith, C.L., Hanlon, R.T. et al. Female receptivity, mating history, and familiarity influence the mating behavior of cuttlefish. Behav Ecol Sociobiol 69, 283–292 (2015).

Download citation


  • Familiarity discrimination
  • Coolidge effect
  • Mate choice
  • Semelparous
  • Visual signaling
  • Sepia apama