Advertisement

Marine Biology

, Volume 160, Issue 3, pp 553–561 | Cite as

Sperm transfer or spermatangia removal: postcopulatory behaviour of picking up spermatangium by female Japanese pygmy squid

  • Noriyosi SatoEmail author
  • Takashi Kasugai
  • Hiroyuki Munehara
Original Paper

Abstract

In the Japanese pygmy squid Idiosepius paradoxus, females often pick up the spermatangium using their mouth (buccal mass) after copulation. To examine whether the female I. paradoxus directly transfers sperm into the seminal receptacle via this picking behaviour, or removes the spermatangium, we conducted detailed observations of picking behaviour in both virgin and copulated females and compared the sperm storage conditions in the seminal receptacle between females with and without spermatangia picking after copulation in virgin females. In all observations, elongation of the buccal mass occurred within 5 min after copulation. However, sperm volume in the seminal receptacle was not related to spermatangia picking. Observations using slow-motion video revealed that females removed the spermatangia by blowing or eating after picking. These results suggest that picking behaviour is used for sperm removal but not for sperm transfer. Moreover, the frequency of buccal mass elongation was higher in copulated females than in virgin females, consistent with the sequential mate choice theory whereby virgin females secure sperm for fertilisation, while previously copulated females are more selective about their mate. Female I. paradoxus may choose its mate cryptically through postcopulatory picking behaviour.

Keywords

Virgin Female Seminal Receptacle Cryptic Female Choice Buccal Mass Dorsal Mantle Length 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank S. Awata for critical comments on the manuscript. We also thank T. Wada and three anonymous referees for their helpful comments. This study was supported financially by the Mikimoto Fund for Marine Ecology (to NS).

Supplementary material

Picking behaviour of spermatangia by a female. The female elongated its buccal mass (mouth) to the spermatangia. Supplementary material 1 (WMV 6490 kb)

A female picked up some spermatangia using the buccal mass and blew them away by jetting water from the funnel. The latter part of the video shows a slow-motion replay of the blowing behaviour. Supplementary material 2 (WMV 5615 kb)

References

  1. Alexander RD, Otte D (1967) The evolution of genitalia and mating behavior in crickets (Gryllidae) and other orthoptera. Misc Publ Mus Zool Univ Mich 133:1–62Google Scholar
  2. Bakker TCM, Milinski M (1991) Sequential female choice and the previous male effect in sticklebacks. Behav Ecol Sociobiol 29(3):205–210CrossRefGoogle Scholar
  3. Bauer RT (1978) Antifouling adaptations of caridean shrimps—cleaning of antennal flagellum and general body grooming. Mar Biol 49:69–82CrossRefGoogle Scholar
  4. Bauer B (1998) Sperm competition in molluscs. In: Birkhead TR, Moller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 255–305CrossRefGoogle Scholar
  5. Becker K, Wahl M (1996) Behaviour patterns as natural antifouling mechanisms of tropical marine crabs. J Exp Mar Biol Ecol 203(2):245–258. doi: 10.1016/0022-0981(96)02575-0 CrossRefGoogle Scholar
  6. Buresch KC, Maxwell MR, Cox MR, Hanlon RT (2009) Temporal dynamics of mating and paternity in the squid Loligo pealeii. Mar Ecol Prog Ser 387:197–203CrossRefGoogle Scholar
  7. Bussiere LF, Hunt J, Jennions MD, Brooks R (2006) Sexual conflict and cryptic female choice in the black field cricket, Teleogryllus commodus. Evolution 60(4):792–800CrossRefGoogle Scholar
  8. Drew GA (1911) Sexual activities of the squid, Loligo pealii (Les.). 1. Copulation, egg laying and fertilization. J Morphol 22:327–359CrossRefGoogle Scholar
  9. Drew GA (1919) Sexual activities of the squid, Loligo pealii (Les.) 2. The spermatophore; its structure, ejaculation and formation. J Morphol 32:379–436CrossRefGoogle Scholar
  10. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, PrincetonGoogle Scholar
  11. Fedina TY, Lewis SM (2007) Female mate choice across mating stages and between sequential mates in flour beetles. J Evol Biol 20(6):2138–2143. doi: 10.1111/j.1420-9101.2007.01432.x CrossRefGoogle Scholar
  12. Fleischer J, Grell M, Hoeg JT, Olesen J (1992) Morphology of grooming limbs in species of Petrolisthes and Pachycheles (Crustacea, Decapoda, Anomura, Porcellanidae)—a scanning electron-microscopy study. Mar Biol 113(3):425–435. doi: 10.1007/bf00349168 CrossRefGoogle Scholar
  13. Gabor CR, Halliday TR (1997) Sequential mate choice by multiply mating smooth newts: females become more choosy. Behav Ecol 8(2):162–166CrossRefGoogle Scholar
  14. Halliday TR (1983) The study of mate choice. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 3–32Google Scholar
  15. Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, CambridgeGoogle Scholar
  16. Hanlon RT, Ament SA, Gabr H (1999) Behavioral aspects of sperm competition in cuttlefish, Sepia officinalis (Sepioidea: Cephalopoda). Mar Biol 134(4):719–728CrossRefGoogle Scholar
  17. Hanlon RT, Smale MJ, Sauer WHH (2002) The mating system of the squid Loligo vulgaris reynaudii (Cephalopoda, Mollusca) off South Africa: fighting, guarding, sneaking, mating and egg laying behavior. Bull Mar Sci 71(1):331–345Google Scholar
  18. Ikeda Y, Sakurai Y, Shimazaki K (1993) Fertilizing capacity of squid (Todarodes pacificus) spermatozoa collected from various sperm storage sites, with special reference to the role of gelatinous substance from oviducal gland in fertilization and embryonic development. Invertebr Reprod Dev 23:39–44CrossRefGoogle Scholar
  19. Iwata Y, Sakurai Y (2007) Threshold dimorphism in ejaculate characteristics in the squid Loligo bleekeri. Mar Ecol Prog Ser 345:141–146CrossRefGoogle Scholar
  20. Iwata Y, Munehara H, Sakurai Y (2005) Dependence of paternity rates on alternative reproductive behaviors in the squid Loligo bleekeri. Mar Ecol Prog Ser 298:219–228CrossRefGoogle Scholar
  21. Iwata Y, Shaw P, Fujiwara E, Shiba K, Kakiuchi Y, Hirohashi N (2011) Why small males have big sperm: dimorphic squid sperm linked to alternative mating behaviours. BMC Evol Biol 11:9. doi: 10.1186/1471-2148-11-236 CrossRefGoogle Scholar
  22. Izzo AS, Gray DA (2011) Heterospecific courtship and sequential mate choice in sister species of field crickets. Anim Behav 81(1):259–264. doi: 10.1016/j.anbehav.2010.10.015 CrossRefGoogle Scholar
  23. Kasugai T (2000) Reproductive behavior of the pygmy cuttlefish Idiosepius paradoxus in an aquarium. Venus 59(1):37–44Google Scholar
  24. Kasugai T (2001) Feeding behaviour of the Japanese pygmy cuttlefish Idiosepius paradoxus (Cephalopoda: Idiosepiidae) in captivity: evidence for external digestion? J Mar Biol Assoc UK 81:979–981Google Scholar
  25. Kasugai T, Segawa S (2005) Life cycle of the Japanese pygmy squid Idiosepius pardoxus (Cephalopoda: Idiosepiidae) in the zostera beds of the temperate coast of central honshu, Japan. Phuket Mar Biol Cent Res Bull 66:249–258Google Scholar
  26. Lu CC, Dunning MC (1998) Subclass Coleoidea. In: Beesley PL, Ross GJB, Wells A (eds) Fauna of Australia, vol 5. CSIRO, Melbourne, pp 499–563Google Scholar
  27. Lumkong A (1992) A histological study of the accessory reproductive-organs of female Loligo Forbesi (Cephalopoda, Loliginidae). J Zool 226:469–490CrossRefGoogle Scholar
  28. Marian JEAR (2012) Spermatophoric reaction reappraised: novel insights into the functioning of the loliginid spermatophore based on Doryteuthis plei (Mollusca: Cephalopoda). J Morphol 273(3):248–278CrossRefGoogle Scholar
  29. Moynihan M (1983) Notes on the behavior of Idiosepius Pygmaeus (Cephalopoda, Idiosepiidae). Behaviour 85:42–57CrossRefGoogle Scholar
  30. Moynihan M, Arcadio FR (1982) The behavior and natural history of the Caribbean reef squid, sepioteuthis sepioidea, vol 25. Advances in ethology. Verlag Paul Parey, Berlin, HamburgGoogle Scholar
  31. Nabhitabhata J (1998) Distinctive behaviour of thai pygmy squid, Idiosepius thailandicus Chotiyaputta, Okutani & Chaitiamvong, 1991. Phuket Mar Biol Cent Special Publ 18(1):25–40Google Scholar
  32. Nabhitabhata J, Suwanamala J (2008) Reproductive behaviour and cross-mating of two closely related pygmy squids Idiosepius biserialis and Idiosepius thailandicus (Cephalopoda: Idiosepiidae). J Mar Biol Assoc UK 88(5):987–993CrossRefGoogle Scholar
  33. Natsukari Y (1970) Egg-laying behavior, embryonic development and hatched larva of the pygmy cuttlefish, Idiosepius pygmaeus paradoxus Ortmann. Contrib Fish Exp Stn Nagasaki Univ 30:15–29Google Scholar
  34. 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 67:1043–1050CrossRefGoogle Scholar
  35. Naud MJ, Shaw PW, Hanlon RT, Havenhand JN (2005) Evidence for biased use of sperm sources in wild female giant cuttlefish (Sepia apama). Proc R Soc Lond B 272(1567):1047–1051CrossRefGoogle Scholar
  36. Nesis KN, Katugin ON, Ratnikov AV (2002) Pygmy cuttlefish Idiosepius paradoxus (Ortmann, 1888) (Cephalopoda)—first record of Idiosepiidae in Russian seas. Ruthenica 12(1):81–84Google Scholar
  37. Nigmatullin CM, Laptikhovsky VV, Moustahfid H (2002) Brief review on the ecology in the North African population of arrow squid Todarodes sagittatus (Cephalopoda: Ommastrephidae). Bull Mar Sci 71(2):581–590Google Scholar
  38. Pitcher TE, Neff BD, Rodd FH, Rowe L (2003) Multiple mating and sequential mate choice in guppies: females trade up. Proc R Soc Lond B 270(1524):1623–1629CrossRefGoogle Scholar
  39. Sakaluk SK (1984) Male crickets feed females to ensure complete sperm transfer. Science 223(4636):609–610CrossRefGoogle Scholar
  40. Sakaluk SK, Eggert AK (1996) Female control of sperm transfer and intraspecific variation in sperm precedence: antecedents to the evolution of a courtship food gift. Evolution 50(2):694–703CrossRefGoogle Scholar
  41. Sasaki M (1923) On an adhering habit of a pygmy cuttlefish, Idiosepius pygmaeus steenstrup. Annot Zool Jpn 10(21):209–213Google Scholar
  42. Sato N, Kasugai T, Munehara H (2008) Estimated life span of the Japanese pygmy squid, Idiosepius paradoxus from statolith growth increments. J Mar Biol Assoc UK 88(2):391–394CrossRefGoogle Scholar
  43. Sato N, Kasugai T, Ikeda Y, Munehara H (2010) Structure of the seminal receptacle and sperm storage in the Japanese pygmy squid. J Zool 282(3):151–156. doi: 10.1111/j.1469-7998.2010.00733.x CrossRefGoogle Scholar
  44. Takahama H, Kinoshita T, Sato M, Sasaki F (1991) Fine-structure of the spermatophores and their ejaculated forms, sperm reservoirs, of the Japanese common squid, Todarodes Pacificus. J Morphol 207(3):241–251CrossRefGoogle Scholar
  45. Thornhill R (1983) Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am Nat 122(6):765–788CrossRefGoogle Scholar
  46. van Oordt GJ (1938) The spermatheca of Loligo vulgaris. 1 T. Structure of the spermatheca and function of its unicellular glands. Q J Microsc Sci 80:593–600Google Scholar
  47. Wada T, Takegaki T, Mori T, Natsukari Y (2005) Sperm displacement behavior of the cuttlefish Sepia esculenta (Cephalopoda: Sepiidae). J Ethol 23(2):85–92. doi: 10.1007/s10164-005-0146-6 CrossRefGoogle Scholar
  48. Wada T, Takegaki T, Mori T, Natsukari Y (2006) Reproductive behavior of the Japanese spineless cuttlefish Sepiella japonica. Venus 65(3):221–228Google Scholar
  49. 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(3):613–619. doi: 10.1016/j.anbehav.2009.12.004 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Noriyosi Sato
    • 1
    • 4
    Email author
  • Takashi Kasugai
    • 2
  • Hiroyuki Munehara
    • 3
  1. 1.Division of Biosphere Science, Graduate School of Environmental ScienceHokkaido Universitykita-ku, SapporoJapan
  2. 2.Port of Nagoya Public AquariumMinato-ku, NagoyaJapan
  3. 3.Usujiri Fisheries Station, Field Science Centre for Northern BiosphereHokkaido UniversityHakodateJapan
  4. 4.Graduate School of Fisheries Science and Environmental StudiesNagasaki UniversityNagasakiJapan

Personalised recommendations