Journal of Ethology

, Volume 37, Issue 1, pp 21–29 | Cite as

A nudibranch removes rival sperm with a disposable spiny penis

  • Ayami SekizawaEmail author
  • Shin G. Goto
  • Yasuhiro Nakashima


Simultaneous hermaphroditism is, at least initially, favoured by selection under low density — and therefore it can be assumed that sperm competition has little importance in this sexual system. However, many simultaneously hermaphroditic nudibranchs have both an allo-sperm storage organ (the seminal receptacle) and an allo-sperm digesting organ (the copulatory bursa), suggesting the possibility of the occurrence of sperm competition. A nudibranch, Chromodoris reticulata, autotomizes its penis after every copulation and replenishes it within about 24 h to perform another copulation. We observed that the surface of the autotomized penis was covered with many backward-pointing spines and that a sperm mass was often entangled on the spines. This suggests that the nudibranch removes sperm that is already stored in a mating partner’s sperm storage organ(s) with its thorny penis. Using six microsatellite markers, we determined that the sperm mass attached to the penis were allo-sperm originating from individual(s) that had participated in prior copulations. We revealed that C. reticulata performed sperm removal using the thorny penis. These results suggest that competition in fertilization is quite intense and mating frequency in the wild is relatively high in this species.


Sexual selection Sperm removal Sperm competition Nudibranch Simultaneous hermaphrodite 



We are grateful to K. Sakai of the Sesoko Station of the University of Ryukyus, for his help during the field survey in Okinawa. We are also thankful to A. Shimizu and M. Okubo of the National Research Institute of Fisheries Science, Fisheries Research; N. Sato of Shimane University; and S. Nanami of Osaka City University, for their help performing DNA analysis. We thank S. Shiga for her help and encouragement. This work was financially supported by a Grant-in-Aid (#22570029) for Scientific Research to Y. N. from the Japanese Ministry of Education, Culture, Sports, Science and Technology.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Informed consent



  1. Angeloni L, Bradbury JW, Burton RS (2003) Multiple mating, paternity, and body size in a simultaneous hermaphrodite, Aplysia californica. Behav Ecol 14(4):554–560CrossRefGoogle Scholar
  2. Baur B (1994) Multiple paternity and individual variation in sperm precedence in the simultaneously hermaphroditic land snail Arianta arbustorum. Behav Ecol Sociobiol 35(6):413–421CrossRefGoogle Scholar
  3. Baur B (1998) Sperm competition in molluscs. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 255–305CrossRefGoogle Scholar
  4. Brandriff B, Beemen RD (1973) Observations on the gametolytic gland in the anaspidean opisthobranchs, Phyllaplysia taylori and Aplysia californica. J Morphol 141:395–409CrossRefGoogle Scholar
  5. Cooper G, Miller P, Holland PWH (1996) Molecular genetic analysis of sperm competition in the damselfly Ischnura elegans (Vader Linden). Proc R Soc Lond B 263:1343–1349CrossRefGoogle Scholar
  6. Cordero A, Miller PL (1992) Sperm transfer, displacement and precedence in Ischnura graellsii (Odonata: Coenagrionidae). Behav Ecol Sociobiol 30:261–267CrossRefGoogle Scholar
  7. Córdoba-Aguilar A, Uhía E, Rivera AC (2003) Sperm competition in Odonata (Insecta): the evolution of female sperm storage and rivals’ sperm displacement. J Zool 261:381–398CrossRefGoogle Scholar
  8. Dillen L, Jordaens K, Backeljau T (2009) Sperm transfer, sperm storage, and sperm digestion in the hermaphroditic land snail Succinea putris (Gastropoda, Pulmonata). Invertebr Biol 128:97–106CrossRefGoogle Scholar
  9. Evanno G, Madec L, Arnaud J (2005) Multiple paternity and postcopulatory sexual selection in a hermaphrodite: what influences sperm precedence in the garden snail Helix aspersa? Mol Ecol 14(3):805–812CrossRefGoogle Scholar
  10. Fischer EA (1980) The relationship between mating system and simultaneous hermaphroditism in the coral reef fish Hypoplectrus nigricans (Serranidae). J Anim Behav 28:620–633CrossRefGoogle Scholar
  11. Fischer EA (1981) Sexual allocation in a simultaneously hermaphroditic coral reef fish. Am Nat 177:64–82CrossRefGoogle Scholar
  12. Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208CrossRefGoogle Scholar
  13. Gosliner TM, Behrens DW, Valdés Á (2008) Indo-Pacific nudibranchs and sea slugs: a field guide to the world’s most diverse fauna. Sea Challengers Natural History Books, Washington, p 426Google Scholar
  14. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefGoogle Scholar
  15. Kamimura Y (2000) Possible removal of rival sperm by the elongated genitalia of the earwig, Euborella plebeja. Zool Sci 17:667–672CrossRefGoogle Scholar
  16. Kamimura Y (2003) Effects of broken male intromittent organ on the sperm storage capacity of female earwig, Euborella plebeja. J Ethol 21:29–35Google Scholar
  17. Kamimura Y (2005) Last-male paternity of Euborella plebeja, an earwig with elongated genitalia and sperm-removal behavior. J Ethol 23:35–41CrossRefGoogle Scholar
  18. Kupfernagel S, Rusterholz H, Baur B (2010) Variation in multiple paternity and sperm utilization patterns in natural populations of a simultaneous hermaphrodite land snail. Biol J Linn Soc 99(2):350–361CrossRefGoogle Scholar
  19. Lange R, Werminghausen J, Anthes N (2013) Does traumatic secretion transfer manipulate mating roles or reproductive output in hermaphroditic sea slug? Behav Ecol Sociobiol 67:1239–1247CrossRefGoogle Scholar
  20. Lange R, Werminghausen J, Anthes N (2014) Cephalo-traumatic secretion transfer in a hermaphrodite sea slug. Proc R Soc B 281: 20132424. CrossRefGoogle Scholar
  21. Leonard J, Westfall J, Pearse J (2007) Phally polymorphism and reproductive biology in Ariolimax (Ariolimax) buttoni (Pilsbry and Vanatta, 1896) (Stylommatophora: Arionidae). Am Malacol Bull 23:121–135CrossRefGoogle Scholar
  22. Lind H (1973) The functional significance of the spermatophore and the fate of spermatozoa in the genital tract of Helix pomatia (Gastropoda: Stylommatophora). J Zool 169:39–64CrossRefGoogle Scholar
  23. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655CrossRefGoogle Scholar
  24. Michiels NK (1998) Mating conflicts and sperm competition in simultaneous hermaphrodites. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 219–254CrossRefGoogle Scholar
  25. Michiels NK, Newman LJ (1998) Sex and violence in hermaphrodites. Nature 391:647CrossRefGoogle Scholar
  26. Miller PL (1987) Sperm competition in Ischnura elegans (Vander Linden) (Zygoptera: Coenagrionidae). Odonatologica 16:201–207Google Scholar
  27. Rudman WB (1984) The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: a review of the genera. Zool J Linn Soc Lond 81:115–273CrossRefGoogle Scholar
  28. Sato N, Sekizawa A, Awata S, Munehara H, Nakashima Y (2011) Isolation and characterization of microsatellite markers in the nudibranch Chromodoris tinctoria. Venus 69:214–217Google Scholar
  29. Sekizawa A, Seki S, Tokuzato M, Shiga S, Nakashima Y (2013) Disposable penis and its replenishment in a simultaneous hermaphrodite. Biol Lett 9:20121150. CrossRefGoogle Scholar
  30. Siva-Jothy MT, Hooper R (1995) The disposition and genetic diversity of stored sperm in the damselfly Calopteryx splendens xanthostoma (Charpentier). Proc R Soc Lond B 259:313–318CrossRefGoogle Scholar
  31. Takami Y (2007) Spermatophore displacement and male fertilization success in the ground beetle Carabus insulicola. Behav Ecol 18(3):628–634CrossRefGoogle Scholar
  32. Thompson TE (1966) Studies on the reproduction of Archidoris pseudoargus (Rapp) (Gastropoda Opisthobranchia). Phil Trans R Soc Lond B 343:343–374Google Scholar
  33. Valdés Á, Gosliner TM, Ghiselin MT (2010) Opisthobranchs. In: Leonard J, Cordoba-aguilar A (eds) The evolution of primary sexual characters in animals. Oxford University, UK, pp 148–172Google Scholar
  34. Waage JK (1979) Dual function of the damselfly penis: sperm removal and transfer. Science 203:916–918CrossRefGoogle Scholar

Copyright information

© Japan Ethological Society and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Ayami Sekizawa
    • 1
    • 2
    Email author
  • Shin G. Goto
    • 1
  • Yasuhiro Nakashima
    • 3
  1. 1.Department of Biology and Geosciences, Graduate School of ScienceOsaka City UniversityOsakaJapan
  2. 2.Graduate School of Agricultural ScienceTohoku UniversitySendaiJapan
  3. 3.Nihon University, College of EconomicsTokyoJapan

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