Marine Biology

, Volume 162, Issue 4, pp 881–888 | Cite as

Novel mating modes on wave-swept shores: aerial copulation and sperm release in an intertidal stalked barnacle

  • Marjan BarazandehEmail author
  • A. Richard Palmer
Original Paper


Mating behavior of the intertidal stalked barnacle, Pollicipes polymerus, is unusual. Spermcast mating is unexpectedly common, but its prevalence and mechanisms of sperm release and capture are unknown. Moreover, copulation has never been observed in P. polymerus, despite possessing a well-developed penis and despite numerous attempts to observe it. This raises questions about whether spermcasting is a primary or secondary mode of mating in P. polymerus. Through field observations at sites in Barkley Sound, British Columbia (48°N, 125°W) in the northern hemisphere summers of 2012–2014, (a) the incidence of sperm leakage at low tide and (b) the type and prevalence of copulatory behaviors were quantified. Sperm leakage was an infrequent event: ~0.1 % of P. polymerus released a milky, viscous liquid between their opercular plates at low tide. Microscopic examination confirmed that this liquid contained abundant sperm, although sperm viability could not be verified. Some leaker individuals (31 % of 13 examined) contained newly released egg sacks, so sperm leakage in these may have been a post-mating response. However, the remaining leakers contained either fully mature egg masses (egg lamellae), or no eggs or sperm at all, suggesting that sperm leakage was an active process. Transects of P. polymerus beds revealed that sperm leakage at low tide was independent of most weather and tidal conditions. However, sperm leakage was more common lower in the intertidal at more wave-exposed sites. Rates of copulation in the field were about four times those of sperm leakage, suggesting that leakage may be a secondary mode of fertilization. Unique among barnacles, copulation occurred mostly when barnacles were partially emersed, shortly after contact with breaking waves on an incoming tide. Aerial copulation may allow P. polymerus to mate more reliably on shores with high wave exposure. Also unlike other barnacles, reciprocal copulation was occasionally observed in P. polymerus.


Breaking Wave Mantle Cavity Sperm Release Incoming Tide High Shore 
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.



This work was supported by NSERC Discovery Grants to A.R.P. (A7245). We thank J. Sykes, C. Keates, N. Webster, and S. Anthony for field assistance, the director and staff of the Bamfield Marine Sciences Centre for logistical support, and C. Cameron, J. Healy, S. Leys, E. Lovas and A. Oatway for advice regarding sperm imaging.

Supplementary material

227_2015_2631_MOESM1_ESM.ppt (27.5 mb)
Supplementary material 1 (PPT 28186 kb)

Supplementary material 2 (MPG 62736 kb)


  1. Addison JA, Hart MW (2005) Spawning, copulation and inbreeding coefficients in marine invertebrates. Biol Lett 1:450–453CrossRefGoogle Scholar
  2. Anderson DT (1994) Barnacles: structure, function, development and evolution. Chapman and Hall, LondonGoogle Scholar
  3. Barazandeh M, Davis CS, Neufeld CJ, Coltman DW, Palmer AR (2013) Something Darwin didn’t know about barnacles: spermcast mating in a common stalked species. Proc R Soc B Biol Sci 280:20122919CrossRefGoogle Scholar
  4. Barazandeh M, Davis CS, Palmer AR (2014) Where even a long penis can’t help: evidence of long-distance spermcast mating in two acorn barnacles. J Exp Mar Biol Ecol 454:49–54CrossRefGoogle Scholar
  5. Barnes M (1992) The reproductive periods and condition of the penis in several species of common cirripedes. Oceanogr Mar Biol 30:483–525Google Scholar
  6. Barnes M (1996) Pedunculate cirripedes of the genus Pollicipes. Oceanogr Mar Biol 34:303–394Google Scholar
  7. Barnes H, Barnes M (1958) Further observations on self-fertilization in Chthamalus sp. Ecology 39:550CrossRefGoogle Scholar
  8. Barnes H, Crisp DJ (1956) Evidence of self-fertilization in certain species of barnacles. J Mar Biol Assoc UK 35:631–639CrossRefGoogle Scholar
  9. Barnes H, Barnes M, Klepal W (1977) Studies on the reproduction of cirripedes. I. Introduction: copulation, release of oocytes, and formation of the egg lamellae. J Exp Mar Biol Ecol 27:195–218CrossRefGoogle Scholar
  10. Bishop JDD (1998) Fertilization in the sea: are the hazards of broadcast spawning avoided when free-spawned sperm fertilize retained eggs? Proc R Soc B Biol Sci 265:725–731CrossRefGoogle Scholar
  11. Bishop JDD, Pemberton AJ (2006) The third way: spermcast mating in sessile marine invertebrates. Integr Comp Biol 46:398–406CrossRefGoogle Scholar
  12. Charnov EL (1982) The theory of sex allocation. Princeton University Press, PrincetonGoogle Scholar
  13. Charnov EL (1987) Sexuality and hermaphroditism in barnacles: a natural selection approach. In: Southward AJ (ed) Crustacean issues 5: barnacle biology. A. A. Balkema, Rotterdam, pp 89–103Google Scholar
  14. Darwin C (1851) A monograph of the sub-class Cirripedia. I. The Lepadidae. The Ray Society, LondonGoogle Scholar
  15. Darwin C (1854) A monograph of the sub-class Cirripedia. II. The Balanidae (or sessile cirripedes); the Verrucidae, etc. The Ray Society, LondonGoogle Scholar
  16. Denny MW (1987) Life in the maelstrom: the biomechanics of wave-swept rocky shores. Trends Ecol Evol 2:61–66CrossRefGoogle Scholar
  17. Furman ER, Yule AB (1990) Self-fertilization in Balanus improvisus Darwin. J Exp Mar Biol Ecol 144:235–239CrossRefGoogle Scholar
  18. Healy JM, Anderson DT (1990) Sperm ultrastructure in the Cirripedia and its phylogenetic significance. Rec Aust Mus 42:1–26CrossRefGoogle Scholar
  19. Helmuth B, Denny MW (2003) Predicting wave exposure in the rocky intertidal zone: do bigger waves always lead to larger forces? Limnol Oceanogr 48:1338–1345CrossRefGoogle Scholar
  20. Hilgard GH (1960) A study of reproduction in the intertidal barnacle, Mitella polymerus, in Monterey Bay, California. Biol Bull 119:169–188CrossRefGoogle Scholar
  21. Hoch JM (2009) Adaptive plasticity of the penis in a simultaneous hermaphrodite. Evolution 63:1946–1953CrossRefGoogle Scholar
  22. Hoffman DL (1989) Settlement and recruitment patterns of a pedunculate barnacle, Pollicipes polymerus Sowerby, off La Jolla, California. J Exp Mar Biol Ecol 125:83–98CrossRefGoogle Scholar
  23. Johnson SL, Yund PO (2004) Remarkable longevity of dilute sperm in a free-spawning colonial ascidian. Biol Bull 206:144–151CrossRefGoogle Scholar
  24. Neufeld CJ, Palmer AR (2008) Precisely proportioned: intertidal barnacles alter penis form to suit coastal wave action. Proc R Soc B Biol Sci 275:1081–1087CrossRefGoogle Scholar
  25. Newman WA, Abbott DP (1980) Cirripedia: the barnacles. In: Morris RH, Abbott DP, Haderlie EC (eds) Intertidal invertebrates of California. Stanford University Press, Stanford, pp 504–535Google Scholar
  26. Plough LV, Moran A, Marko P (2014) Density drives polyandry and relatedness influences paternal success in the Pacific gooseneck barnacle Pollicipes elegans. BMC Evol Biol 14:81CrossRefGoogle Scholar
  27. Raimondi PT, Martin JE (1991) Evidence that mating group size affects allocation of reproductive resources in a simultaneous hermaphrodite. Am Nat 138:1206–1217CrossRefGoogle Scholar
  28. Watson LP, McKee AE, Merrell BR (1980) Preparation of microbiological specimens for scanning electron microscopy. Scan Electron Microsc II:45–56Google Scholar
  29. Yamaguchi S, Ozaki Y, Yusa Y, Takahashi S (2007) Do tiny males grow up? Sperm competition and optimal resource allocation schedule of dwarf males of barnacle. J Theor Biol 245:319–328CrossRefGoogle Scholar
  30. Yamaguchi S, Yusa Y, Yamato S, Urano S, Takahashi S (2008) Mating group size and evolutionarily stable pattern of sexuality in barnacles. J Theor Biol 253:61–73CrossRefGoogle Scholar
  31. Yusa Y, Yoshikawa M, Kitaura J, Kawane M, Ozaki Y, Shigeyuki Y, Høeg JT (2012) Adaptive evolution of sexual systems in pedunculate barnacles. Proc R Soc B Biol Sci 279:959–966CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  2. 2.Bamfield Marine Sciences CentreBamfieldCanada

Personalised recommendations