Identification of Crustacean Sex Pheromones

  • Joerg D. Hardege
  • John A. Terschak


Odor and fragrances can carry information about an organism and have long been suggested as vital mechanisms that affect or control animal behavior. The use of such chemical signals is widespread in the aquatic environment, and crustaceans such as lobsters, shrimps, crabs, barnacles, and crayfish are known to utilize odor for predator–prey interactions, mating, establishing of dominance or social hierarchies as well as hatching of young and settlement of larvae. Nevertheless, the chemical identity of these behavior-modifying odors remains largely unknown. Here, we briefly review the literature on crustacean chemical signals and describe our approach to identify these using the example of the shore crab (Carcinus maenas) sex pheromones. We describe the principles of a bioassay-driven purification that is combined with a metabolomic approach where differences in the odor profiles of sexually active and inactive crabs are examined. Using such an integrated approach, we identified the female produced signal to be a nucleotide with its production being linked with the female molt (ecdysis). The pheromone enables males to detect the optimal time to mate just after the female molt with the timing of the reproductive event enabling crabs to use a simple, not species-specific, chemical as a sex pheromone. Based on our recent findings, we discuss the implications for future studies on crustacean chemical signaling.


High Performance Liquid Chromatography Mate Choice Shore Crab Molt Stage Conditioned Water 
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.


  1. Asai N, Fusetani N, Matsunaga S, Sasaki J (2000) Sex pheromones of the hair crab Erimacrus isenbeckii. Part 1: isolation and structures of novel ceramides. Tetrahedron 56:9895–9899CrossRefGoogle Scholar
  2. Bamber SD, Naylor E (1996) Chemical communication and behavioral interaction between sexually mature male and female shore crabs (Carcinus maenas). J Mar Biol Assoc UK 76:691–699CrossRefGoogle Scholar
  3. Beckmann M, Hardege JD, Zeeck E (1995) Effects of the volatile fraction of crude oil on the reproductive behaviour of nereids (Annelida, Polychaeta). Mar Environ Res 40:267–276CrossRefGoogle Scholar
  4. Beltz BS (1999) The distribution and functional anatomy of amine containing neurons in decapod crustaceans. Microsc Res Tech 44:105–120CrossRefPubMedGoogle Scholar
  5. Bublitz R, Sainte-Marie B, Newcomb-Hodgetts C, Fletcher N, Smith M, Hardege JD (2008) Interspecific activity of sex pheromone of the European shore crab (Carcinus maenas). Behaviour 145:1465–1478CrossRefGoogle Scholar
  6. Butenandt A, Beckmann R, Stamm D, Hecker E (1959) Über den Sexuallockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z Naturforsch 14:283–284Google Scholar
  7. Caskey JD, Hasenstein KH, Bauer RT (2009) Studies on contact sex pheromones of the caridean shrimp Palaemonetes pugio: I. Cuticular hydrocarbons associated with mate recognition. Inv Reprod Dev 53:93–103Google Scholar
  8. Caspers H (1984) Spawning periodicity and habitat of the Palolo worm Eunice viridis (Polychaeta: Eunicidae) in the Samoan Islands. Mar Biol 79:229–236CrossRefGoogle Scholar
  9. Clare AS, Matsumura K (2000) Nature and perception of barnacle settlement pheromones. Biofouling 15:57–71CrossRefGoogle Scholar
  10. Darwin C (1871) The descent of man, and sexual selection in relation to sex. John Murray, LondonGoogle Scholar
  11. Derby CD (2000) Learning from spiny lobsters about chemosensory coding of mixtures. Physiol Behav 69:203–209CrossRefPubMedGoogle Scholar
  12. Dunham PJ (1978) Sex pheromones in Crustacea. Biol Rev 53:555–583CrossRefGoogle Scholar
  13. Dunham PJ (1988) Pheromones and behaviour in Crustacea. In: Laufer H, Downer R (eds) Endocrinology of selected invertebrate types. Alan R. Liss, New York, pp 375–392Google Scholar
  14. Eales AJ (1974) Sex pheromone in the shore crab Carcinus maenas, and the site of its release from females. Mar Behav Physiol 2:345–355CrossRefGoogle Scholar
  15. Ekerholm M, Hallberg E (2005) Primer and short-range releaser pheromone properties of premolt female urine from the shore crab Carcinus maenas. J Chem Ecol 31:1845–1864CrossRefPubMedGoogle Scholar
  16. Fletcher N, Hardege JD (2009) The cost of conflict: agonistic encounters influence responses to chemical signals in the shore crab, Carcinus maenas. Anim Behav 77:357–361CrossRefGoogle Scholar
  17. Forward RB Jr, Ritttschof D, De Vries MC (1987) Peptide pheromones synchronize crustacean egg hatching and larval release. Chem Senses 12:491–498CrossRefGoogle Scholar
  18. Gleeson RA, Adams MA, Smith AB (1984) Characterisation of a sex pheromone in the blue crab Callinectes sapidus. J Chem Ecol 10:913–921CrossRefGoogle Scholar
  19. Grosholz ED, Ruiz GM (1995) Spread and potential impact of the recently introduced European green crab, Carcinus maenas, in central California. Mar Biol 122:239–247Google Scholar
  20. Hardege JD (1999) Nereid polychaetes as model organism for marine chemical ecology: a review. Hydrobiologia 402:145–161CrossRefGoogle Scholar
  21. Hardege JD, Bartels-Hardege HD, Zeeck E, Grimm FT (1990) Induction of swarming in Nereis succinea. Mar Biol 104:291–295CrossRefGoogle Scholar
  22. Hardege JD, Mueller CT, Beckmann M, Bartels-Hardege HD, Bentley MG (1998) Timing of reproduction in marine polychaetes: the role of sex pheromones. Ecoscience 5:395–404Google Scholar
  23. Hardege JD, Jennings A, Hayden D, Müller CT, Pascoe D, Bentley MG, Clare AS (2002) Novel behavioural assay and partial purification of a female-derived sex pheromone in Carcinus maenas. Mar Ecol Prog Ser 244:179–189CrossRefGoogle Scholar
  24. Hartnoll RG (1969) Mating in the Brachyura. Crustaceana 16:161–181CrossRefGoogle Scholar
  25. Hay ME (2009) Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Annu Rev Mar Sci 1:193–212CrossRefGoogle Scholar
  26. Hayden D, Jennings A, Mueller C, Pascoe D, Bublitz R, Webb H, Breithaupt T, Watkins L, Hardege JD (2007) Sex specific mediation of foraging in the shore crab, Carcinus maenas. Horm Behav 52:162–168CrossRefPubMedGoogle Scholar
  27. Hazlett BA (1999) Responses to multiple chemical cues by the crayfish Orconectes virilis. Behaviour 136:161–177Google Scholar
  28. Huber R, Smith K, Delago A, Isaksson K, Kravitz EA (1997) Serotonin and aggressive motivation in crustaceans: altering the decision to retreat. Proc Natl Acad Sci U S A 94:5939–5942CrossRefPubMedGoogle Scholar
  29. Huntingford FA, Taylor AC, Smith IP, Thorpe KE (1995) Behavioural and physiological studies of aggression in swimming crabs. J Exp Mar Biol Ecol 193:21–39CrossRefGoogle Scholar
  30. Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289CrossRefPubMedGoogle Scholar
  31. Kittredge JS, Terry M, Takahashi FT (1971) Sex pheromone activity of the moulting hormone crustecdysone on male crabs (Pachygrapsus crassipes, Cancer antennarius and Cancer anthonyi). Fish Bull 69:337–343Google Scholar
  32. Koehl MAR (2006) The fluid mechanics of arthropod sniffing in turbulent odor plumes. Chem Senses 31:93–105CrossRefPubMedGoogle Scholar
  33. Li W, Scott AP, Siefkes MJ, Yan H, Liu Q, Yun SS, Gage DA (2002) Bile acid secreted by male sea lamprey that acts as a sex pheromone. Science 296:138–141CrossRefPubMedGoogle Scholar
  34. Macías-Garcia C, Ramirez E (2005) Evidence that sensory traps can evolve into honest signals. Nature 434:501–505CrossRefGoogle Scholar
  35. Mansecal R (1999) Chitin. In: Polymer data handbook. Mark JE (ed) Oxford University Press, New York, pp 67–69Google Scholar
  36. Painter S, Clough B, Garden RW, Sweedler JV, Nagle GT (1998) Characterization of Aplysia attraction, the first water-borne peptide pheromone in invertebrates. Biol Bull 194:120–131CrossRefPubMedGoogle Scholar
  37. Pettis RJ, Erickson BW, Forward RB, Rittschof D (1993) Superpotent synthetic tripeptide mimics of the mud-crab pumping pheromone. Int J Pept Protein Res 42:312–319CrossRefPubMedGoogle Scholar
  38. Pickett JA, Griffiths DC (1980) Composition of aphid alarm pheromones. J Chem Ecol 6:349–360CrossRefGoogle Scholar
  39. Ram JL, Mueller CT, Beckmann M, Hardege JD (1999) The spawning pheromone cysteine-glutathione disulfide (“Nereithione”) arouses a multicomponent nuptial behaviour and electrophysiological activity in Nereis succinea males. FASEB J 13:945–952PubMedGoogle Scholar
  40. Ram JL, Fei X, Danaher SM, Lu S, Breithaupt T, Hardege JD (2008) Finding females: pheromone-guided reproductive tracking behavior by male Nereis succinea in the marine environment. J Exp Biol 211:757–765CrossRefPubMedGoogle Scholar
  41. Ratchford SG, Eggleston DB (1998) Size- and scale-dependent chemical attraction contribute to an ontogenetic shift in sociality. Anim Behav 56:1027–1034CrossRefPubMedGoogle Scholar
  42. Rodríguez EM, Medesani DA, Fingerman M (2007) Endocrine disruption in crustaceans due to pollutants: a review. Comp Biochem Physiol A 146:661–671CrossRefGoogle Scholar
  43. Röhl I, Schneider B, Schmidt B, Zeeck E (1999) L-Ovothiol A: the egg release pheromone of the marine polychaete Platynereis dumerilii: Annelida: Polychaeta. Z Naturforsch 54:1145–1147Google Scholar
  44. Ryan EP (1966) Pheromone: evidence in decapod Crustacea. Science 151:340–341CrossRefPubMedGoogle Scholar
  45. Seifert P (1982) Studies on the sex pheromone of the shore crab, Carcinus maenas, with special regard to ecdysone excretion. Ophelia 21:147–158Google Scholar
  46. Smallegange IM, Van der Meer J (2007) Interference from a game theoretical perspective: shore crabs suffer most from equal competitors. Behav Ecol 18:215–221CrossRefGoogle Scholar
  47. Sneddon LU, Huntingford FA, Taylor AC (1997) Weapon size versus body size as a predictor of winning in fight between shore crabs, Carcinus maenas. Behav Ecol Sociobiol 41:237–242CrossRefGoogle Scholar
  48. Sneddon LU, Huntingford FA, Taylor AC, Clare AS (2003) Female sex pheromone-mediated effects on behaviour and consequences of male competition in the shore crab (Carcinus maenas). J Chem Ecol 29:55–70CrossRefPubMedGoogle Scholar
  49. Sorensen PW, Stacey NE (1999) Evolution and specialization in fish hormonal pheromones. In: Johnston RE, Müller-Schwarze D, Sorensen PW (eds) Advances in chemical signals in vertebrates. Kluwer Publishers, Amsterdam, pp 15–47Google Scholar
  50. Stacey N, Sorensen P (2002) Hormonal pheromones in fish. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Non-mammalian hormone-behavior system. Harcourt Publishers, London, pp 375–434Google Scholar
  51. Stacey NE, Sorensen P (2006) Reproductive pheromones. In: Sloman KA, Balshine S, Wilson RI (eds) Behaviour and physiology of fish. Elsevier, Amsterdam, pp 359–412Google Scholar
  52. Tierney AJ, Atema J (1988) Amino-acid chemoreception – effects of pH on receptors and stimuli. J Chem Ecol 14:135–141CrossRefGoogle Scholar
  53. Tomaschko KH (1994) Ecdysteroids from Pycnogonum litorale (Arthropoda, Pantopoda) act as a chemical defense against Carcinus maenas (Crustacea, Decapoda). J Chem Ecol 20:1445–1455CrossRefGoogle Scholar
  54. Van der Meeren GI (1994) Sex- and size-dependent mating tactics in a natural population of shore crabs Carcinus maenas. J Anim Ecol 63:307–314CrossRefGoogle Scholar
  55. Wagner CM, Jones ML, Twohey MB, Sorensen PW (2006) A field test verifies that pheromones can be useful for sea lamprey (Petromyzon marinus) control in the Great Lakes. Can J Fish Aquat Sci 63:475–479CrossRefGoogle Scholar
  56. Willig A (1974) Die Rolle der Ecdyosne im Häutungszyklus der Crustaceen. Fortschr Zool 22:55–74PubMedGoogle Scholar
  57. Wood DE, Derby CD (1996) Distribution of dopamine-like immunoreactivity suggests a role for dopamine in the courtship display behavior of the blue crab, Callinectes sapidus. Cell Tissue Res 285:321–330CrossRefPubMedGoogle Scholar
  58. Wyatt TD (2003) Pheromones and animal behavior. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  59. Wyatt TD (2009) Fifty years of pheromones. Nature 457:262–263CrossRefPubMedGoogle Scholar
  60. Zahavi A, Zahavi A (1997) The handicap principle: a missing piece in Darwin’s puzzle. Oxford University Press, OxfordGoogle Scholar
  61. Zeeck E, Hardege JD, Bartels-Hardege HD, Wesselmann G (1988) Sex pheromone in a marine polychaete: determination of the chemical structure. J Exp Zool 246:285–292CrossRefGoogle Scholar
  62. Zhang D, Lin J (2006) Mate recognition in a simultaneous hermaphroditic shrimp, Lysmata wurdemanni (Caridea: Hippolytidae). Anim Behav 71:1191–1196CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of HullHullUK

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