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Chemical Communication in Crustaceans: Research Challenges for the Twenty-First Century

  • Martin Thiel
  • Thomas Breithaupt
Chapter

Abstract

Chemical signals play an important role during various life stages of crustaceans. Settling of larvae, parent–offspring communication, mate finding, mate choice, aggressive contests, and dominance hierarchies are all mediated by chemical signals. Enormous advances have been made on understanding the function of chemical signals in crustaceans and we are on the doorstep of major advances in chemical characterization of pheromones. In many species urine is the carrier of chemical signals. Crustaceans control release and transfer direction of urine, but it is unknown whether crustacean senders can manipulate the composition of urineborne pheromones. Chemicals contained in the urine effectively convey information about conspecific properties such as sex, sexual receptivity, species identity, health status, motivation to fight, dominance, individual identity, and molt stage. In larger species (shrimp, crabs, lobsters, crayfish) signal delivery is often aided by self-generated fanning currents that flush chemicals towards receivers, which themselves might actively pull water towards their sensory structures. Antennal flicking also supports molecule exchange at the receptor level. Contact pheromones play a role in sex recognition in several crustacean taxa and in settlement of barnacles. Large crustacean species show little or no sexual dimorphism in receptor structures, but in smaller taxa, e.g. peracarids and copepods, males often have larger antennae than females. Whether differences in sexual roles have also resulted in sex-specific brain centers is not known at present. While pheromones play an important role in mate finding and species recognition, there are numerous examples from peracarids and copepods where males pursue or even form precopulatory pairs with females of closely related congeners. Differentiation of chemicals often appears to be insufficient to guarantee reproductive isolation. In many freshwater and coastal habitats, pollutants may also disrupt chemical communication in crustaceans, but the specific mechanisms of interference are not well understood. The chemical characterization of crustacean pheromones is viewed as a major step in improving our understanding of chemical communication. Knowing the chemical nature of pheromones in freshwater species will boost research on aquatic crustaceans. Interdisciplinary work between chemists (metabolomics), behavioral ecologists (bioassays), neurobiologists (chemoreception), and molecular biologists (genomics) promises to produce significant advances in our understanding of crustacean chemical communication during the coming decade.

Keywords

Reproductive Isolation Chemical Signal Round Goby Chemical Communication Decapod Crustacean 
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 Iván A. Hinojosa for his help in preparing the final figures and Drs. Chuck Derby and Marc Weissburg for helpful comments on the manuscript.

References

  1. Agosta WC (1992) Chemical communication – the language of pheromones. Scientific American Library, New YorkGoogle Scholar
  2. Ameyaw-Akumfi C, Hazlett B (1975) Sex recognition in the crayfish Procambarus clarkii. Science 190:1225–1226CrossRefPubMedGoogle Scholar
  3. 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
  4. Atema J, Engstrom DG (1971) Sex pheromone in the lobster, Homarus americanus. Nature 232:261–263CrossRefPubMedGoogle Scholar
  5. Atema J, Steinbach MA (2007) Chemical communication and social behavior of the lobster Homarus americanus and other decapod Crustacea. In: Duffy JE, Thiel M (eds) Evolutionary ecology of social and sexual systems – crustaceans as model organisms. Oxford University Press, New York, pp 115–144CrossRefGoogle Scholar
  6. Bargmann CI (2006) Comparative chemosensation from receptors to ecology. Nature 444:295–301CrossRefPubMedGoogle Scholar
  7. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2006) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155CrossRefPubMedGoogle Scholar
  8. Borowsky B (1989) The effects of residential tubes on reproductive behaviors in Microdeutopus gryllotalpa (Costa) (Crustacea: Amphipoda). J Exp Mar Biol Ecol 128:117–125CrossRefGoogle Scholar
  9. Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, SunderlandGoogle Scholar
  10. Breithaupt T (2001) Fan organs of crayfish enhance chemical information flow. Biol Bull 200:150–154CrossRefPubMedGoogle Scholar
  11. Bryant BP, Atema J (1987) Diet manipulation affects social behavior of catfish: importance of body odor. J Chem Ecol 13:1645–1661CrossRefGoogle Scholar
  12. 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
  13. Caskey JL, Watson GM, Bauer RT (2009) Studies on contact pheromones of the caridean shrimp Palaemonetes pugio: II. The role of glucosamine in mate recognition. Invertebr Reprod Dev 53:105–116Google Scholar
  14. Catania KC (2006) Underwater “sniffing” by semi-aquatic animals. Nature 444:1024–1025CrossRefPubMedGoogle Scholar
  15. Cheer AYL, Koehl MAR (1987) Paddles and rakes: fluid flow through bristled appendages of small organisms. J Theor Biol 129:17–39CrossRefGoogle Scholar
  16. Clark NL, Gasper J, Sekino M, Springer SA, Aquadro CF, Swanson WJ (2009) Coevolution of interacting fertilization proteins. PLoS Genet 5(7):e1000570CrossRefPubMedGoogle Scholar
  17. Clayton D (2008) Singing and dancing in the ghost crab Ocypode platytarsus (Crustacea, Decapoda, Ocypodidae). J Nat Hist 42:141–155CrossRefGoogle Scholar
  18. Dahl E, Emanuelsson H, von Mecklenburg C (1970) Pheromone transport and reception in an amphipod. Science 170:739–740CrossRefPubMedGoogle Scholar
  19. Denissenko P, Lukaschuk S, Breithaupt T (2007) The flow generated by an active olfactory system of the red swamp crayfish. J Exp Biol 210:4083–4091CrossRefPubMedGoogle Scholar
  20. Dixon CJ, Ahyong ST, Schram FR (2003) A new hypothesis of decapod phylogeny. Crustaceana 76:935–975CrossRefGoogle Scholar
  21. Dreanno C, Kirby RR, Clare AS (2007) Involvement of the barnacle settlement-inducing protein complex (SIPC) in species recognition at settlement. J Exp Mar Biol Ecol 351:276–282CrossRefGoogle Scholar
  22. Freitag J, Krieger J, Strotmann J, Breer H (1995) Two classes of olfactory receptors in Xenopus laevis. Neuron 15:1383–1392CrossRefPubMedGoogle Scholar
  23. Goetze E (2008) Heterospecific mating and partial prezygotic reproductive isolation in the planktonic marine copepods Centropages typicus and Centropages hamatus. Limnol Oceanogr 53:33–45CrossRefGoogle Scholar
  24. Hargeby A, Erlandsson J (2006) Is size-assortative mating important for rapid pigment differentiation in a freshwater isopod? J Evol Biol 19:1911–1919CrossRefPubMedGoogle Scholar
  25. Holdich DM (1984) The cuticular surface of woodlice: a search for receptors. Symp Zool Soc Lond 53:9–48Google Scholar
  26. Hurst JL (2005) Scent marking and social communication. In: McGregor PK (ed) Animal communication networks. Cambridge University Press, Cambridge, pp 219–243CrossRefGoogle Scholar
  27. Ingvarsdóttir A, Birkett MA, Duce I, Mordue W, Pickett JA, Wadhams LJ, Mordue (Luntz) AJ (2002) Role of semiochemicals in mate location by parasitic sea louse, Lepeophtheirus salmonis. J Chem Ecol 28:2107–2117CrossRefPubMedGoogle Scholar
  28. Johansson KUI, Hallberg E (1992) Male-specific structures in the olfactory system of mysids (Mysidacea; Crustacea). Cell Tissue Res 268:359–368CrossRefGoogle Scholar
  29. Johnson NS, Li W (2010) Understanding behavioral responses of fish to pheromones in natural freshwater environments. J Comp Physiol A. 196:701–711Google Scholar
  30. Kamio M, Matsunaga S, Fusetani N (2000) Studies on sex pheromones of the helmet crab, Telmessus cheiragonus. 1. An assay based on precopulatory mate-guarding. Zool Sci 6:731–733CrossRefGoogle Scholar
  31. Kamio M, Matsunaga S, Fusetani N (2002) Copulation pheromone in the crab Telmessus cheiragonus (Brachyura: Decapoda). Mar Ecol Prog Ser 234:183–190CrossRefGoogle Scholar
  32. Koehl MAR (2001) Fluid dynamics of animal appendages that capture molecules: Arthropod olfactory antennae. In: Fauci L, Gueron S (eds) Computational modeling in biological fluid dynamics. Springer, New York, pp 97–116Google Scholar
  33. Kolding S (1986) Interspecific competition for mates and habitat selection in five species of Gammarus (Amphipoda: Crustacea). Mar Biol 91:491–495CrossRefGoogle Scholar
  34. Lee JK, Strausfeld NJ (1990) Structure, distribution and number of surface sensilla and their receptor cells on the olfactory appendage of the male moth Manduca sexta. J Neurocytol 19:519–538CrossRefPubMedGoogle Scholar
  35. Loudon C, Koehl MAR (2000) Sniffing by a silkworm moth: wing fanning enhances air penetration through and pheromone interception by antennae. J Exp Biol 203:2977–2990PubMedGoogle Scholar
  36. Lürling M, Scheffer M (2007) Info-disruption: pollution and the transfer of chemical information between organisms. Trends Ecol Evol 22:374–379CrossRefPubMedGoogle Scholar
  37. Mead F, Gabouriaut D (1977) Chevauchée nuptiale et accouplement chez l’isopode terrestre Helleria brevicornis Ebner (Tylidae). Analyse des facteurs qui contrólent ces deux phases du comportement sexuel. Behaviour 63:262–280CrossRefGoogle Scholar
  38. Moore P, Fields DM, Jen Y (1999) Physical constraints of chemoreception in foraging copepods. Limnol Oceanogr 44:166–177CrossRefGoogle Scholar
  39. Mordue (Luntz) AJ, Birkett MA (2009) A review of host finding behaviour in the parasitic sea louse, Lepeophtheirus salmonis (Caligidae: Copepoda). J Fish Dis 32:3–13CrossRefGoogle Scholar
  40. Painter SD, Clough B, Garden RW, Sweedler JV, Nagle GT (1998) Characterization of Aplysia attractin, the first water-borne peptide pheromone in invertebrates. Biol Bull 194:120–131CrossRefPubMedGoogle Scholar
  41. Peñalva-Arana DC, Lynch M, Robertson HM (2009) The chemoreceptor genes of the waterflea Daphnia pulex: many Grs but no Ors. BMC Evol Biol 9:79. doi: 10.1186/1471-2148-9-79 CrossRefPubMedGoogle Scholar
  42. Phelan PL (1997) Evolution of mate-signalling in moths: phylogenetic considerations and prediction from the asymmetric tracking hypothesis. In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and Arachnids. Cambridge University Press, Cambridge, pp 240–256CrossRefGoogle Scholar
  43. Poore AGB, Hill NA, Sotka EE (2008) Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae. Evolution 62:21–38PubMedGoogle Scholar
  44. Ratchford SG, Eggleston DB (1998) Size- and scale-dependent chemical attraction contribute to an ontogenetic shift in sociality. Anim Behav 56:1027–1034CrossRefPubMedGoogle Scholar
  45. Ravi Ram K, Wolfner MF (2007) Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr Comp Biol 47:427–445CrossRefGoogle Scholar
  46. Rittschof D, Cohen JH (2004) Crustacean peptide and peptide-like pheromones and kairomones. Peptides 25:1503–1516CrossRefPubMedGoogle Scholar
  47. Roberts JA, Uetz GW (2004) Species-specificity of chemical signals: Silk source affects discrimination in a wolf spider (Araneae: Lycosidae). Insect Behav 17:477–491CrossRefGoogle Scholar
  48. Roberts JA, Uetz GW (2005) Discrimination of female reproductive state from chemical cues in silk by males of the wolf spider, Schizocosa ocreata (Araneae, Lycosidae). Anim Behav 70:217–223CrossRefPubMedGoogle Scholar
  49. Roper TJ, Conradt J, Butler JE, Ostler CJ, Schmid TK (1993) Territorial marking with faeces in badgers (Meles meles): a comparison of boundary and hinterland latrine use. Behaviour 127:289–307CrossRefPubMedGoogle Scholar
  50. Ryan EP (1966) Pheromone: evidence in a decapod crustacean. Science 151:340–341CrossRefPubMedGoogle Scholar
  51. Seelinger G (1983) Response characteristics and specificity of chemoreceptors in Hemilepistus reaumuri (Crustacea, Isopoda). J Comp Physiol A 152:219–229CrossRefGoogle Scholar
  52. Smajda C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102:77–97CrossRefGoogle Scholar
  53. Sorensen PW, Stacey NE (2004) Brief review of fish pheromones and discussion of their possible uses in the control of non-indigenous teleost fishes. N Z J Mar Freshwater Res 38:399–417CrossRefGoogle Scholar
  54. Stanhope MJ, Connelly MM, Hartwick B (1992) Evolution of a crustacean chemical communication channel: behavioral and ecological genetic evidence for a habitat-modified, race-specific pheromone. J Chem Ecol 18:1871–1887CrossRefGoogle Scholar
  55. Strausfeld N, Reisenman CE (2009) Dimorphic olfactory lobes in the Arthropoda. Ann N Y Acad Sci 1170:487–496CrossRefPubMedGoogle Scholar
  56. Sutherland DL, Hogg ID, Waas JR (2010) Phylogeography and species discrimination in the Paracalliope fluviatilis species complex (Crustacea: Amphipoda): can morphologically similar heterospecifics identify compatible mates? Biol J Linn Soc 99:196–205CrossRefGoogle Scholar
  57. Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–144CrossRefPubMedGoogle Scholar
  58. Symonds MRE, Elgar MA (2004) The mode of pheromone evolution: evidence from bark beetles. Proc Biol Sci 271:839–846CrossRefPubMedGoogle Scholar
  59. Symonds MRE, Elgar MA (2008) The evolution of pheromone diversity. Trends Ecol Evol 23:220–228CrossRefPubMedGoogle Scholar
  60. 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
  61. Van Son TC, Thiel M (2007) Anthropogenic stressors and their effects on the behavior of aquatic crustaceans. In: Duffy JE, Thiel M (eds) Evolutionary ecology of social and sexual systems: Crustaceans as model organisms. Oxford University Press, New York, pp 413–441CrossRefGoogle Scholar
  62. Vickers NJ (2000) Mechanisms of animal navigation in odor plumes. Biol Bull 198:203–212CrossRefPubMedGoogle Scholar
  63. Voigt CC, von Helversen O (1999) Storage and display of odour by male Saccopteryx bilineata (Chiroptera, Emballonuridae). Behav Ecol Sociobiol 47:29–40CrossRefGoogle Scholar
  64. Voigt CC, Caspers B, Speck S (2005) Bats, bacteria, and bat smell: sex-specific diversity of microbes in a sexually selected scent organ. J Mammal 86:745–749CrossRefGoogle Scholar
  65. Weissburg MJ (2000) The fluid dynamical context of chemosensory behavior. Biol Bull 198:188–202CrossRefPubMedGoogle Scholar
  66. 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
  67. Zhang D, Lin J, Harley M, Hardege JD (2010a) Characterization of a sex pheromone in a simultaneous hermaphroditic shrimp, Lysmata wurdemanni. Mar Biol 157:1–6CrossRefGoogle Scholar
  68. Zhang D, Zhu J, Hardege JD, Lin J (2010b) Surface glycoproteins are not the contact pheromones in the Lysmata shrimp. Mar Biol 157:171–176CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Facultad Ciencias del MarUniversidad Católica del NorteCoquimboChile

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