Chemical cues mediate social monogamy in a marine caridean shrimp, Lysmata debelius

  • Xin Liu
  • Dong ZhangEmail author
  • Tingting Lin
  • Zhenzhen Yan


To better understand the social monogamy in decapod crustaceans, individual recognition in a socially monogamous shrimp, Lysmata debelius, was investigated. We hypothesized that chemical cues play an important role in mediating monogamy, because chemical cues is the primary form of communicaition. To test this, we first examined mate recognition and second tested the presence of chemical cues in individual recognition. The individual recognition to conspecifics of different reproductive statuses was tested in a Y-maze excluding visual cues and tactile cues. Inter-molt and pre-molt euhermaphrodite-phase shrimps served as males and females, respectively. A focal male (cue detector) was placed in the bottom chamber, and two shrimps (cue releasers) of different statuses were placed in the upper two champers, respectively. We find that the focal male spent more time in the front of the chamber holding the paired partner when the other shrimp was not female, and prefered to the female stranger rather than its male partner. Interestingly, when both stranger and partner were females, the focal male actually spent more time in the chamber holding the female stranger. The results indicate that olfactory chemical cues mediate monogamy in L. debelius in place of visual cues, and the chemical cues are probably individual specific (i.e. identification odor). The courtship and mating behaviors of L. debelius were also reported for the first time. During mating, L. debelius displayed no courtship behavior, differing from its sister species, L. wurdemanni which live in aggregation, and L. amboinensis which live in low denstiy. Combining the previous results in L. wurdemanni and L. amboinensis, we can conclude that L. wurdemanni has the most elaborate precopulatory courtship rituals, L. amboinesis has less, and L. debelius has none, i.e. the behavioral activity between male and pre- and post-molt female decreases with the population intensity. This behavioral pattern should be sexually selected in different social systems. The present study would enrich our understanding of the evolution of social-dependent behaviors in crustaceans.


Individual recognition Chemical cue Lysmata debelius Monogamy 



We thank Xiong Zou for the help with animal transportation. We are grateful for the valuable comments made by the reviewers of the manuscript.


This work was supported by the National Natural Science Foundation of China (grant number: 41576161).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval and consent to participate

Ethical approval and consent to participate were not required for this work.

Consent for publication

Not applicable.


  1. Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJGoogle Scholar
  2. Alcock J (2001) Animal behavior: an evolutionary approach. Sinauer Associates, SunderlandGoogle Scholar
  3. Atema J (1984) Review of sexual selection and chemical communication in the lobster, Homarus americanus. Can J Fish Aquatic Sci 43:2283–2290. CrossRefGoogle Scholar
  4. Atema J (1995) Chemical signals in the marine environment: dispersal, detection, and temporal signal analysis. Proc Natl Acad Sci USA 92:62–66. CrossRefPubMedGoogle Scholar
  5. Baeza JA (2013) Molecular phylogeny of broken-back shrimps (genus Lysmata and allies): A test of the ‘Tomlinson–Ghiselin’ hypothesis explaining the evolution ofhermaphroditism. Mol Phylog Evol 69:46–62CrossRefGoogle Scholar
  6. Bagnères AG, Hanus R (2015) Communication and social regulation in termites. In: Aquiloni L, Tricarico E (eds) Social recognition in invertebrates. Springer, Heidelberg, pp 193–248Google Scholar
  7. 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 76:691–699. CrossRefGoogle Scholar
  8. Bauer RT (1979) Sex attraction and recognition in the caridean shrimp Heptacarpus paludicola Holmes (Decapoda: Hippolytidae). Mar Behav Physiol 6:157–174. CrossRefGoogle Scholar
  9. Bauer RT (2000) Simultaneous hermaphroditism in caridean shrimps: a unique and puzzling sexual system in the Decapoda. J Crust Biol 20:116–128CrossRefGoogle Scholar
  10. Bauer RT (2006) Same sexual system but variable sociobiology: evolution of protandric simultaneous hermaphroditism in Lysmata shrimps. Integr Comp Biol 46:430–438. CrossRefPubMedGoogle Scholar
  11. Bauer RT, Holt GJ (1998) Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): an undescribed sexual system in the decapod Crustacea. Mar Biol 132:223–235. CrossRefGoogle Scholar
  12. Bauer RT (2002) Reproductive ecology of a protandric simultaneous hermaphrodite, the shrimp Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae). J Crust Biol 22:742–749CrossRefGoogle Scholar
  13. Bauer RT, Thiel M (2011) First description of a pure-search mating system and protandry in the shrimp Rhynchocinetes uritai (Decapoda:Caridea). J Crust Biol 31:286–295. CrossRefGoogle Scholar
  14. Caldwell RL (1985) A test of individual recognition in the stomatopod Gonodactylus festae. Anim Behav 33:101–106. CrossRefGoogle Scholar
  15. Cely C, Tibbetts E (2017) Individual recognition. In: Vonk J, Shackelford T (eds) Encyclopedia of animal cognition and behavior. Springer, Heidelberg, pp 1–13Google Scholar
  16. Chak S, Bauer R, Thiel M (2015) Social behaviour and recognition in decapod shrimps, with emphasis on the Caridea. In: Aquiloni L, Tricarico E (eds) Social recognition in invertebrates. Springer, Heidelberg, pp 57–84Google Scholar
  17. Correa C, Thiel M (2003) Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology. Rev Chil Hist Nat 76:187–203. CrossRefGoogle Scholar
  18. Díaz ER, Thiel M (2004) Chemical and visual communication during mate searching in rock shrimp. Biol Bull 206:134–143. CrossRefPubMedGoogle Scholar
  19. Ellis PE, Free JB (1964) Social organization of animal communities. Nature 201:861–863. CrossRefGoogle Scholar
  20. Fiedler GC (1998) Functional, simultaneous hermaphroditism in female-phase Lysmata amboinensis (Decapoda: Caridea: Hippolytidae) Pac Sci 52:161–169Google Scholar
  21. Fletcher DJ, Kötter I, Wunsch M et al (1995) Preliminary observations on the reproductive biology of ornamental cleaner prawns Stenopus hispidus, Lysmata amboinensis, and Lysmata debelius. Intl Zoo Yearbook 34:73–77. CrossRefGoogle Scholar
  22. Gherardi F, Tiedemann J (2004) Binary individual recognition in hermit crabs. Behav Ecol Sociobiol 55:524–530. CrossRefGoogle Scholar
  23. Gherardi F, Aquiloni L, Tricarico E (2012) Revisiting social recognition systems in invertebrates. Anim Cogn 15:745–762. CrossRefPubMedGoogle Scholar
  24. Hardege JD, Terschak JA (2010) Identification of crustacean sex pheromones. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 373–392CrossRefGoogle Scholar
  25. Johnson VR (1977) Individual recognition in the banded shrimp Stenopus hispidus. Anim Behav 25:418–428. CrossRefGoogle Scholar
  26. Karavanich C, Atema J (1998) Olfactory recognition of urine signals in dominance fights between male lobster, Homarus Americanus. Behaviour 135:719-730. http://
  27. Kelly LS, Snell TW, Lonsdale DJ (1998) Chemical communication during mating of the harpacticoid Tigriopus japonicus. Phil Trans R Soc Lond B 353:737-744. http://
  28. Kenison EK, Weldy PY, Williams RN (2018) There must be something in the water: assessing the behavioral responses of rusty crayfish (Orconectes rusticus) to fish and amphibian predator kairomones. J Ethol 36:77–84. CrossRefGoogle Scholar
  29. Kvarnemo C (2018) Why do some animals mate with one partner rather than many? A review of causes and consequences of monogamy. Biol Rev 93:1795-1812. http://
  30. Lin J, Zhang D (2001) Reproduction in a simultaneous hermaphrodite shrimp, Lysmata wurdemanni: any two will do? Mar Biol 139:919–922.
  31. Mateo JM (2004) Recognition systems and biological organization: the perception component of social recognition. Ann Zool Fennici 41:729–745Google Scholar
  32. Meunier J, Delemont O, Lucas C (2011) Recognition in ants: social origin matters. PLoS ONE 6(5):e19347. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Page RE, Breed MD (1987) Kin recognition in social bees. Trends Ecol Evol 2:272–275. CrossRefPubMedGoogle Scholar
  34. Palmtag MR, Holt GJ (2007) Experimental studies to evaluate larval survival of the fire shrimp, Lysmata debelius, to the juvenile Stage. J World Aquacul Soc 38(1):102–113. CrossRefGoogle Scholar
  35. Rahman N, Dunham DW, Govind CK (2001) Mate recognition and pairing in the big-clawed snapping shrimp, Alpheus herterochelis. Mar Fresh Behav Physiol 34:213–226. CrossRefGoogle Scholar
  36. Rhyne AL, Lin J (2006) A Western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bull Mar Sci 79:165–204Google Scholar
  37. Rufino M, Jones D (2001) Binary individual recognition in Lysmata debelius (Decapoda: Hippolytidae) under laboratory conditions. J Crust Biol 21:388–392.;2
  38. Schoepf I, Schradin C (2012) Differences in social behaviour between group-living and solitary African striped mice, Rhabdomys pumilio. Anim Behav 84:1159–1167. CrossRefGoogle Scholar
  39. Seibt U (1973) Sense of smell and pair bond in Hymeoncera picta Dana. Micronesica 9:231–236Google Scholar
  40. Signorotti L, Cervo R, D’Ettorre P (2015) Ontogeny of nestmate recognition in social Hymenoptera. In: Aquiloni L, Tricarico E (eds) Social recognition in invertebrates. Springer, Cham (Switzerland), pp 165–191CrossRefGoogle Scholar
  41. Tibbetts EA (2002) Visual signals of individual identity in the wasp Polistes fuscatus. Proc R Soc B: Biol Sci 269:1423–1428. CrossRefGoogle Scholar
  42. Wickler W (1973) Biology of Hymenocera picta Dana. Micronesica 9:225–230Google Scholar
  43. Wiley RH (2013) Specificity and multiplicity in the recognition of individuals: implications for the evolution of social behaviour. Biol Rev Camb Phil Soc 88:179–195. CrossRefGoogle Scholar
  44. Wong JW, Michiels NK (2011) Control of social monogamy through aggression in a hermaphroditic shrimp. Front Zool 8(1):30. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Wyatt TD (2014) Pheromones and animal behavior: chemical signals and signature. Cambridge University Press, CambridgeGoogle Scholar
  46. Zhang D, Lin J, Creswell RL (1998) Mating behavior and spawning of the banded coral shrimp Stenopus hispidus in the laboratory. J Crust Biol 18(3):511–518. CrossRefGoogle Scholar
  47. Zhang D, Lin J (2004a) Mating without anterior pleopods in a simultaneous hermaphroditic shrimp, Lysmata wurdemanni (Decapoda, Caridea). Crustaceana 77:1203–1212. CrossRefGoogle Scholar
  48. Zhang D, Lin J (2004b) Fertilization success without anterior pleopods in Lysmata wurdemanni (decapoda: caridea), a protandric simultaneous hermaphrodite. J Crust Biol 24(3):470–473. CrossRefGoogle Scholar
  49. Zhang D, Lin J (2006) Mate recognition in a simultaneous hermaphroditic shrimp, Lysmata wurdemanni (Caridea: Hippolytidae). Anim Behav 71:1191–1196. CrossRefGoogle Scholar
  50. Zhang D, Rhyne AL, Lin J (2007) Density-dependent effect on reproductive behavior of Lysmata amboinensis and L. boggessi (Decapoda: Caridea: Hippolytidae). J Mar Biol Assoc UK 87:517–522. CrossRefGoogle Scholar
  51. Zhang D, Cai S, Liu H, Lin J (2008) Antennal sensilla in the genus Lysmata (Caridea). J Crust Biol 28:433–438. CrossRefGoogle Scholar
  52. Zhang D, Lin J, Hardege JD, Rhyne A (2009) Reproductive isolation between two sympatric simultaneous hermaphroditic shrimp, Lysmata wurdemanni and L. boggessi. Mar Boil Res 5:470–477. CrossRefGoogle Scholar
  53. Zhang D, Lin J, Harley M, Hardege JD (2010a) Characterization of a sex pheromone in a simultaneous hermaphroditic shrimp, Lysmata wurdemanni (Caridea: Hippolytidae). Mar Biol 157:1–6. CrossRefGoogle Scholar
  54. Zhang D, Zhu J, Lin J, Hardege JD (2010b) Surface glycoproteins are not the contact phremones in the Lysmata shrimp. Mar Biol 157:171–176. CrossRefGoogle Scholar
  55. Zhang D, Terschak JA, Harley MA, Lin J, Hardege JD (2011) Simultaneously hermaphroditic shrimp use lipophilic cuticular hydrocarbons as contact sex pheromones. PLoS ONE 6(4): e17720.
  56. Zhang D, Yao Z, Lai Q, Lin J (2012) Effects of sex change on number of olfactory chemoreceptors in Lysmata shrimp. J Shellfish Res 31:861–865. CrossRefGoogle Scholar
  57. Zhu J, Zhang D, Lin J, Michael SG (2012) Aesthetascs in Lysmata spp. shrimp: sexual dimorphism and relationship with social environments. Mar Biol 159:507–517. CrossRefGoogle Scholar

Copyright information

© Japan Ethological Society 2019

Authors and Affiliations

  • Xin Liu
    • 1
    • 2
  • Dong Zhang
    • 1
    • 2
    Email author
  • Tingting Lin
    • 1
    • 2
  • Zhenzhen Yan
    • 1
    • 2
  1. 1.Key Laboratory of East China Sea Fishery Resources ExploitationMinistry of Agriculture and Rural AffairsShanghaiPeople’s Republic of China
  2. 2.East China Sea Fisheries Research InstituteChinese Academy of Fishery SciencesShanghaiPeople’s Republic of China

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