Ecological Research

, Volume 27, Issue 1, pp 53–59 | Cite as

Morphological asymmetry and behavioral laterality in the crayfish, Procambarus clarkii

Original Article

Abstract

Lateral asymmetry is found widely among vertebrates, but is scarcely observed in invertebrates. Here, morphological asymmetry and behavioral laterality of a wild crayfish, Procambarus clarkii, was investigated. The carapace morphology of crayfish showed left–right differences; in some, the right side of the carapace was larger than the left side, while in others, the left side was larger. A bimodal distribution in the direction of escape behaviors induced by a tactile stimulus was also observed. Experimental crayfish were definitively divided into two groups: individuals that frequently jumped leftward (right type) and those that jumped rightward (left type). Moreover, carapace asymmetry and lateralized escape responses were significantly correlated. These results suggest that crayfish exhibit left–right dimorphism in natural populations. The ecological advantages and maintenance mechanisms underlying these behaviors are also discussed.

Keywords

Laterality Escape behavior Crustacean Morphological asymmetry 

Notes

Acknowledgments

We deeply appreciate Yasuhiro Takemon and members of the Aquatic life study group of Mizorogai-ke pond for permission and help with sampling. Hiroshi Ashiwa, Tomohiro Takeyama, Masaki Yasugi for help with daily care of crayfish. And other all members of Animal Ecology Laboratory for advice and inspired discussion throughout this research. This study was partly supported by JSPS research fellowships to S.T. and Y.T., the Grant for the Biodiversity Research of the 21st Century COE (A14), the Global Center of Excellence Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” and Grants-in-aid of Scientific Research on Priority Areas (#14087203) of the Japanese Ministry of Education, Culture, Sports, Science and Technology.

References

  1. Ades C, Ramires EN (2002) Asymmetry of leg use during prey handling in the spider Scytodes globula (Scytodedae). J Insect Behav 15:563–570CrossRefGoogle Scholar
  2. Babcock LE (1993) Trilobite malformation and the fossil record of behavioral asymmetry. J Paleontol 67:217–229Google Scholar
  3. Bisazza A, Rogers LJ, Vallortigara G (1998) The origin of cerebral asymmetry: a review of evidence of behavioral and brain lateralization in fishes, reptiles and amphibians. Neurosci Biobehav Rev 22:411–426PubMedCrossRefGoogle Scholar
  4. Bisazza A, Cantalupo C, Capocchiano M, Vallortigara G (2000) Population lateralization and social behaviour: a study with 16 species of fish. Laterality 5:269–284PubMedCrossRefGoogle Scholar
  5. Boesch C (1991) Handedness in wild chimpanzees. Int J Primatol 12:541–588CrossRefGoogle Scholar
  6. Byrne RA, Kuba MJ, Meisel DV (2004) Lateralised eye use in Octopus vulgaris shows antisymmetrical distribution. Anim Behav 68:1107–1114CrossRefGoogle Scholar
  7. Cantalupo C, Bisazza A, Vallortigara G (1995) Lateralization of predator–evasion response in a teleost fish (Girardinus falcatus). Neuropsychologia 33:1637–1646PubMedCrossRefGoogle Scholar
  8. Deckel AW (1995) Laterality of aggressive responses in Anolis. J Exp Zool 272:194–200CrossRefGoogle Scholar
  9. Edwards DH, Heitler WJ, Krasne FB (1999) Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends Neurosci 22:153–161PubMedCrossRefGoogle Scholar
  10. Hamilton PV, Nishimoto RT, Halusky JG (1976) Cheliped laterality in Callinectes sapidus (Crustacea: Portunidae). Biol Bull 150:393–401PubMedCrossRefGoogle Scholar
  11. Harris LJ (2000) On the evolution of handedness: a speculative analysis of Darwin’s views and a review of early studies of handedness in “the Nearest Allies of Man”. Brain Lang 73:132–188PubMedCrossRefGoogle Scholar
  12. Hori M (1991) Feeding relationships among cichlid fishes in Lake Tanganyika: effects of intra- and interspecific variations of feeding behavior on their coexistence. Ecol Int Bull 19:89–101Google Scholar
  13. Hori M (1993) Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 260:216–219PubMedCrossRefGoogle Scholar
  14. Hori M, Ochi H, Kohda M (2007) Inheritance pattern of lateral dimorphism in two cichlids, a scale eater Perissodus microlepis and the herbivore Neolamprogus moorii, in Lake Tanganyika. Zool Sci 24:486–492PubMedCrossRefGoogle Scholar
  15. Izvekov EI, Nepomnyashchikh VA (2008) Laterality of the initial stage of escape response in roach (Rutilus rutilus) upon impact of alternating electric current. Biol Bull 35:30–36CrossRefGoogle Scholar
  16. Jackson DJ, Mcmillan DL (2000) Tailflick escape behavior in larval and juvenile lobsters (Homarus americanus) and crayfish (Cherax destructor). Biol Bull 198:307–318PubMedCrossRefGoogle Scholar
  17. Kawai T, Kobayashi Y (2005) Origin and current distribution of the alien crayfish, Procambarus clarkii (Girard, 1852) in Japan. Crustaceana 78:1143–1149CrossRefGoogle Scholar
  18. Kells AR, Goulson D (2001) Evidence for handedness in bumblebees. J Insect Behav 14:47–55CrossRefGoogle Scholar
  19. Liem KF, Stewart DJ (1976) Evolution of the scale-eating cichlid fishes of Lake Tanganyika: a genetic revision with a description of a new species. Bull Mus Comp Zool 147:319–350Google Scholar
  20. Lippolis G, Bisazza A, Rogers LJ, Vallortigara G (2002) Lateralisation of predator avoidance responses in three species of toads. Laterality 7:163–183PubMedCrossRefGoogle Scholar
  21. Mariappan P, Balasundaram C, Schmitz B (2000) Decapod crustacean chelipeds: an overview. J Biosci 25:301–313PubMedCrossRefGoogle Scholar
  22. Mboko SK, Kohda M, Hori M (1998) Asymmetry of mouth-opening of a small herbivorous cichlid fish Telmatochromis temporalis in Lake Tanganyika. Zool Sci 15:405–408PubMedCrossRefGoogle Scholar
  23. Nakajima M, Matsuda H, Hori M (2004) Persistence and fluctuation of lateral dimorphism in fishes. Am Nat 163:692–698PubMedCrossRefGoogle Scholar
  24. Nakajima M, Yodo T, Katano O (2007) Righty fish are hooked on the right side of their mouths—observations from an angling experiment with largemouth bass, Micropterus salmoides. Zool Sci 24:855–859PubMedCrossRefGoogle Scholar
  25. Neil DM, Ansell AD (1995) The orientation of tail-flip escape swimming in Decapod and mysid crustaceans. J Marine Biol Assoc UK 75:55–70CrossRefGoogle Scholar
  26. Oseen KL, Newhook LKD, Wassersug RJ (2001) Turning bias in woodfrog (Rana sylvatica) tadpoles. Herpetologica 57:432–437Google Scholar
  27. Palmer AR (1996) Waltzing with asymmetry. Bioscience 46:518–533CrossRefGoogle Scholar
  28. Pratt AE, McLain DK (2002) Antisymmetry in male fiddler crabs and the decision to feed or breed. Funct Ecol 16:89–98CrossRefGoogle Scholar
  29. Read AT, Govind CK (1997) Claw transformation and regeneration in adult snapping shrimp: test of the inhibition hypothesis for maintaining bilateral asymmetry. Biol Bull 193:401–409CrossRefGoogle Scholar
  30. Reddon AR, Hurd PL (2008) Aggression, sex and individual differences in cerebral lateralization in a cichlid fish. Biol Lett 4:338–340PubMedCrossRefGoogle Scholar
  31. Robins A, Lippolis G, Vallortigara G, Rogers LJ (1998) Lateralized agonistic responses and hindlimb use in toads. Anim Behav 56:875–881PubMedCrossRefGoogle Scholar
  32. Rogers LJ (2002) Lateralization in vertebrates: its early evolution, general pattern, and development. Adv Study Behav 31:107–161CrossRefGoogle Scholar
  33. Rogers LJ, Workman L (1993) Footedness in birds. Anim Behav 45:409–411CrossRefGoogle Scholar
  34. Seki S, Kohda M, Hori M (2000) Asymmetry of mouth morph of freshwater goby, Rhinogobius flumineus. Zool Sci 17:1321–1325CrossRefGoogle Scholar
  35. Takeda S, Murai M (1993) Asymmetry in male fiddler-crab is related to the basic pattern of claw-waving display. Biol Bull 184:203–208CrossRefGoogle Scholar
  36. Takeuchi Y, Hori M (2008) Behavioral laterality in the shrimp-eating cichlid fish Neolamprologus fasciatus, in Lake Tanganyika. Anim Behav 75:1359–1366CrossRefGoogle Scholar
  37. Takeuchi Y, Tobo S, Hori M (2008) Morphological asymmetry of the abdomen and behavioral laterality in atyid shrimps. Zool Sci 25:355–363PubMedCrossRefGoogle Scholar
  38. Takeuchi Y, Hori M, Myant O, Kohda M (2010) Lateral bias of agonistic responses to mirror images and morphological asymmetry in the Siamese fighting fish (Betta splendens). Behav Brain Res 20:106–111CrossRefGoogle Scholar
  39. Tommasi L (2009) Mechanisms and functions of brain and behavioural asymmetries. Philos Trans R Soc B 364:855–859Google Scholar
  40. Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–633PubMedGoogle Scholar
  41. Vallortigara G, Rogers LJ, Bisazza A, Lippolis G, Robins A (1998) Complementary right and left hemifield use for predatory and agonistic behaviour in toads. Neuroreport 9:3341–3344PubMedCrossRefGoogle Scholar
  42. Weir AAS, Kenward B, Chappell J, Kacelnik A (2004) Lateralization of tool use in New Caledonian crows (Corvus moneduloides). Proc R Soc London B 271:s344–s346CrossRefGoogle Scholar
  43. Whishaw IQ (1992) Lateralization and reaching skill related: results and implications from a large sample of Long-Evans rats. Behav Brain Res 52:45–48PubMedCrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2011

Authors and Affiliations

  1. 1.Laboratory of Animal Ecology, Division of Biological Science, Graduate School of ScienceKyoto UniversityKyotoJapan
  2. 2.Department of Biological Science, Graduated School of ScienceNagoya UniversityNagoyaJapan

Personalised recommendations