Advertisement

Journal of Comparative Physiology A

, Volume 179, Issue 4, pp 473–481 | Cite as

Behavioural evidence for colour vision in stomatopod crustaceans

  • N. J. Marshall
  • J. P. Jones
  • T. W. Cronin
Original Paper

Abstract

If an organism can be taught to respond in a particular way to a wavelength of light, irrespective of that light's intensity, then it must be able to perceive the colour of the stimulus. No marine invertebrate has yet been shown to have colour vision. Stomatopod crustaceans (mantis shrimps) are colourful animals and their eyes have many adaptations which indicate that they are capable of such spectral analysis. We adopted an associative learning paradigm to attempt to demonstrate colour vision. Stomatopods readily learnt to choose some colours from arrays of greys, even when the correct choice colours were darker than the ones they had been trained to. Possible mechanisms underlying colour vision in these animals, and their ecological significance are discussed. A simple model is presented which may help interpret the complex-stomatopod colour vision system and explain some of the learning anomalies.

Key words

Stomatopod Colour vision Crustacean behaviour 

Abbreviations

ND

neutral density

OD

optical density

R8

Retinular cell 8

R1–7

Retinular cells 1–7

R1D

Distally placed R1–7 retinular cells in mid-band row 1

e.g. R1P

Proximally placed R1–7 retinular cells in mid-band row 1

D/P

Estimate of chromatic signal ratio

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Burkhardt D (1983) Wavelength perception and colour vision. In: Cosens DJ, Vince-Price D (eds) The biology of photoreception. Cambridge University Press, pp 371–397Google Scholar
  2. Burrows M (1969) The mechanics and neural control of the prey capture strike in the mantid shrimps Squilla and Hemisquilla. Z Vergl Physiol 62: 361–381Google Scholar
  3. Caldwell RL (1982) Interspecific chemically mediated recognition in two competing stomatopods. Mar Behav Physiol 8: 189–197Google Scholar
  4. Caldwell RL, Dingle H (1976) Stomatopods. Sci Am 234: 80–89Google Scholar
  5. Cronin TW, Forward RB (1988) The visual pigments of crabs. I. Spectral characteristics. J Comp Physiol A 162: 463–478Google Scholar
  6. Cronin TW, Marshall NJ (1989a) Multiple spectral classes of photo-receptors in the retinas of gonodactyloid stomatopod crustaceans. J Comp Physiol A 166: 261–275Google Scholar
  7. Cronin TW, Marshall NJ (1989b) A retina with at least ten spectral types of photoreceptors in a mantis shrimp. Nature 339: 137–140Google Scholar
  8. Cronin TW, Marshall NJ, Land MF (1994a) The unique visual system of the mantis shrimp. Am Sci 82: 356–365Google Scholar
  9. Cronin TW, Marshall NJ, Caldwell RL (1994b) The intrarhabdomal niters in the retinas of mantis shrimps. Vision Res 34: 279–291Google Scholar
  10. Cronin TW, Marshall NJ, Caldwell RL (1994c) The retinas of mantis shrimps from low light environments (Crustacea; Stomatopoda; Gonodactylidae). J Comp Physiol A 174: 607–619Google Scholar
  11. Cronin TW, Marshall NJ, Caldwell RL, Shashar N (1994d) Specialisation of retinal function in the compound eyes of mantis shrimps. Vision Res 34: 2639–2656Google Scholar
  12. Cronin TW, Marshall NJ, Quinn CA, King CA (1994e) Ultraviolet photoreception in mantis shrimp. Vision Res 34: 1443–1452Google Scholar
  13. Cutler DE, Bennett RR, Stevenson RD, White RH (1995) Feeding behaviour in the nocturnal moth Manduca sexta is mediated mainly by blue receptors, but where are they located in the retina? J Exp Biol 198: 1909–1917Google Scholar
  14. Frisch K von, Kuppelwieser EM (1913) Über den Einfluß der Lichtfarbe auf die phototaktische Reaktion niederer Krebse. Biol Zentralbl 33: 517–522Google Scholar
  15. Fukushi T (1990) Colour discrimination from various shades of grey in the trained blowfly, Lucilia cuprina. J Insect Physiol 36: 69–75Google Scholar
  16. Goldsmith TH (1990) Optimisation, constraint, and history in the evolution of eyes. Q Rev Biol 65: 281–322Google Scholar
  17. Hazlett BA (1979) The meral spot of Gonodactylus oerstedii Hansen as a visual stimulus (Stomatopoda, Gonodactylidae). Crustaceana 36: 196–198Google Scholar
  18. Hyatt GW (1974) Behavioural evidence for light intensity discrimination by the fiddler crab, Uca pugilator (Brachyura, Ocypodidae). Anim Behav 22: 796–801Google Scholar
  19. Hyatt GW (1975) Physiological and behavioural evidence for colour discrimination by fiddler crabs (Brachyura, Ocypodidae, genus Uca). In: Vernberg FJ (ed) Physiological ecology of estuarine organisms. Univ of South Carolina Press, Columbia, pp 333–365Google Scholar
  20. Jacobs GH (1981) Comparative colour vision. Academic Press, New York London Toronto Sydney San FranciscoGoogle Scholar
  21. Lall AB, Cronin TW (1987) Spectral sensitivity of the compound eyes in the purple land crab Gecarcinus lateralis (Freminville). Biol Bull 173: 398–406Google Scholar
  22. Leggett LMW (1979) A retinal substrate for colour discrimination in crabs. J Comp Physiol 133: 159–166Google Scholar
  23. Lunau K, Maier EJ (1995) Innate colour preferences of flower visitors. J Comp Physiol A 177: 1–19Google Scholar
  24. Manning RB, Schiff H, Abbott BC (1984) Eye structure and the classification of stomatopod Crustacea. Zool Scripta 13(1): 41–44Google Scholar
  25. Marshall NJ (1988) A unique colour and polarisation vision system in mantis shrimps. Nature 333: 557–560Google Scholar
  26. Marshall NJ, Land MF, King CA, Cronin TW (1991a) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarised light. Phil Trans R Soc Lond B 334: 33–56Google Scholar
  27. Marshall NJ, Land MF, King CA, Cronin TW (1991b) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). II Colour pigments in the eyes of stomatopod crustaceans: polychromatic vision by serial and lateral filtering. Phil Trans R Soc Lond 334: 57–84Google Scholar
  28. Menzel R (1979) Spectral sensitivity and colour vision in invertebrates. In: Autrum H (ed) Handbook of Sensory Physiology, VII/6A. Springer, Berlin Heidelberg New York, pp 503–580Google Scholar
  29. MenzelR, Backhaus W (1991) Colour vision in insects. In: Cronly-Dillon JR, Gregory RL (eds) Evolution of the eye and visual system. Vision and visual dysfunction, vol 2. Macmillan, pp 262–293Google Scholar
  30. Nässel DR (1976) The retina and retinal projection on the lamina ganglionaris of the crayfish Pacifastacus leniusculus (Dana). J Comp Neurol 167: 341–360Google Scholar
  31. Neumeyer C (1991) Evolution of colour vision. In: Cronly-Dillon JR, Gregory RL (eds) Evolution of the eye and visual system. Vision and visual dysfunction, vol 2. Macmillan, pp 284–305Google Scholar
  32. Sabra R, Glantz RM (1985) Polarisation sensitivity of crayfish photoreceptors is correlated with their termination sites in the lamina ganglionaris. J Comp Physiol A 156: 315–318Google Scholar
  33. Scherer C, Kolb G (1987a) Behavioural experiments on the visual processing of colour stimuli in Pieris brassicae L. (Lepidoptera). J Comp Physiol A 160: 645–656Google Scholar
  34. Scherer C, Kolb G (1987b) The influence of colour stimuli on visually controlled behaviour in Aglais urticae L. and Pararge aegeria L. (Lepidoptera). J Comp Physiol A 161: 891–898Google Scholar
  35. Smith FE, Baylor ER (1953) Colour responses in the Cladocera and their ecological significance. Am Nat 87: 49–55Google Scholar
  36. Smith KC, Macagno ER (1990) UV photoreceptors in the compound eye of Daphnia mayna (Crustacea, Branchiopoda). A fourth spectral class in single ommatidia. J Comp Physiol A 166: 597–606Google Scholar
  37. Stearns SC (1975) Light responses of Daphnia pulex. Limnol Oceanogr 20: 564–570Google Scholar
  38. Stowe S (1977) The retina-lamina projection in the crab Leptograpsus variegatus. Cell Tissue Res 185: 515–525Google Scholar
  39. Stowe S (1980) Spectral sensitivity and retinal pigment movement in the crab Leptoyrapsus variegatus (Fabricus). J Exp Biol 87: 73–98Google Scholar
  40. Strausfeld NJ, Nässel DR (1981) Neuroarchitecture of brain regions that subserve compound eyes of crustaceans and insects. In: Autrum H (ed) Handbook of sensory physiology, VII/6A. Springer, Berlin Heidelberg New York, pp 1–132Google Scholar
  41. Thompson E, Palacios A, Varela FJ (1992) Ways of colouring: Comparative colour vision as a case study for cognitive science. Behav Brain Sci 15: 1–74Google Scholar
  42. Troje N (1993) Spectral categories in the learning behaviour of blowflies. Z Naturforsch 48c: 96–104Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • N. J. Marshall
    • 1
  • J. P. Jones
    • 1
  • T. W. Cronin
    • 2
  1. 1.Sussex Centre for Neuroscience, University of SussexBrightonUK
  2. 2.Department of Biological SciencesUMBC CatonsvilleBaltimoreUSA

Personalised recommendations