Skip to main content
SpringerLink
Log in

Multiple spectral classes of photoreceptors in the retinas of gonodactyloid stomatopod crustaceans

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

  1. 1.

    We examined the compound eyes of 2 species of gonodactyloid stomatopods, Gonodactylus oerstedii and Pseudosquilla ciliata, using end-on microspectrophotometry of frozen sections of dark-adapted retinas.

  2. 2.

    The cornea and crystalline cones of both species were virtually transparent from 350 to 700 nm. Primary screening pigment granules in the retinular cells had the broad absorption spectra typical of ommochromes. Colored vesicles, of unknown function, also were found in the cytoplasm of the retinular cells. The intrarhabdomal filters appeared to act as long-pass spectral filters, and had maximum optical densities in situ of 0.94 to 11.1.

  3. 3.

    A variety of visual pigments were found in both species, each in a specific retinal region. Their maximum absorption peaked at wavelengths from 400 nm to well beyond 530 nm.

  4. 4.

    Spectral sensitivity functions of all retinal regions were estimated. In both species, each of the 4 most dorsal ommatidial rows of the central band had a pair of narrow spectral sensitivitity curves, usually separated by 50 to 75 nm. These 4 pairs covered the spectrum from below 400 to beyond 650 nm. The other 2 rows of the central band had identical, broad sensitivity functions. Spectral sensitivities of all peripheral ommatidia in each species were identical, but different from any region of the central band.

  5. 5.

    These stomatopod species have retained the typical crustacean layered rhabdoms in the peripheral retina and the 2 most ventral rows of the central band, but have converted the photoreceptors of the 4 dorsal rows of the central band into as many as 8 narrowly tuned spectral classes. This design could serve a high-quality hue discrimination system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arikawa K, Kawamata K, Suzuki T, Eguchi E (1987a) Daily changes of structure, function, and rhodopsin content in the compound eye of the crab Hemigrapsus sanguineus. J Comp Physiol A 161:161–174

    Google Scholar 

  • Arikawa K, Inokuma K, Eguchi E (1987b) Pentachromatic visual system in a butterfly. Naturwissenschaften 74:297–298

    Google Scholar 

  • Arnold K, Neumeyer C (1987) Wavelength discrimination in the turtle Pseudemys elegans. Vision Res 27:1501–1511

    Google Scholar 

  • Barlow HB (1982) What causes trichromacy? A theoretical analysis using comb-filtered spectra. Vision Res 22:635–643

    Google Scholar 

  • Bernard GD (1987) Spectral characterization of butterfly L-receptors using extended Dartnall/MacNichol template functions. J Opt Soc Am A4:P123

    Google Scholar 

  • Bowmaker JK (1983) Trichromatic colour vision: why only three receptor channels? TINS 6:41–43

    Google Scholar 

  • Bowmaker JK, Dartnall HJA, Herring PJ (1988) Longwave-sensitive visual pigments in some deep-sea fishes: segregation of ‘paired’ rhodopsins and porphyropsins. J Comp Physiol A 163:685–698

    Google Scholar 

  • Bridges CDB (1972) The rhodopsin-porphyropsin visual system. In: Dartnall HJA (ed) Photochemistry of vision (Handbook of sensory physiology, vol VII/1). Springer, Berlin Heidelberg New York, pp 417–480

    Google Scholar 

  • Bruno MS, Goldsmith TH (1974) Rhodopsin of the blue crab Callinectes sapidus: Evidence for absorption differences in vitro and in vivo. Vision Res 14:653–658

    Google Scholar 

  • Bruno MS, Mote MI, Goldsmith TH (1973) Spectral absorption and sensitivity measurements in single ommatidia of the green crab, Carcinus. J Comp Physiol 82:151–163

    Google Scholar 

  • Caldwell RL (1979) Cavity occupation and defensive behaviour in the stomatopod Gonodactylus festae: Evidence for chemically mediated individual recognition. Anim Behav 27:194–201

    Google Scholar 

  • Caldwell RL (1985) A test of individual recognition in the stomatopod Gonodactylus festae. Anim Behav 33:101–106

    Google Scholar 

  • Caldwell RL, Dingle H (1975) Ecology and evolution of agonistic behavior in stomatopods. Naturwissenschaften 62:214–222

    Google Scholar 

  • Carlson SD, Philipson B (1972) Microspectrophotometry of the dioptric apparatus and compound rhabdom of the moth (Manduca sexta) eye. J Insect Physiol 18:1721–1731

    Google Scholar 

  • Cronin TW (1985) The visual pigment of a stomatopod crustacean, Squilla empusa. J Comp Physiol A 156:679–687

    Google Scholar 

  • Cronin TW (1986) Optical design and evolutionary adaptation in crustacean compound eyes. J Crust Biol 6:1–23

    Google Scholar 

  • Cronin TW (1989) Application of intracellular optical techniques to the study of stomatopod crustacean vision. J Comp Physiol A 164:737–749

    Google Scholar 

  • Cronin TW, Forward RB Jr (1988) The visual pigments of crabs I. Spectral properties. J Comp Physiol A 162:463–478

    Google Scholar 

  • Cronin TW, Marshall NJ (1989) A retina with at least ten spectral types of photoreceptors in a mantis shrimp. Nature 339:137–140

    Google Scholar 

  • Cronin TW, Nair JN, Doyle RD, Caldwell RL (1988) Ocular tracking of rapidly moving visual targets by stomatopod Crustacea. J Exp Biol 138:155–179

    Google Scholar 

  • Cummins DR, Goldsmith TH (1981) Cellular identification of the violet receptor in the crayfish eye. J Comp Physiol 142:199–202

    Google Scholar 

  • Dartnall HJA, Lythgoe JN (1965) The spectral clustering of visual pigments. Vision Res 5:81–100

    Google Scholar 

  • Demoll R (1909) Über die Augen und die Augenstiel-Reflexe von Squilla mantis. Zool Jahrb, Abt Anat Ontog Tiere 27:171–212

    Google Scholar 

  • Dingle H (1964) A colour polymorphism in Gonodactylus oerstedii Hansen, 1895 (Stomatopoda). Crustaceana 7:236–240

    Google Scholar 

  • Dominguez JH, Reaka M (1988) Temporal activity patterns in reef-dwelling stomatopods: a test of alternative hypotheses. J Exp Mar Biol Ecol 117:47–69

    Google Scholar 

  • Exner S (1891) Die Physiologie der facettirten Augen von Krebsen und Insecten. Deuticke, Leipzig Wien

    Google Scholar 

  • Goldsmith TH (1978a) The effects of screening pigments on the spectral sensitivity of some Crustacea with scotopic (superposition) eyes. Vision Res 18:475–482

    Google Scholar 

  • Goldsmith TH (1978b) The spectral absorption of crayfish rhabdoms: pigment, photoproduct and pH sensitivity. Vision Res 18:463–473

    Google Scholar 

  • Goldsmith TH, Collins JS, Licht S (1984) The cone oil droplets of avian retinas. Vision Res 24:1661–1671

    Google Scholar 

  • Goldsmith TH, Fernández HR (1968) Comparative studies of crustacean spectral sensitivity. Z Vergl Physiol 60:156–175

    Google Scholar 

  • Govardovskii VI (1983) On the role of oil drops in colour vision. Vision Res 23:1739–1740

    Google Scholar 

  • Hardie R (1985) Functional organization of the fly retina. In: Ottoson D (ed) Progress in sensory physiology 5. Springer, Berlin Heidelberg New York Tokyo, pp 1–79

    Google Scholar 

  • Hardie RC (1988) The eye of the mantid shrimp. Nature 333:499–500

    Google Scholar 

  • Hárosi FI (1985) Ultraviolet- and violet-absorbing vertebrate visual pigments: Dichoic and bleaching properties. In: Fein A, Levine JS (eds) The visual system. Alan R Liss, New York, pp 41–55

    Google Scholar 

  • Hárosi FI, Hashimoto Y (1983) Ultraviolet visual pigment in a vertebrate: A tetrachromatic cone system in the dace. Science 222:1021–1023

    Google Scholar 

  • Hays D, Goldsmith TH (1969) Microspectrophotometry of the visual pigment of the spider crab Libinia emarginata. Z Vergl Physiol 65:218–232

    Google Scholar 

  • Killer-Adams P, Widder EA, Case JF (1988) The visual pigments of four deep-sea crustacean species. J Comp Physiol A 163:63–72

    Google Scholar 

  • Horridge GE (1978) The separation of visual axes in apposition compound eyes. Phil Trans R Soc Lond B285:1–59

    Google Scholar 

  • Hyatt GW (1975) Physiological and behavioral evidence for color discrimination by fiddler crabs (Brachyura, Ocypodidae, genus Uca) In: Vernberg FJ (ed) Physiological ecology of estuarine organisms. University of South Carolina Press, Columbia SC, pp 333–365

    Google Scholar 

  • Labhart T (1988) Polarization-opponent interneurons in the insect visual system. Nature 331:435–437

    Google Scholar 

  • Larrivee D, Goldsmith TH (1982) Spectral dimorphism of crayfish visual pigment in solution. Vision Res 22:727–737

    Google Scholar 

  • Leggett LMW (1976) Polarised light-sensitive interneurones in a swimming crab. Nature 262:709–711

    Google Scholar 

  • Lipetz LE, Cronin TW (1988) Application of an invariant spectral form to the visual pigments of crustaceans: implications regarding the binding of the chromophore. Vision Res 28:1083–1093

    Google Scholar 

  • Ludolph C, Pagnanelli D, Mote MI (1973) Neural control of migration of proximal screening pigment by retinular cells of the swimming crab Callinectes sapidus. Biol Bull 145:159–170

    Google Scholar 

  • MacNichol EF Jr (1986) A unifying presentation of photopigment spectra. Vision Res 26:1543–1556

    Google Scholar 

  • Manning RB, Schiff H, Abbott BC (1984) Eye structure and the classification of stomatopod Crustacea. Zool Scripta 13:41–44

    Google Scholar 

  • Mansfield RJW (1985) Primate photopigments and cone mechanisms. In: Fein A, Levine JS (eds) The visual system. Alan R. Liss, New York, pp 566–603

    Google Scholar 

  • Marshall NJ (1988) A unique colour and polarisation vision system in mantis shrimps. Nature 333:557–560

    Google Scholar 

  • Martin FG, Mote MI (1982) Color receptors in marine crustaceans: a second spectral class of retinular cell in the compound eyes of Callinectes and Carcinus. J Comp Physiol 145:549–554

    Google Scholar 

  • McFarland WN, Munz FW (1975) The photic environment of clear tropical seas during the day. Vision Res 15:1063–1070

    Google Scholar 

  • Ohtsuka T (1985a) Relation of spectral types to oil droplets in cones of turtle retina. Science 229:874–877

    Google Scholar 

  • Ohtsuka T (1985b) Spectral sensitivities of seven morphological types of photoreceptors in the retina of the turtle, Geoclemys reevesii. J Comp Neurol 237:145–154

    Google Scholar 

  • Sabra R, Glantz RM (1985) Polarization sensitivity of crayfish photoreceptors is correlated with their termination sites in the lamina ganglionaris. J Comp Physiol A 156:315–318

    Google Scholar 

  • Schiff H, Abbott BC (1987) Shape, structure, and optics of the eyes of two lysiosquilloid stomatopods. J Crust Biol 7:158–170

    Google Scholar 

  • Schiff H, Candone P (1986) Superposition and scattering of visual fields in a compound, double eye — II. Stimulation sequences for different distances in a stomatopod from a bright habitat. Comp Biochem Physiol 83A:445–455

    Google Scholar 

  • Schiff H, Manning RB, Abbott BC (1986) Structure and optics of ommatidia from eyes of stomatopod crustaceans from different luminous habitats. Biol Bull 170:461–480

    Google Scholar 

  • Schönenberger N (1977) The fine structure of the compound eye of Squilla mantis (Crustacea, Stomatopoda). Cell Tissue Res 176:205–233

    Google Scholar 

  • Shaw SR, Stowe S (1982) Photoreception. In: Sandeman DC, Atwood HL (eds) The biology of Crustacea, vol 3. Academic Press, New York, pp 291–367

    Google Scholar 

  • Sokal RR, Rohlf FJ (1969) Biometry. WH Freeman, San Francisco, p 776

    Google Scholar 

  • Snyder AW, Menzel R, Laughlin SB (1973) Structure and function of the fused rhabdom. J Comp Physiol 87:99–135

    Google Scholar 

  • Stavenga DG, Schwemer J (1984) Visual pigments of invertebrates. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, Oxford New York, pp 11–61

    Google Scholar 

  • Stowe S (1980) Spectral sensitivity and retinal pigment movement in the crab Leptograpsus variegatus (Fabricius). J Exp Biol 87:73–98

    Google Scholar 

  • Trevino DL, Larimer JL (1969) The spectral sensitivity and flicker response of the eye of the stomatopod Squilla empusa Say. Comp Biochem Physiol 31:987–991

    Google Scholar 

  • Waterman TH (1981) Polarization sensitivity. In: Autrum H (ed) Invertebrate visual centers and behavior I. (Handbook of sensory physiology, vol VII/6B). Springer, Berlin Heidelberg New York, pp 281–470

    Google Scholar 

  • Waterman TH, Fernández HR, Goldsmith TH (1969) Dichroism of photosensitive pigment in rhabdoms of the crayfish Orconectes. J Gen Physiol 54:415–432

    Google Scholar 

  • Yamaguchi T, Katagiri Y, Ochi K (1976) Polarized light responses from retinula cells and sustaining fibers of the mantis shrimp. Biol J Okayama Univ 17:61–66

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Maryland Baltimore County, 21228, Catonsville, Maryland, USA

    Thomas W. Cronin

  2. School of Biological Sciences, University of Sussex, BN1 9QG, Falmer, Brighton, England

    N. Justin Marshall

Authors
  1. Thomas W. Cronin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Justin Marshall
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cronin, T.W., Marshall, N.J. Multiple spectral classes of photoreceptors in the retinas of gonodactyloid stomatopod crustaceans. J Comp Physiol A 166, 261–275 (1989). https://doi.org/10.1007/BF00193471

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00193471

Key words

Search

Navigation