Skip to main content
SpringerLink
Log in

The ontogeny of facultative superposition optics in a shrimp eye: hatching through metamorphosis

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Footnote 1Compound eyes of larval and first postlarval grass shrimp (Palaemonetes pugio Holthuis) were studied with light and electron microscopy following adaptation to darkness or bright light. Larvae have well-developed apposition eyes, including 3 main types of accessory screening and reflecting pigments and a fourth class of putatively reflective granules recently described in adult shrimps. Rhabdoms contain orthogonally layered microvilli, and by the last larval stage, 8 retinular cells. Ocular accessory pigments in both light- and dark-adapted larvae are distributed much like those of light-adapted adults, but the distal mass of reflecting pigment is concentrated dorsally in larvae and ventrally in adults. Since larvae swim upside-down, reflecting pigment is oriented downward in all developmental stages and may function for countershading. Light and dark adaptational migrations of all 3 major accessory pigments commence abruptly at metamorphosis to the first postlarva. Upon dark adaptation in postlarvae, superposition optics remain impossible because (1) distal screening pigment migrates only slightly, (2) no clear zone has developed, and (3) the crystalline cones remain circular in cross section. Nevertheless, a slight improvement in photon catch is expected due to extensive redistributions of reflecting pigment and retinular cell screening pigment granules.

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.

Institutional subscriptions

Similar content being viewed by others

Notes

  1. A preliminary report on this research has appeared in the form of an abstract (Douglass 1985)

References

  • Autrum H (1981) Light and dark adaptation in invertebrates. In: Autrum H (ed) Comparative physiology and evolution of vision in invertebrates. Invertebrate visual centers and behavior II. Handbook of sensory physiology, vol VII/6C. Springer, Berlin Heidelberg New York, pp 1–91

    Google Scholar 

  • Bagnara JT (1983) Developmental aspects of vertebrate chromatophores. Am Zool 23:465–478

    Google Scholar 

  • Ball EE, Kao LC, Stone RC, Land MF (1986) Eye structure and optics in the pelagic shrimp Acetes sibogae (Decapoda, Natantia, Sergestidae) in relation to light-dark adaptation and natural history. Philos Trans R Soc Lond [Biol] 313:251–270

    Google Scholar 

  • Bennitt R (1924) The migration of the retinal pigment in crustaceans. J Exp Zool 40:381–435

    Google Scholar 

  • Broad AC (1955) Reproduction, larval development and metamorphosis of some Natantia from Beaufort, North Carolina. Ph D Thesis, Duke University, Durham, NC

    Google Scholar 

  • Broad AC, Hubschman JH (1962) A comparison of larvae and larval development of species of Eastern U S Palaemonetes with special reference to the development of Palaemonetes intermedius Holthuis. Am Zool 2:394–395a

    Google Scholar 

  • Broch ES (1960) Endocrine control of chromatophores of the zoeae of the prawn, Palaemonetes vulgaris. Biol Bull (Woods Hole) 119:305–306a

    Google Scholar 

  • Congdon ED (1907) The effect of temperature on the migration of retinal pigment in decapod crustaceans. J Exp Zool 4:539–548

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Debaisieux P (1944) Les yeux de Crustacés. Structure, développement, réactions à l'éclairement. Cellule 50:9–122

    Google Scholar 

  • Doughtie DG, Rao KR (1984) Ultrastructure of the eyes of the grass shrimp, Palaemonetes pugio. General morphology, and light and dark adaptation at noon. Cell Tissue Res 238:271–288

    Google Scholar 

  • Douglass JK (1985) The ontogeny of ocular pigment migrations in grass shrimp, Palaemonetes pugio. Am Zool 25:211a

    Google Scholar 

  • Douglass JK (1986) The ontogeny of light and dark adaptation in the compound eyes of grass shrimp, Palaemonetes pugio. PhD Thesis, Duke University, Durham, NC

    Google Scholar 

  • Eloffson R (1969) The development of the compound eye of Penaeus duorarum (Crustacea, Decapoda) with remarks on the nervous system. Z Zellforsch Mikrosk Anat 97:323–350

    Google Scholar 

  • Fincham AA (1984) Ontogeny and optics of the eyes of the common prawn Palaemon (Palaemon) serratus (Pennant, 1777). Zool J Linn Soc 81:89–113

    Google Scholar 

  • Forward RB Jr, Douglass JK (1989) Crustacean larval visual sensitivity during diel vertical migration. Proc 21st Eur Marine Biol Symp (in press)

  • Hafner GS, Tokarski T, Hammond-Soltis G (1982) Development of the crayfish retina: A light and electron microscopic study. J Morphol 173:101–118

    Google Scholar 

  • Herrick FH (1891) Alpheus: A study in the development of crustaea. Memoirs Nat Acad Sci 5:370–461

    Google Scholar 

  • Hubschman JH (1963) Development and function of neurosecretory sites in the eyestalks of larval Palaemonetes (Decapoda: Natantia). Biol Bull (Woods Hole) 125:96–113

    Google Scholar 

  • Kirschfeld K, Franceschini N (1969) Ein Mechanismus zur Steuerung des Lichtflusses in den Rhabdomeren des Komplexauges von Musca. Kybernetik 6:13–22

    Google Scholar 

  • Kirschfeld K, Snyder AW (1975) Waveguide mode effects, birefringence and dichroism in fly photoreceptors. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin Heidelberg New York, pp 56–77

    Google Scholar 

  • Kleinholz LH (1961) Pigmentary effectors. In: Waterman TH (ed) The physiology of crustacea, vol II. Academic Press, New York, pp 133–169

    Google Scholar 

  • Land MF (1981a) Optics and vision in invertebrates. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6B. Springer, Berlin Heidelberg New York, pp 471–592

    Google Scholar 

  • Land MF (1981b) Optical mechanisms in the higher crustacea with a comment on their evolutionary origins. In: Laverack MS, Cosens DJ (eds) Sense organs. Blackie, Glasgow, pp 31–48

    Google Scholar 

  • Land MF (1984) Crustacea. In: Ali MA (ed) Photoreception and vision in invertebrates. NATO ASI Series, vol 74. Plenum Press, New York, pp 401–438

    Google Scholar 

  • Lythgoe JN (1979) The ecology of vision. Clarendon Press, Oxford, Oxford Univ Press, New York

    Google Scholar 

  • Meyer-Rochow VB (1975) Larval and adult eye of the western rock lobster (Panulirus longipes). Cell Tissue Res 162:439–457

    Google Scholar 

  • Meyer-Rochow VB, Tiang KM (1982) Comparison between temperature-induced changes and effects caused by dark/light adaptation in the eyes of two species of Antarctic crustaceans. Cell Tissue Res 221:625–632

    Google Scholar 

  • Munz FW, McFarland WN (1973) The significance of spectral position in the rhodopsins of tropical marine fishes. Vision Res 13:1829–1874

    Google Scholar 

  • Nilsson D-E (1983) Evolutionary links between apposition and superposition optics in crustacean eyes. Nature 302:818–821

    Google Scholar 

  • Nilsson D-E (1988) A new type of imaging optics in compound eyes. Nature 332:76–78

    Google Scholar 

  • Nilsson D-E, Nilsson HL (1983) Eye camouflage in the isopod crustacean Astacilla longicornis (Sowerby). J Exp Mar Biol Ecol 68:105–110

    Google Scholar 

  • Nilsson D-E, Land MF, Howard J (1988) Optics of the butterfly eye. J Comp Physiol [A] 162:341–366

    Google Scholar 

  • Parker GH (1890) The histology and development of the eye in the lobster. Bull Mus Comp Zool Harv Univ 20:1–60

    Google Scholar 

  • Parker GH (1891) The compound eyes in crustaceans. Bull Mus Comp Zool Harv Univ 21:45–140

    Google Scholar 

  • Parker GH (1897) Photomechanical changes in the retinal pigment cells of Palaemonetes, and their relation to the central nervous system. Bull Mus Comp Zool Harv Univ 30:273–300

    Google Scholar 

  • Parker GH (1932) The movement of the retinal pigment. Ergeb Biol 9:239–291

    Google Scholar 

  • Plate L (1924) Die Sinnesorgane der Tiere. In: Allgemeine Zoologie und Abstammungslehre, Teil II., pp 404–407

  • Rao KR (1985) Pigmentary effectors. In: Bliss DE, Mantel LH (eds) The biology of Crustacea, vol 9 : Integuments, pigments, and hormonal processes, pp 395–462

  • Sato T (1968) A modified method for lead staining of thin sections. J Electron Microsc (Tokyo) 17:158–159

    Google Scholar 

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

    Google Scholar 

  • Sollaud E (1923) Le développement larvaire des “Palaemoninae”. Bull Biol Fr Belg 57, Ch IV, La fin de la vie larvaire. La métamorphose, pp 597–603

  • Strausfeld NJ, Nassel DR (1981) Neuroarchitecture of brain regions that subserve the compound eyes of crustacea and insects. In: Autrum H (ed) Handbook of sensory physiology, vol. VII/ 6B. Springer, Berlin Heidelberg New York, pp 1–132

    Google Scholar 

  • Via SE, Forward RB Jr (1975) The ontogeny and spectral sensitivity of polarotaxis in larvae of the crab Rhithropanopeus harrisi (Gould). Biol Bull (Woods Hole) 149:251–266

    Google Scholar 

  • Walpole RE (1974) Introduction to statistics (2nd ed). Macmillan Publishing Co, New York

    Google Scholar 

  • Wilson JE, Forward RB Jr, Costlow JD (1985) Effects of embryonic exposure to sublethal concentrations of Dimilin on the photobehavior of grass shrimp larvae. In: Vernberg FJ, Thurberg FP, Calabrese A, Vernberg W (eds) Marine pollution and physiology: Recent advances. Univ of South Carolina Press, Columbia, SC, Belle W Baruch Library in Marine Science, No 13. pp 377–396

    Google Scholar 

  • Zyznar ES (1970) The eyes of white shrimp, Penaeus setiferus (Linnaeus), with a note on the rock shrimp, Sicyonia brevirostris Stimpson. Contrib Mar Sci 15:87–102

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Duke University Marine Laboratory, Beaufort, North Carolina, USA

    John K. Douglass & Richard B. Forward Jr.

  2. Department of Zoology, Duke University, Durham, North Carolina, USA

    John K. Douglass & Richard B. Forward Jr.

Authors
  1. John K. Douglass
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard B. Forward Jr.
    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

Douglass, J.K., Forward, R.B. The ontogeny of facultative superposition optics in a shrimp eye: hatching through metamorphosis. Cell Tissue Res. 258, 289–300 (1989). https://doi.org/10.1007/BF00239449

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00239449

Key words

Search

Navigation