Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

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

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 to check access.

Notes

  1. 1.

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

References

  1. 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

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

  3. 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

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

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

  6. 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

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

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

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

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

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

  12. 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

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

  14. 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

  15. 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

  16. 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

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

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

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

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

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

  22. 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

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

  24. 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

  25. 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

  26. 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

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

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

  29. 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

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

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

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

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

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

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

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

  37. 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

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

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

  40. 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

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

  42. 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

  43. 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

  44. 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

  45. 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

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

  47. 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

  48. 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

Download references

Author information

Correspondence to Dr. John K. Douglass.

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

Key words

  • Adaptation, light/dark
  • Compound eye
  • Development, ontogenetic
  • Pigment migration, visual system
  • Palaemonetes pugio (Crustacea)