Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Calcitic microlenses as part of the photoreceptor system in brittlestars

Abstract

Photosensitivity in most echinoderms has been attributed to ‘diffuse’ dermal receptors1,2,3. Here we report that certain single calcite crystals used by brittlestars for skeletal construction4,5 are also a component of specialized photosensory organs, conceivably with the function of a compound eye. The analysis of arm ossicles in Ophiocoma6 showed that in light-sensitive species, the periphery of the labyrinthic calcitic skeleton extends into a regular array of spherical microstructures that have a characteristic double-lens design. These structures are absent in light-indifferent species. Photolithographic experiments in which a photoresist film was illuminated through the lens array showed selective exposure of the photoresist under the lens centres. These results provide experimental evidence that the microlenses are optical elements that guide and focus the light inside the tissue. The estimated focal distance (4–7 µm below the lenses) coincides with the location of nerve bundles—the presumed primary photoreceptors. The lens array is designed to minimize spherical aberration and birefringence and to detect light from a particular direction. The optical performance is further optimized by phototropic chromatophores that regulate the dose of illumination reaching the receptors. These structures represent an example of a multifunctional biomaterial that fulfills both mechanical and optical functions.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Appearance and skeletal structure of ophiocomid brittlestars.
Figure 2: Lithographic experiment showing the focusing ability of the lens layer.
Figure 3: Analysis of the focusing effect of the lens layer.
Figure 4: Transmission electron micrograph of the decalcified section of the DAP of O. wendtii.

References

  1. Hyman, L. H. The Invertebrates Vol. 4 (McGraw-Hill, New York, 1955).

    Google Scholar 

  2. Millott, N. The photosensitivity of echinoids. Adv. Mar. Biol. 13, 1–52 (1975).

    Google Scholar 

  3. Yoshida, M., Takasu, N. & Tamotsu, S. in Photoreception and Vision in Invertebrates; (ed. Ali, M. A.) 743–771 (Plenum, New York, 1984).

    Book  Google Scholar 

  4. Lowenstam, H. A. & Weiner, S. On Biomineralization 123–134 (Oxford Univ. Press, Oxford, 1989).

    Google Scholar 

  5. Wainwright, S. A., Biggs, W. D., Currey, J. D. & Gosline, J. M. Mechanical Design in Organisms (John Wiley, New York, 1976).

    Google Scholar 

  6. Hendler, G. & Byrne, M. Fine structure of the dorsal arm plate of Ophiocoma wendti (Echinodermata, Ophiuroidea). Zoomorphology 107, 261–272 (1987).

    Article  Google Scholar 

  7. Hendler, G. Brittlestar color-change and phototaxis (Echinodermata: Ophiuroidea: Ophiocomidae). Mar. Ecol. 5, 379–401 (1984).

    Article  ADS  Google Scholar 

  8. Cowles, R. P. Stimuli produced by light and by contact with solid walls as factors in the behavior of ophiuroids. J. Exp. Zool. 9, 387–416 (1910).

    Article  Google Scholar 

  9. Donnay, G. & Pawson, D. L. X-ray diffraction studies of echinoderm plates. Science 166, 1147–1150 (1969).

    Article  ADS  CAS  Google Scholar 

  10. Ameye, L., Hermann, R., Wilt, F. & Dubois, P. Ultrastructural localization of proteins involved in sea urchin biomineralization. J. Histochem. Cytochem. 47, 1189–1200 (1999).

    Article  CAS  Google Scholar 

  11. Clarkson, E. N. K. & Levi-Setti, R. Trilobite eyes and the optics of Des Cartes and Huygens. Nature 254, 663–667 (1975).

    Article  ADS  CAS  Google Scholar 

  12. Gal, J., Horvath, G., Clarkson, E. N. K. & Haiman, O. Image formation by bifocal lenses in a trilobite eye? Vision Res. 40, 843–853 (2000).

    Article  CAS  Google Scholar 

  13. Towe, K. M. Trilobite eyes: calcified lenses in vivo. Science 179, 1007–1010 (1973).

    Article  ADS  CAS  Google Scholar 

  14. Döderlein, L. Ueber ‘Krystallkörper’ bei Seesternen. Denkschr. Med. Nat. Ges. Jena 8, 491–494 (1898).

    Google Scholar 

  15. Smith, A. B. in Special Papers in Palaeontology 25, 1–81 (Palaeontology Association, London, 1980).

    Google Scholar 

  16. Xia, Y. N. & Whitesides, G. M. Soft lithography. Annu. Rev. Mater. Sci. 28, 153–184 (1998).

    Article  ADS  CAS  Google Scholar 

  17. Aizenberg, J., Rogers, J. A., Paul, K. E. & Whitesides, G. M. Imaging the irradiance distribution in the optical near field. Appl. Phys. Lett. 71, 3773–3775 (1997).

    Article  ADS  CAS  Google Scholar 

  18. Flint, H. T. Geometrical Optics (Methuen, London, 1936).

    MATH  Google Scholar 

  19. Cobb, J. L. S. & Moore, A. Comparative studies on receptor structure in the brittlestar Ophiura ophiura. J. Neurocytol. 15, 97–108 (1986).

    Article  CAS  Google Scholar 

  20. Johnsen, S. Identification and localization of a possible rhodopsin in the echinoderms Asterias forbesi (Asteroidea) and Ophioderma brevispinum (Ophiuroidea). Biol. Bull. 193, 97–105 (1997).

    Article  CAS  Google Scholar 

  21. Cobb, J. L. S. & Hendler, G. Neurophysiological characterization of the photoreceptor system in brittlestars. Comp. Biochem. Physiol. 97A, 329–333 (1990).

    Article  CAS  Google Scholar 

  22. Stubbs, T. R. in Echinoderms (ed. Lawrence, J. M.) 403–408 (Proc. Int. Echinoderms Conf., Tampa Bay, 1982).

    Google Scholar 

  23. Land, M. F. in Comparative Physiology and Evolution in Invertebrates B: Invertebrate Visual Centers and Behavior I (ed. Autrum, H.) 471–592 (Springer, Berlin, 1981).

    Book  Google Scholar 

  24. Mann, S. & Ozin, G. A. Synthesis of inorganic materials with complex form. Nature 382, 313–318 (1996).

    Article  ADS  CAS  Google Scholar 

  25. Belcher, A. M., Hansma, P. K., Stucky, G. D. & Morse, D. E. First steps in harnessing the potential of biomineralization. Acta Mater. 46, 733–736 (1998).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank P. Wiltzius and M. Megens for helpful discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joanna Aizenberg.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Aizenberg, J., Tkachenko, A., Weiner, S. et al. Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature 412, 819–822 (2001). https://doi.org/10.1038/35090573

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35090573

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing