Long-Wavelength Reflecting Filters Found in the Larval Retinas of One Mantis Shrimp Family (Nannosquillidae)

Kathryn Feller, David Wilby, Gianni Jacucci, Silvia Vignolini, Judith Mantell, Trevor J. Wardill, Thomas W. Cronin, Nicholas W. Roberts

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

Both vertebrates and invertebrates commonly exploit photonic structures adjacent to their photoreceptors for visual benefits. For example, use of a reflecting structure (tapetum) behind the retina increases photon capture, enhancing vision in dim light [1–5]. Colored filters positioned lateral or distal to a photoreceptive unit may also be used to tune spectral sensitivity by selective transmission of wavelengths not absorbed or scattered by the filters [6–8]. Here we describe a new category of biological optical filter that acts simultaneously as both a transmissive spectral filter and narrowband reflector. Discovered in the larval eyes of only one family of mantis shrimp (stomatopod) crustaceans (Nannosquillidae), each crystalline structure bisects the photoreceptive rhabdom into two tiers and contains an ordered array of membrane-bound vesicles with sub-wavelength diameters of 153 ± 5 nm. Axial illumination of the intrarhabdomal structural reflector (ISR) in vivo produces a narrow band of yellow reflectance (mean peak reflectivity, 572 ± 18 nm). The ISR is similar to several synthetic devices, such as bandgap filters, laser mirrors, and (in particular) fiber Bragg gratings used in optical sensors for a wide range of industries. To our knowledge, the stomatopod larval ISR is the first example of a naturally occurring analog to these human-made devices. Considering what is known about these animals’ visual ecology, we propose that these reflecting filters may help improve the detection of pelagic bioluminescence in shallow water at night. Video Abstract: Feller et al. report how one family of mantis shrimp larvae uses visual filtering structures to selectively reflect and transmit light within photoreceptors. These reflective filters likely enhance bioluminescence detection underwater at night and are similar to human-made optical devices such as fiber Bragg gratings or band gap filters.

Original languageEnglish (US)
Pages (from-to)3101-3108.e4
JournalCurrent Biology
Volume29
Issue number18
DOIs
StatePublished - Sep 23 2019

Bibliographical note

Funding Information:
We would like to thank the following people for help with this work. Animal collection and identification: Megan L. Porter, Roy L. Caldwell, Elliott P. Steele, Sitara Palecanda, Jenny Gumm, Lindsey DeMelo, the Marine Resources Center at the Marine Biological Laboratory, and the Australian Museum Lizard Island Research Station, run by Lyle Vale and Anne Hoggart. Spectral measurements and analysis: Tom Jordan, Justin Marshall, John Cataldi, Sonke Johnsen, and Simon Lauchlan. Manuscript feedback: Paloma Gonzalez-Bellido, Alice Chiou, Camilla Sharkey, Rachael Feord, and Jenny Gumm. This work was supported by the US Air Force Office of Scientific Research (FA8655-12-2112 and FA9550-12-1-0321), a travel grant from the Australian Microscopy and Microanalysis Research Facility Travel and Access Program (2010), and the Company of Biologists Travel Fellowship (2018). K.D.F. made the initial discovery, performed experiments, and coordinated all aspects of the project. K.D.F. T.W.C. and N.W.R. designed experiments, analyzed the data, and wrote and edited the manuscript. TEM was performed by K.D.F. and J.M. Photonic modeling was performed by G.J. and S.V. Visual modeling was performed by D.W. Two-photon microscopy tissue preparation was performed by K.D.F. with imaging by T.J.W. Figures created by K.D.F. with additions by D.W. and G.J. and revisions by co-authors. The authors declare no competing interests.

Funding Information:
We would like to thank the following people for help with this work. Animal collection and identification: Megan L. Porter, Roy L. Caldwell, Elliott P. Steele, Sitara Palecanda, Jenny Gumm, Lindsey DeMelo, the Marine Resources Center at the Marine Biological Laboratory, and the Australian Museum Lizard Island Research Station, run by Lyle Vale and Anne Hoggart. Spectral measurements and analysis: Tom Jordan, Justin Marshall, John Cataldi, Sonke Johnsen, and Simon Lauchlan. Manuscript feedback: Paloma Gonzalez-Bellido, Alice Chiou, Camilla Sharkey, Rachael Feord, and Jenny Gumm. This work was supported by the US Air Force Office of Scientific Research ( FA8655-12-2112 and FA9550-12-1-0321 ), a travel grant from the Australian Microscopy and Microanalysis Research Facility Travel and Access Program ( 2010 ), and the Company of Biologists Travel Fellowship (2018).

Publisher Copyright:
© 2019 Elsevier Ltd

Keywords

  • bioluminescence
  • compound eye
  • crustacean
  • crystal
  • larvae
  • mantis shrimp
  • photonic structure
  • stomatopod
  • vision

PubMed: MeSH publication types

  • Journal Article

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