Photon hunting in the twilight zone: visual features of mesopelagic bioluminescent sharks.

The mesopelagic zone is a visual scene continuum in which organisms have developed various strategies to optimize photon capture. Here, we used light microscopy, stereology-assisted retinal topographic mapping, spectrophotometry and microspectrophotometry to investigate the visual ecology of deep-se...

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Autores principales: Julien M Claes, Julian C Partridge, Nathan S Hart, Eduardo Garza-Gisholt, Hsuan-Ching Ho, Jérôme Mallefet, Shaun P Collin
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Publicado: Public Library of Science (PLoS) 2014
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Acceso en línea:https://doaj.org/article/95e5873f31324a9a948006a74dde3bf3
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spelling oai:doaj.org-article:95e5873f31324a9a948006a74dde3bf32021-11-25T06:05:47ZPhoton hunting in the twilight zone: visual features of mesopelagic bioluminescent sharks.1932-620310.1371/journal.pone.0104213https://doaj.org/article/95e5873f31324a9a948006a74dde3bf32014-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/25099504/?tool=EBIhttps://doaj.org/toc/1932-6203The mesopelagic zone is a visual scene continuum in which organisms have developed various strategies to optimize photon capture. Here, we used light microscopy, stereology-assisted retinal topographic mapping, spectrophotometry and microspectrophotometry to investigate the visual ecology of deep-sea bioluminescent sharks [four etmopterid species (Etmopterus lucifer, E. splendidus, E. spinax and Trigonognathus kabeyai) and one dalatiid species (Squaliolus aliae)]. We highlighted a novel structure, a translucent area present in the upper eye orbit of Etmopteridae, which might be part of a reference system for counterillumination adjustment or acts as a spectral filter for camouflage breaking, as well as several ocular specialisations such as aphakic gaps and semicircular tapeta previously unknown in elasmobranchs. All species showed pure rod hexagonal mosaics with a high topographic diversity. Retinal specialisations, formed by shallow cell density gradients, may aid in prey detection and reflect lifestyle differences; pelagic species display areae centrales while benthopelagic and benthic species display wide and narrow horizontal streaks, respectively. One species (E. lucifer) displays two areae within its horizontal streak that likely allows detection of conspecifics' elongated bioluminescent flank markings. Ganglion cell topography reveals less variation with all species showing a temporal area for acute frontal binocular vision. This area is dorsally extended in T. kabeyai, allowing this species to adjust the strike of its peculiar jaws in the ventro-frontal visual field. Etmopterus lucifer showed an additional nasal area matching a high rod density area. Peak spectral sensitivities of the rod visual pigments (λmax) fall within the range 484-491 nm, allowing these sharks to detect a high proportion of photons present in their habitat. Comparisons with previously published data reveal ocular differences between bioluminescent and non-bioluminescent deep-sea sharks. In particular, bioluminescent sharks possess higher rod densities, which might provide them with improved temporal resolution particularly useful for bioluminescent communication during social interactions.Julien M ClaesJulian C PartridgeNathan S HartEduardo Garza-GisholtHsuan-Ching HoJérôme MallefetShaun P CollinPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 9, Iss 8, p e104213 (2014)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Julien M Claes
Julian C Partridge
Nathan S Hart
Eduardo Garza-Gisholt
Hsuan-Ching Ho
Jérôme Mallefet
Shaun P Collin
Photon hunting in the twilight zone: visual features of mesopelagic bioluminescent sharks.
description The mesopelagic zone is a visual scene continuum in which organisms have developed various strategies to optimize photon capture. Here, we used light microscopy, stereology-assisted retinal topographic mapping, spectrophotometry and microspectrophotometry to investigate the visual ecology of deep-sea bioluminescent sharks [four etmopterid species (Etmopterus lucifer, E. splendidus, E. spinax and Trigonognathus kabeyai) and one dalatiid species (Squaliolus aliae)]. We highlighted a novel structure, a translucent area present in the upper eye orbit of Etmopteridae, which might be part of a reference system for counterillumination adjustment or acts as a spectral filter for camouflage breaking, as well as several ocular specialisations such as aphakic gaps and semicircular tapeta previously unknown in elasmobranchs. All species showed pure rod hexagonal mosaics with a high topographic diversity. Retinal specialisations, formed by shallow cell density gradients, may aid in prey detection and reflect lifestyle differences; pelagic species display areae centrales while benthopelagic and benthic species display wide and narrow horizontal streaks, respectively. One species (E. lucifer) displays two areae within its horizontal streak that likely allows detection of conspecifics' elongated bioluminescent flank markings. Ganglion cell topography reveals less variation with all species showing a temporal area for acute frontal binocular vision. This area is dorsally extended in T. kabeyai, allowing this species to adjust the strike of its peculiar jaws in the ventro-frontal visual field. Etmopterus lucifer showed an additional nasal area matching a high rod density area. Peak spectral sensitivities of the rod visual pigments (λmax) fall within the range 484-491 nm, allowing these sharks to detect a high proportion of photons present in their habitat. Comparisons with previously published data reveal ocular differences between bioluminescent and non-bioluminescent deep-sea sharks. In particular, bioluminescent sharks possess higher rod densities, which might provide them with improved temporal resolution particularly useful for bioluminescent communication during social interactions.
format article
author Julien M Claes
Julian C Partridge
Nathan S Hart
Eduardo Garza-Gisholt
Hsuan-Ching Ho
Jérôme Mallefet
Shaun P Collin
author_facet Julien M Claes
Julian C Partridge
Nathan S Hart
Eduardo Garza-Gisholt
Hsuan-Ching Ho
Jérôme Mallefet
Shaun P Collin
author_sort Julien M Claes
title Photon hunting in the twilight zone: visual features of mesopelagic bioluminescent sharks.
title_short Photon hunting in the twilight zone: visual features of mesopelagic bioluminescent sharks.
title_full Photon hunting in the twilight zone: visual features of mesopelagic bioluminescent sharks.
title_fullStr Photon hunting in the twilight zone: visual features of mesopelagic bioluminescent sharks.
title_full_unstemmed Photon hunting in the twilight zone: visual features of mesopelagic bioluminescent sharks.
title_sort photon hunting in the twilight zone: visual features of mesopelagic bioluminescent sharks.
publisher Public Library of Science (PLoS)
publishDate 2014
url https://doaj.org/article/95e5873f31324a9a948006a74dde3bf3
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