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

PLoS One. 2014 Aug 6;9(8):e104213. doi: 10.1371/journal.pone.0104213. eCollection 2014.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Luminescence*
  • Pigmentation / physiology*
  • Retinal Rod Photoreceptor Cells / cytology
  • Retinal Rod Photoreceptor Cells / physiology*
  • Sharks / anatomy & histology
  • Sharks / physiology*

Grants and funding

Financial support (specimen collection, open access fee) was provided by the Fonds National de la Recherche Scientifique (FNRS, Belgium) (http://www.fnrs.be) through a Fonds de la Recherche Fondamentale Collective grant (FRFC – 2.4525.12) and travel grants to JMC (postdoctoral researcher at FNRS) and JM (research associate at FNRS). Part of the research (data collection and analysis) was supported by an Australian Research Council (http://www.arc.gov.au) grant (DP110103294) to SPC, NSH and others, the Western Australian State Government (http://wa.gov.au) to SPC, and the National Museum of Marine Biology and Aquarium (http://www.nmmba.gov.tw/english/index.aspx) to HCH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.