Biofluorescence in Catsharks (Scyliorhinidae): Fundamental Description and Relevance for Elasmobranch Visual Ecology

David F. Gruber; Ellis R. Loew; Dimitri D. Deheyn; Derya Akkaynak; Jean P. Gaffney; W. Leo Smith; Matthew P. Davis; Jennifer H. Stern; Vincent A. Pieribone; John S. Sparks

doi:10.1038/srep24751

Biofluorescence in Catsharks (Scyliorhinidae): Fundamental Description and Relevance for Elasmobranch Visual Ecology

David F. Gruber, Ellis R. Loew, Dimitri D. Deheyn, Derya Akkaynak, Jean P. Gaffney, W. Leo Smith, Matthew P. Davis, Jennifer H. Stern, Vincent A. Pieribone, John S. Sparks

Department of Marine Technologies

Research output: Contribution to journal › Article › peer-review

Abstract

Biofluorescence has recently been found to be widespread in marine fishes, including sharks. Catsharks, such as the Swell Shark (Cephaloscyllium ventriosum) from the eastern Pacific and the Chain Catshark (Scyliorhinus retifer) from the western Atlantic, are known to exhibit bright green fluorescence. We examined the spectral sensitivity and visual characteristics of these reclusive sharks, while also considering the fluorescent properties of their skin. Spectral absorbance of the photoreceptor cells in these sharks revealed the presence of a single visual pigment in each species. Cephaloscyllium ventriosum exhibited a maximum absorbance of 484 ± 3 nm and an absorbance range at half maximum (λ_1/2max) of 440-540 nm, whereas for S. retifer maximum absorbance was 488 ± 3 nm with the same absorbance range. Using the photoreceptor properties derived here, a "shark eye" camera was designed and developed that yielded contrast information on areas where fluorescence is anatomically distributed on the shark, as seen from other sharks' eyes of these two species. Phylogenetic investigations indicate that biofluorescence has evolved at least three times in cartilaginous fishes. The repeated evolution of biofluorescence in elasmobranchs, coupled with a visual adaptation to detect it; and evidence that biofluorescence creates greater luminosity contrast with the surrounding background, highlights the potential importance of biofluorescence in elasmobranch behavior and biology.

Original language	English
Article number	24751
Journal	Scientific Reports
Volume	6
DOIs	https://doi.org/10.1038/srep24751
State	Published - 25 Apr 2016

Bibliographical note

Funding Information:
The study was funded by Air Force Office of Scientific Research (AFOSR) grant #FA9550-14-1-0008 and #MURI BIOPAINTS FA9550-10-1-0555 to DDD for the hyperspectral imager, National Science Foundation grants DEB #1257555 to JSS, #1258141 to WLS and MPD, and MRI# 1040321 to DFG, National Geographic Society grants (W101-10 to D.F.G. and W114-12 to J.S.S.), and The Ray and Barbara Dalio Family Foundation Explore 21 expedition grant to JSS, DFG, and VAP. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank the John B. Pierce Laboratory Machine Shop for building underwater lights; the Maurice Hatter Foundation for post-doctoral fellowship support to DA; Rick Elkus, Patty Elkus, Kyle McBurnie, and Nicholas Lebeouf for assistance and support in filming C. ventriosum in Scripps Canyon; the BBC Natural History Unit and Christoph Pierre for assistance in Santa Barbara; Joe Yaiullo of the Long Island Aquarium, Todd Gardner of Suffolk County Community College, Donnie Harrington and Tracy Romano of Mystic Aquarium for assistance imaging S. retifer; and Fernando Nosratpour and Leslee Matsushige of the Birch Aquarium for assistance imaging C. ventriosum. We thank Biopixel for generously allowing use of their image of an orectolobid and Kathleen Smith for reading and commenting on the manuscript.

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General

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Cite this

@article{789b2e216e7e498184d7c6491ef80367,

title = "Biofluorescence in Catsharks (Scyliorhinidae): Fundamental Description and Relevance for Elasmobranch Visual Ecology",

abstract = "Biofluorescence has recently been found to be widespread in marine fishes, including sharks. Catsharks, such as the Swell Shark (Cephaloscyllium ventriosum) from the eastern Pacific and the Chain Catshark (Scyliorhinus retifer) from the western Atlantic, are known to exhibit bright green fluorescence. We examined the spectral sensitivity and visual characteristics of these reclusive sharks, while also considering the fluorescent properties of their skin. Spectral absorbance of the photoreceptor cells in these sharks revealed the presence of a single visual pigment in each species. Cephaloscyllium ventriosum exhibited a maximum absorbance of 484 ± 3 nm and an absorbance range at half maximum (λ1/2max) of 440-540 nm, whereas for S. retifer maximum absorbance was 488 ± 3 nm with the same absorbance range. Using the photoreceptor properties derived here, a {"}shark eye{"} camera was designed and developed that yielded contrast information on areas where fluorescence is anatomically distributed on the shark, as seen from other sharks' eyes of these two species. Phylogenetic investigations indicate that biofluorescence has evolved at least three times in cartilaginous fishes. The repeated evolution of biofluorescence in elasmobranchs, coupled with a visual adaptation to detect it; and evidence that biofluorescence creates greater luminosity contrast with the surrounding background, highlights the potential importance of biofluorescence in elasmobranch behavior and biology.",

author = "Gruber, {David F.} and Loew, {Ellis R.} and Deheyn, {Dimitri D.} and Derya Akkaynak and Gaffney, {Jean P.} and Smith, {W. Leo} and Davis, {Matthew P.} and Stern, {Jennifer H.} and Pieribone, {Vincent A.} and Sparks, {John S.}",

note = "Funding Information: The study was funded by Air Force Office of Scientific Research (AFOSR) grant #FA9550-14-1-0008 and #MURI BIOPAINTS FA9550-10-1-0555 to DDD for the hyperspectral imager, National Science Foundation grants DEB #1257555 to JSS, #1258141 to WLS and MPD, and MRI# 1040321 to DFG, National Geographic Society grants (W101-10 to D.F.G. and W114-12 to J.S.S.), and The Ray and Barbara Dalio Family Foundation Explore 21 expedition grant to JSS, DFG, and VAP. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank the John B. Pierce Laboratory Machine Shop for building underwater lights; the Maurice Hatter Foundation for post-doctoral fellowship support to DA; Rick Elkus, Patty Elkus, Kyle McBurnie, and Nicholas Lebeouf for assistance and support in filming C. ventriosum in Scripps Canyon; the BBC Natural History Unit and Christoph Pierre for assistance in Santa Barbara; Joe Yaiullo of the Long Island Aquarium, Todd Gardner of Suffolk County Community College, Donnie Harrington and Tracy Romano of Mystic Aquarium for assistance imaging S. retifer; and Fernando Nosratpour and Leslee Matsushige of the Birch Aquarium for assistance imaging C. ventriosum. We thank Biopixel for generously allowing use of their image of an orectolobid and Kathleen Smith for reading and commenting on the manuscript.",

year = "2016",

month = apr,

day = "25",

doi = "10.1038/srep24751",

language = "English",

volume = "6",

journal = "Scientific Reports",

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T2 - Fundamental Description and Relevance for Elasmobranch Visual Ecology

AU - Gruber, David F.

AU - Loew, Ellis R.

AU - Deheyn, Dimitri D.

AU - Akkaynak, Derya

AU - Gaffney, Jean P.

AU - Smith, W. Leo

AU - Davis, Matthew P.

AU - Stern, Jennifer H.

AU - Pieribone, Vincent A.

AU - Sparks, John S.

N1 - Funding Information: The study was funded by Air Force Office of Scientific Research (AFOSR) grant #FA9550-14-1-0008 and #MURI BIOPAINTS FA9550-10-1-0555 to DDD for the hyperspectral imager, National Science Foundation grants DEB #1257555 to JSS, #1258141 to WLS and MPD, and MRI# 1040321 to DFG, National Geographic Society grants (W101-10 to D.F.G. and W114-12 to J.S.S.), and The Ray and Barbara Dalio Family Foundation Explore 21 expedition grant to JSS, DFG, and VAP. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank the John B. Pierce Laboratory Machine Shop for building underwater lights; the Maurice Hatter Foundation for post-doctoral fellowship support to DA; Rick Elkus, Patty Elkus, Kyle McBurnie, and Nicholas Lebeouf for assistance and support in filming C. ventriosum in Scripps Canyon; the BBC Natural History Unit and Christoph Pierre for assistance in Santa Barbara; Joe Yaiullo of the Long Island Aquarium, Todd Gardner of Suffolk County Community College, Donnie Harrington and Tracy Romano of Mystic Aquarium for assistance imaging S. retifer; and Fernando Nosratpour and Leslee Matsushige of the Birch Aquarium for assistance imaging C. ventriosum. We thank Biopixel for generously allowing use of their image of an orectolobid and Kathleen Smith for reading and commenting on the manuscript.

PY - 2016/4/25

Y1 - 2016/4/25

N2 - Biofluorescence has recently been found to be widespread in marine fishes, including sharks. Catsharks, such as the Swell Shark (Cephaloscyllium ventriosum) from the eastern Pacific and the Chain Catshark (Scyliorhinus retifer) from the western Atlantic, are known to exhibit bright green fluorescence. We examined the spectral sensitivity and visual characteristics of these reclusive sharks, while also considering the fluorescent properties of their skin. Spectral absorbance of the photoreceptor cells in these sharks revealed the presence of a single visual pigment in each species. Cephaloscyllium ventriosum exhibited a maximum absorbance of 484 ± 3 nm and an absorbance range at half maximum (λ1/2max) of 440-540 nm, whereas for S. retifer maximum absorbance was 488 ± 3 nm with the same absorbance range. Using the photoreceptor properties derived here, a "shark eye" camera was designed and developed that yielded contrast information on areas where fluorescence is anatomically distributed on the shark, as seen from other sharks' eyes of these two species. Phylogenetic investigations indicate that biofluorescence has evolved at least three times in cartilaginous fishes. The repeated evolution of biofluorescence in elasmobranchs, coupled with a visual adaptation to detect it; and evidence that biofluorescence creates greater luminosity contrast with the surrounding background, highlights the potential importance of biofluorescence in elasmobranch behavior and biology.

AB - Biofluorescence has recently been found to be widespread in marine fishes, including sharks. Catsharks, such as the Swell Shark (Cephaloscyllium ventriosum) from the eastern Pacific and the Chain Catshark (Scyliorhinus retifer) from the western Atlantic, are known to exhibit bright green fluorescence. We examined the spectral sensitivity and visual characteristics of these reclusive sharks, while also considering the fluorescent properties of their skin. Spectral absorbance of the photoreceptor cells in these sharks revealed the presence of a single visual pigment in each species. Cephaloscyllium ventriosum exhibited a maximum absorbance of 484 ± 3 nm and an absorbance range at half maximum (λ1/2max) of 440-540 nm, whereas for S. retifer maximum absorbance was 488 ± 3 nm with the same absorbance range. Using the photoreceptor properties derived here, a "shark eye" camera was designed and developed that yielded contrast information on areas where fluorescence is anatomically distributed on the shark, as seen from other sharks' eyes of these two species. Phylogenetic investigations indicate that biofluorescence has evolved at least three times in cartilaginous fishes. The repeated evolution of biofluorescence in elasmobranchs, coupled with a visual adaptation to detect it; and evidence that biofluorescence creates greater luminosity contrast with the surrounding background, highlights the potential importance of biofluorescence in elasmobranch behavior and biology.

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U2 - 10.1038/srep24751

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Biofluorescence in Catsharks (Scyliorhinidae): Fundamental Description and Relevance for Elasmobranch Visual Ecology

Abstract

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