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Red fluorescence in reef fish: a novel signalling mechanism?

Michiels NK, Anthes N, Hart NS, Herler J, Meixner AJ, Schleifenbaum F, Schulte G, Siebeck UE, Sprenger D, Wucherer MF - BMC Ecol. (2008)

Bottom Line: In most cases peak emission was around 600 nm and fluorescence was associated with guanine crystals, which thus far were known for their light reflecting properties only.Fluorescence patterns were typically associated with the eyes or the head, varying substantially even between species of the same genus.Our findings challenge the notion that red light is of no importance to marine fish, calling for a reassessment of its role in fish visual ecology in subsurface marine environments.

View Article: PubMed Central - HTML - PubMed

Affiliation: Faculty of Biology, University of Tübingen, Auf der Morgenstelle 28, 72076 Tübingen, Germany. nico.michiels@uni-tuebingen.de

ABSTRACT

Background: At depths below 10 m, reefs are dominated by blue-green light because seawater selectively absorbs the longer, 'red' wavelengths beyond 600 nm from the downwelling sunlight. Consequently, the visual pigments of many reef fish are matched to shorter wavelengths, which are transmitted better by water. Combining the typically poor long-wavelength sensitivity of fish eyes with the presumed lack of ambient red light, red light is currently considered irrelevant for reef fish. However, previous studies ignore the fact that several marine organisms, including deep sea fish, produce their own red luminescence and are capable of seeing it.

Results: We here report that at least 32 reef fishes from 16 genera and 5 families show pronounced red fluorescence under natural, daytime conditions at depths where downwelling red light is virtually absent. Fluorescence was confirmed by extensive spectrometry in the laboratory. In most cases peak emission was around 600 nm and fluorescence was associated with guanine crystals, which thus far were known for their light reflecting properties only. Our data indicate that red fluorescence may function in a context of intraspecific communication. Fluorescence patterns were typically associated with the eyes or the head, varying substantially even between species of the same genus. Moreover red fluorescence was particularly strong in fins that are involved in intraspecific signalling. Finally, microspectrometry in one fluorescent goby, Eviota pellucida, showed a long-wave sensitivity that overlapped with its own red fluorescence, indicating that this species is capable of seeing its own fluorescence.

Conclusion: We show that red fluorescence is widespread among marine fishes. Many features indicate that it is used as a private communication mechanism in small, benthic, pair- or group-living fishes. Many of these species show quite cryptic colouration in other parts of the visible spectrum. High inter-specific variation in red fluorescence and its association with structures used in intra-specific signalling further corroborate this view. Our findings challenge the notion that red light is of no importance to marine fish, calling for a reassessment of its role in fish visual ecology in subsurface marine environments.

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General introduction to light attenuation and observation of natural fluorescence in near-shore marine environments. a. The visual spectrum ranges from 400 to 700 nm at the water surface, but downwelling sunlight loses the red component (600–700 nm) rapidly within 10–15 m (modified from Pinet PR (2000) Invitation to Oceanography. Jones and Bartlett). UV and violet wavelengths are attenuated less rapidly. The attenuation with depth of spectral composition (and light intensity, not shown) varies strongly with the concentration of organic matter in the water column. b. Most red pigmentation is based on reflectance of the red component of ambient light and therefore only appears "red" when close to the surface during daytime or under broad spectral light (e.g. dive torch). Fish with this pigmentation appear dull grey in deeper water. Red fluorescent patterns, however, continue to appear reddish and bright, even in deeper water, where excitation of fluorescent pigments by shorter wavelengths induces redness. Note that red fluorescence is rarely perceived as pure red, but is mostly an enhancer of mixed colours such as pink, lilac or red brown. Even so, it remains clearly visible in deeper water as a contrast enhancer. Closer to the surface, fluorescent patterns are masked by reflective colouration (e.g. yellow and red in Eviota pellucida, Fig. 3). c. Since excitation frequencies (blue-green) are brighter than emission frequencies (red in our example) red fluorescence is best seen when viewed through a filter that blocks the excitation frequencies and only allows the emission frequencies to pass. When looking through a red filter in e.g. 20 m depth, all remaining red light must be "locally produced" through fluorescence or bioluminescence. Given that fluorescence exploits light energy from ambient light, it is more efficient than bioluminescence and therefore likely to be the mechanism of choice for diurnal fish.
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Figure 1: General introduction to light attenuation and observation of natural fluorescence in near-shore marine environments. a. The visual spectrum ranges from 400 to 700 nm at the water surface, but downwelling sunlight loses the red component (600–700 nm) rapidly within 10–15 m (modified from Pinet PR (2000) Invitation to Oceanography. Jones and Bartlett). UV and violet wavelengths are attenuated less rapidly. The attenuation with depth of spectral composition (and light intensity, not shown) varies strongly with the concentration of organic matter in the water column. b. Most red pigmentation is based on reflectance of the red component of ambient light and therefore only appears "red" when close to the surface during daytime or under broad spectral light (e.g. dive torch). Fish with this pigmentation appear dull grey in deeper water. Red fluorescent patterns, however, continue to appear reddish and bright, even in deeper water, where excitation of fluorescent pigments by shorter wavelengths induces redness. Note that red fluorescence is rarely perceived as pure red, but is mostly an enhancer of mixed colours such as pink, lilac or red brown. Even so, it remains clearly visible in deeper water as a contrast enhancer. Closer to the surface, fluorescent patterns are masked by reflective colouration (e.g. yellow and red in Eviota pellucida, Fig. 3). c. Since excitation frequencies (blue-green) are brighter than emission frequencies (red in our example) red fluorescence is best seen when viewed through a filter that blocks the excitation frequencies and only allows the emission frequencies to pass. When looking through a red filter in e.g. 20 m depth, all remaining red light must be "locally produced" through fluorescence or bioluminescence. Given that fluorescence exploits light energy from ambient light, it is more efficient than bioluminescence and therefore likely to be the mechanism of choice for diurnal fish.

Mentions: At depths below 10 m, reefs are dominated by blue-green light because seawater selectively absorbs the longer, 'red' wavelengths (600 nm and more) from downwelling sunlight (Fig. 1)[1,2]. Consequently, many reef fish have visual pigments matched to shorter wavelengths, which are transmitted better by water [3-5]. In addition, ecological studies of fish vision must correct for the spectrum available at the depth where they live [1,6,7] and therefore routinely correct spectral sensitivity measurements from the laboratory for the available (mostly downwelling) light on the reef. This reduces the relevance of red light to reef fish even more. However, this procedure ignores the fact that several marine organisms, including deep sea fish, produce their own red bioluminescence and are capable of seeing it [8,9]. The purpose of this study was (1) to see "with our own eyes" whether there is indeed a lack of red light at depth in the euphotic zone during daytime and (2) to identify the observed sources of natural red fluorescence in fish in particular. This work combines results from several studies carried out on coral reefs in the Red Sea and the Great Barrier Reef and has been supplemented by observations and measurements on fish in the laboratory.


Red fluorescence in reef fish: a novel signalling mechanism?

Michiels NK, Anthes N, Hart NS, Herler J, Meixner AJ, Schleifenbaum F, Schulte G, Siebeck UE, Sprenger D, Wucherer MF - BMC Ecol. (2008)

General introduction to light attenuation and observation of natural fluorescence in near-shore marine environments. a. The visual spectrum ranges from 400 to 700 nm at the water surface, but downwelling sunlight loses the red component (600–700 nm) rapidly within 10–15 m (modified from Pinet PR (2000) Invitation to Oceanography. Jones and Bartlett). UV and violet wavelengths are attenuated less rapidly. The attenuation with depth of spectral composition (and light intensity, not shown) varies strongly with the concentration of organic matter in the water column. b. Most red pigmentation is based on reflectance of the red component of ambient light and therefore only appears "red" when close to the surface during daytime or under broad spectral light (e.g. dive torch). Fish with this pigmentation appear dull grey in deeper water. Red fluorescent patterns, however, continue to appear reddish and bright, even in deeper water, where excitation of fluorescent pigments by shorter wavelengths induces redness. Note that red fluorescence is rarely perceived as pure red, but is mostly an enhancer of mixed colours such as pink, lilac or red brown. Even so, it remains clearly visible in deeper water as a contrast enhancer. Closer to the surface, fluorescent patterns are masked by reflective colouration (e.g. yellow and red in Eviota pellucida, Fig. 3). c. Since excitation frequencies (blue-green) are brighter than emission frequencies (red in our example) red fluorescence is best seen when viewed through a filter that blocks the excitation frequencies and only allows the emission frequencies to pass. When looking through a red filter in e.g. 20 m depth, all remaining red light must be "locally produced" through fluorescence or bioluminescence. Given that fluorescence exploits light energy from ambient light, it is more efficient than bioluminescence and therefore likely to be the mechanism of choice for diurnal fish.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2567963&req=5

Figure 1: General introduction to light attenuation and observation of natural fluorescence in near-shore marine environments. a. The visual spectrum ranges from 400 to 700 nm at the water surface, but downwelling sunlight loses the red component (600–700 nm) rapidly within 10–15 m (modified from Pinet PR (2000) Invitation to Oceanography. Jones and Bartlett). UV and violet wavelengths are attenuated less rapidly. The attenuation with depth of spectral composition (and light intensity, not shown) varies strongly with the concentration of organic matter in the water column. b. Most red pigmentation is based on reflectance of the red component of ambient light and therefore only appears "red" when close to the surface during daytime or under broad spectral light (e.g. dive torch). Fish with this pigmentation appear dull grey in deeper water. Red fluorescent patterns, however, continue to appear reddish and bright, even in deeper water, where excitation of fluorescent pigments by shorter wavelengths induces redness. Note that red fluorescence is rarely perceived as pure red, but is mostly an enhancer of mixed colours such as pink, lilac or red brown. Even so, it remains clearly visible in deeper water as a contrast enhancer. Closer to the surface, fluorescent patterns are masked by reflective colouration (e.g. yellow and red in Eviota pellucida, Fig. 3). c. Since excitation frequencies (blue-green) are brighter than emission frequencies (red in our example) red fluorescence is best seen when viewed through a filter that blocks the excitation frequencies and only allows the emission frequencies to pass. When looking through a red filter in e.g. 20 m depth, all remaining red light must be "locally produced" through fluorescence or bioluminescence. Given that fluorescence exploits light energy from ambient light, it is more efficient than bioluminescence and therefore likely to be the mechanism of choice for diurnal fish.
Mentions: At depths below 10 m, reefs are dominated by blue-green light because seawater selectively absorbs the longer, 'red' wavelengths (600 nm and more) from downwelling sunlight (Fig. 1)[1,2]. Consequently, many reef fish have visual pigments matched to shorter wavelengths, which are transmitted better by water [3-5]. In addition, ecological studies of fish vision must correct for the spectrum available at the depth where they live [1,6,7] and therefore routinely correct spectral sensitivity measurements from the laboratory for the available (mostly downwelling) light on the reef. This reduces the relevance of red light to reef fish even more. However, this procedure ignores the fact that several marine organisms, including deep sea fish, produce their own red bioluminescence and are capable of seeing it [8,9]. The purpose of this study was (1) to see "with our own eyes" whether there is indeed a lack of red light at depth in the euphotic zone during daytime and (2) to identify the observed sources of natural red fluorescence in fish in particular. This work combines results from several studies carried out on coral reefs in the Red Sea and the Great Barrier Reef and has been supplemented by observations and measurements on fish in the laboratory.

Bottom Line: In most cases peak emission was around 600 nm and fluorescence was associated with guanine crystals, which thus far were known for their light reflecting properties only.Fluorescence patterns were typically associated with the eyes or the head, varying substantially even between species of the same genus.Our findings challenge the notion that red light is of no importance to marine fish, calling for a reassessment of its role in fish visual ecology in subsurface marine environments.

View Article: PubMed Central - HTML - PubMed

Affiliation: Faculty of Biology, University of Tübingen, Auf der Morgenstelle 28, 72076 Tübingen, Germany. nico.michiels@uni-tuebingen.de

ABSTRACT

Background: At depths below 10 m, reefs are dominated by blue-green light because seawater selectively absorbs the longer, 'red' wavelengths beyond 600 nm from the downwelling sunlight. Consequently, the visual pigments of many reef fish are matched to shorter wavelengths, which are transmitted better by water. Combining the typically poor long-wavelength sensitivity of fish eyes with the presumed lack of ambient red light, red light is currently considered irrelevant for reef fish. However, previous studies ignore the fact that several marine organisms, including deep sea fish, produce their own red luminescence and are capable of seeing it.

Results: We here report that at least 32 reef fishes from 16 genera and 5 families show pronounced red fluorescence under natural, daytime conditions at depths where downwelling red light is virtually absent. Fluorescence was confirmed by extensive spectrometry in the laboratory. In most cases peak emission was around 600 nm and fluorescence was associated with guanine crystals, which thus far were known for their light reflecting properties only. Our data indicate that red fluorescence may function in a context of intraspecific communication. Fluorescence patterns were typically associated with the eyes or the head, varying substantially even between species of the same genus. Moreover red fluorescence was particularly strong in fins that are involved in intraspecific signalling. Finally, microspectrometry in one fluorescent goby, Eviota pellucida, showed a long-wave sensitivity that overlapped with its own red fluorescence, indicating that this species is capable of seeing its own fluorescence.

Conclusion: We show that red fluorescence is widespread among marine fishes. Many features indicate that it is used as a private communication mechanism in small, benthic, pair- or group-living fishes. Many of these species show quite cryptic colouration in other parts of the visible spectrum. High inter-specific variation in red fluorescence and its association with structures used in intra-specific signalling further corroborate this view. Our findings challenge the notion that red light is of no importance to marine fish, calling for a reassessment of its role in fish visual ecology in subsurface marine environments.

Show MeSH
Related in: MedlinePlus