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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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How to distinguish a red fish from a red fluorescent fish?. Comparison between a non-fluorescent goby, Trimma cana (left), and a similar sized, red fluorescent goby, Eviota pellucida (right) under four viewing conditions. a. Artificial white light from a strong Schott KL 2500 LCD halogen cold light source under a Leica stereomicroscope (MZ 16F). b. In a halogen-illuminated aquarium with downwelling light filtered through Lee 729 Scuba-Blue filter (transmission range 400–550 nm, λmax = 500 nm), thus simulating light at depth. c. Illumination as in b, but viewed through a red filter, revealing red fluorescence. d. Illumination as in a, seen under a Leica fluorescence stereomicroscope (MZ 16F) using green light for excitation, while viewing through red filter. The differences between the viewing conditions illustrate that red fluorescence can only be reliably seen when excitation and emission frequencies are separated, as at depth in the sea or under blue light, and by using a red filter for viewing.
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Figure 3: How to distinguish a red fish from a red fluorescent fish?. Comparison between a non-fluorescent goby, Trimma cana (left), and a similar sized, red fluorescent goby, Eviota pellucida (right) under four viewing conditions. a. Artificial white light from a strong Schott KL 2500 LCD halogen cold light source under a Leica stereomicroscope (MZ 16F). b. In a halogen-illuminated aquarium with downwelling light filtered through Lee 729 Scuba-Blue filter (transmission range 400–550 nm, λmax = 500 nm), thus simulating light at depth. c. Illumination as in b, but viewed through a red filter, revealing red fluorescence. d. Illumination as in a, seen under a Leica fluorescence stereomicroscope (MZ 16F) using green light for excitation, while viewing through red filter. The differences between the viewing conditions illustrate that red fluorescence can only be reliably seen when excitation and emission frequencies are separated, as at depth in the sea or under blue light, and by using a red filter for viewing.

Mentions: Of central importance here is our discovery of red fluorescence in reef fishes. Using the principle described above to distinguish "regular" red colouration from red fluorescence (Fig. 3) we identified at least 32 fish species belonging to 16 genera in 5 families that fluoresced visibly in red (Fig. 4, 5, Table 1, see also Additional file 2). Fluorescent patterns usually included the eye ring and parts of the head or thorax and varied substantially between congeners (e.g. in the genera Eviota or Enneapterygius). Fins rarely fluoresced, except for the anal fin (some Gobiidae), the first dorsal fin (Tripterygiidae) or the tailfin (Syngnathidae). A 'whole body glow', including all fins, was present in the small wrasses Pseudocheilinus evanidus and Paracheilinus octotaenia. Visual and photographic evidence from the field was confirmed by extensive fluorescence microscopy and spectrometry of representative cases (Table 1). Fluorescence showed peak emission around 600 nm in most species (Fig. 6a, Table 1). Enneapterygius pusillus showed a second small peak at around 680 nm. P. evanidus differed from all others by having a double peak at 650 and 700 nm. We tested various light sources, including UV, but were not able to detect fluorescent emission at other (shorter) wavelengths in the fish described here. Anecdotal field observations suggest that yellow fluorescence may be present in other fishes (pers. obs.).


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)

How to distinguish a red fish from a red fluorescent fish?. Comparison between a non-fluorescent goby, Trimma cana (left), and a similar sized, red fluorescent goby, Eviota pellucida (right) under four viewing conditions. a. Artificial white light from a strong Schott KL 2500 LCD halogen cold light source under a Leica stereomicroscope (MZ 16F). b. In a halogen-illuminated aquarium with downwelling light filtered through Lee 729 Scuba-Blue filter (transmission range 400–550 nm, λmax = 500 nm), thus simulating light at depth. c. Illumination as in b, but viewed through a red filter, revealing red fluorescence. d. Illumination as in a, seen under a Leica fluorescence stereomicroscope (MZ 16F) using green light for excitation, while viewing through red filter. The differences between the viewing conditions illustrate that red fluorescence can only be reliably seen when excitation and emission frequencies are separated, as at depth in the sea or under blue light, and by using a red filter for viewing.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: How to distinguish a red fish from a red fluorescent fish?. Comparison between a non-fluorescent goby, Trimma cana (left), and a similar sized, red fluorescent goby, Eviota pellucida (right) under four viewing conditions. a. Artificial white light from a strong Schott KL 2500 LCD halogen cold light source under a Leica stereomicroscope (MZ 16F). b. In a halogen-illuminated aquarium with downwelling light filtered through Lee 729 Scuba-Blue filter (transmission range 400–550 nm, λmax = 500 nm), thus simulating light at depth. c. Illumination as in b, but viewed through a red filter, revealing red fluorescence. d. Illumination as in a, seen under a Leica fluorescence stereomicroscope (MZ 16F) using green light for excitation, while viewing through red filter. The differences between the viewing conditions illustrate that red fluorescence can only be reliably seen when excitation and emission frequencies are separated, as at depth in the sea or under blue light, and by using a red filter for viewing.
Mentions: Of central importance here is our discovery of red fluorescence in reef fishes. Using the principle described above to distinguish "regular" red colouration from red fluorescence (Fig. 3) we identified at least 32 fish species belonging to 16 genera in 5 families that fluoresced visibly in red (Fig. 4, 5, Table 1, see also Additional file 2). Fluorescent patterns usually included the eye ring and parts of the head or thorax and varied substantially between congeners (e.g. in the genera Eviota or Enneapterygius). Fins rarely fluoresced, except for the anal fin (some Gobiidae), the first dorsal fin (Tripterygiidae) or the tailfin (Syngnathidae). A 'whole body glow', including all fins, was present in the small wrasses Pseudocheilinus evanidus and Paracheilinus octotaenia. Visual and photographic evidence from the field was confirmed by extensive fluorescence microscopy and spectrometry of representative cases (Table 1). Fluorescence showed peak emission around 600 nm in most species (Fig. 6a, Table 1). Enneapterygius pusillus showed a second small peak at around 680 nm. P. evanidus differed from all others by having a double peak at 650 and 700 nm. We tested various light sources, including UV, but were not able to detect fluorescent emission at other (shorter) wavelengths in the fish described here. Anecdotal field observations suggest that yellow fluorescence may be present in other fishes (pers. obs.).

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