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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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Sources of red fluorescence in fishes. a. Guanine crystals from the eye ring of Eviota pellucida (fluorescence microscopy). b. Same from Ctenogobiops tangaroai (fluorescence overlaid with phase contrast). c. As in b, diamond form (fluorescence microscopy). d. Guanine crystals falling apart in characteristic platelets (from eye ring of E. pellucida, scanning electron micrograph). e. Single red fluorescent guanine crystal among normal crystals in eye ring of the non-fluorescent goby Trimma cana (fluorescence microscopy, see also Fig. 3). f. Scale of Pseudocheilinus evanidus, in which the red fluorescent pigment is associated with bony scales and fin rays (fluorescence microscopy). Scale bar = 50 μm unless indicated otherwise.
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Figure 7: Sources of red fluorescence in fishes. a. Guanine crystals from the eye ring of Eviota pellucida (fluorescence microscopy). b. Same from Ctenogobiops tangaroai (fluorescence overlaid with phase contrast). c. As in b, diamond form (fluorescence microscopy). d. Guanine crystals falling apart in characteristic platelets (from eye ring of E. pellucida, scanning electron micrograph). e. Single red fluorescent guanine crystal among normal crystals in eye ring of the non-fluorescent goby Trimma cana (fluorescence microscopy, see also Fig. 3). f. Scale of Pseudocheilinus evanidus, in which the red fluorescent pigment is associated with bony scales and fin rays (fluorescence microscopy). Scale bar = 50 μm unless indicated otherwise.

Mentions: Dissection revealed that red fluorescence was associated with guanine crystals in pipefish, triplefins, blennies and gobies (Fig. 7, Table 1). Guanine crystals are produced by iridophores and are well known as the source of silvery reflection and iridescence in bony fish[14]. However, they have never been described to show strong red fluorescence. In E. pellucida and Ctenogobiops tangaroai, only about half of the crystals isolated from the eye rings showed bright red fluorescence (Fig. 7b), suggesting that the fluorescing substance is produced or sequestered independently from the crystals. Preparations of crystals maintained strong fluorescence after prolonged storage in a dried or liquid form (70% EtOH or 4% formaldehyde), allowing us to confirm fluorescence in preserved gobies collected up to 5 years before (Collection JH, Vienna, Table 1). This is in striking contrast to reflective red pigmentation, which bleaches out within hours after fixation. We did not find fluorescent guanine crystals in P. evanidus. Here, microscopic investigation suggests the presence of a fluorescent pigment associated with the bony tissue of scales and fin rays (Fig. 7f). This pigment has a chemical stability in preserved specimens that matches that of guanine-linked red fluorescence.


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)

Sources of red fluorescence in fishes. a. Guanine crystals from the eye ring of Eviota pellucida (fluorescence microscopy). b. Same from Ctenogobiops tangaroai (fluorescence overlaid with phase contrast). c. As in b, diamond form (fluorescence microscopy). d. Guanine crystals falling apart in characteristic platelets (from eye ring of E. pellucida, scanning electron micrograph). e. Single red fluorescent guanine crystal among normal crystals in eye ring of the non-fluorescent goby Trimma cana (fluorescence microscopy, see also Fig. 3). f. Scale of Pseudocheilinus evanidus, in which the red fluorescent pigment is associated with bony scales and fin rays (fluorescence microscopy). Scale bar = 50 μm unless indicated otherwise.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: Sources of red fluorescence in fishes. a. Guanine crystals from the eye ring of Eviota pellucida (fluorescence microscopy). b. Same from Ctenogobiops tangaroai (fluorescence overlaid with phase contrast). c. As in b, diamond form (fluorescence microscopy). d. Guanine crystals falling apart in characteristic platelets (from eye ring of E. pellucida, scanning electron micrograph). e. Single red fluorescent guanine crystal among normal crystals in eye ring of the non-fluorescent goby Trimma cana (fluorescence microscopy, see also Fig. 3). f. Scale of Pseudocheilinus evanidus, in which the red fluorescent pigment is associated with bony scales and fin rays (fluorescence microscopy). Scale bar = 50 μm unless indicated otherwise.
Mentions: Dissection revealed that red fluorescence was associated with guanine crystals in pipefish, triplefins, blennies and gobies (Fig. 7, Table 1). Guanine crystals are produced by iridophores and are well known as the source of silvery reflection and iridescence in bony fish[14]. However, they have never been described to show strong red fluorescence. In E. pellucida and Ctenogobiops tangaroai, only about half of the crystals isolated from the eye rings showed bright red fluorescence (Fig. 7b), suggesting that the fluorescing substance is produced or sequestered independently from the crystals. Preparations of crystals maintained strong fluorescence after prolonged storage in a dried or liquid form (70% EtOH or 4% formaldehyde), allowing us to confirm fluorescence in preserved gobies collected up to 5 years before (Collection JH, Vienna, Table 1). This is in striking contrast to reflective red pigmentation, which bleaches out within hours after fixation. We did not find fluorescent guanine crystals in P. evanidus. Here, microscopic investigation suggests the presence of a fluorescent pigment associated with the bony tissue of scales and fin rays (Fig. 7f). This pigment has a chemical stability in preserved specimens that matches that of guanine-linked red fluorescence.

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