Red fluorescence in reef fish: A novel signalling mechanism?

Annals of Occupational and Environmental Medicine

Nico K Michiels³  Nils Anthes³  Nathan S Hart¹  Jürgen Herler⁴  Alfred J Meixner²  Frank Schleifenbaum²  Gregor Schulte³  Ulrike E Siebeck¹  Dennis Sprenger³  Matthias F Wucherer³ 

[1] School of Biomedical Sciences, University of Queensland, Brisbane, Queensland 4072, Australia

[2] Institute of Physical and Theoretical Chemistry, University of Tübingen, Auf der Morgenstelle 8, 72076 Tübingen, Germany

[3] Faculty of Biology, University of Tübingen, Auf der Morgenstelle 28, 72076 Tübingen, Germany

[4] Department of Theoretical Biology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria

Others  :  1087054
DOI  :  10.1186/1472-6785-8-16

 received in 2008-06-04, accepted in 2008-09-16,  发布年份 2008

【 摘 要 】

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.

【 授权许可】

   
2008 Michiels et al; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Marshall NJ, Jennings K, McFarland WN, Loew ER, Losey GS: Visual biology of Hawaiian coral reef fishes. III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 2003, 2003(3):467-480.
• [2]Loew ER, Zhang H: Propagation of visual signals in the aquatic environment: An interactive windows-based model. In Communication in Fishes. Volume 2. Edited by Ladich F, Collin SP, Moller P, Kapoor BG. Enfield (NH): Science Publishers; 2006::281-302.
• [3]Losey GS, McFarland WN, Loew ER, Zamzow JP, Nelson PA, Marshall NJ: Visual biology of Hawaiian coral reef fishes. I. Ocular transmission and visual pigments. Copeia 2003, 2003(3):433-454.
• [4]Siebeck UE, Losey GS, Marshall J: UV Communication in Fish. In Communication in Fishes. Volume 2. Edited by Ladich F, Collin SP, Moller P, Kapoor BG. Enfield (NH): Science Publishers; 2006::423-455.
• [5]Marshall J, Vorobyev M, Siebeck UE: What does a reef fish see when it sees a reef fish? Eating 'Nemo'©. In Communication in Fishes. Volume 2. Edited by Ladich F, Collin SP, Moller P, Kapoor BG. Enfield (NH): Science Publishers; 2006::393-422.
• [6]Lythgoe JN, Muntz WRA, Partridge JC, Shand J, Williams DM: The ecology of the visual pigments of snappers (Lutjanidae) on the Great Barrier Reef. J Comp Physiol A 1994, 174(4):461-467.
• [7]Job SD, Shand J: Spectral sensitivity of larval and juvenile coral reef fishes: implications for feeding in a variable light environment. Mar Ecol Prog Ser 2001, 214:267-277.
• [8]Douglas RH, Mullineaux CW, Partridge JC: Long-wave sensitivity in deep-sea stomiid dragonfish with far-red bioluminescence: evidence for a dietary origin of the chlorophyll-derived retinal photosensitizer of Malacosteus niger. Philos T Roy Soc B 2000, 355(1401):1269-1272.
• [9]Bowmaker JK, Dartnall HJA, Herring PJ: Longwave-sensitive visual pigments in some deep-sea fishes: segregation of 'paired' rhodopsins and porphyropsins. J Comp Physiol A 1988, 163(5):685-698.
• [10]Mazel CH, Fuchs E: Contribution of fluorescence to the spectral signature and perceived color of corals. Limnol Oceanogr 2003, 48:390-401.
• [11]Limbaugh C, North WJ: Fluorescent, benthic, Pacific Coast coelenterates. Nature 1956, 178:497-498.
• [12]Field S, Bulina M, Kelmanson I, Bielawski J, Matz M: Adaptive evolution of multicolored fluorescent proteins in reef-building corals. J Mol Evol 2006, 62(3):332.
• [13]Fradkov AF, Chen Y, Ding L, Barsova EV, Matz MV, Lukyanov SA: Novel fluorescent protein from Discosoma coral and its mutants possesses a unique far-red fluorescence. FEBS Letters 2000, 479(3):127-130.
• [14]Levy-Lior A, Pokroy B, Levavi-Sivan B, Leiserowitz L, Weiner S, Addadi L: Biogenic guanine crystals from the skin of fish may be designed to enhance light reflectance. Cryst Growth Des 2008, 8(2):507-511.
• [15]Barry KL, Hawryshyn CW: Spectral sensitivity of the Hawaiian saddle wrasse, Thalassoma duperrey, and implications for visually mediated behaviour on coral reefs. Environ Biol Fish 1999, 56(4):429-442.
• [16]Douglas RH, Partridge JC, Dulai K, Hunt D, Mullineaux CW, Tauber AY, Hynninen PH: Dragon fish see using chlorophyll. Nature 1998, 393(6684):423-424.
• [17]Mosk V, Thomas N, Hart NS, Partridge JC, Beazley LD, Shand J: Spectral sensitivities of the seahorses Hippocampus subelongatus and Hippocampus barbouri and the pipefish Stigmatopora argus. Visual Neuroscience 2007, 24(3):345-354.
• [18]Utne-Palm AC, Bowmaker JK: Spectral sensitivity of the two-spotted goby Gobiusculus flavescens (Fabricius): a physiological and behavioural study. J Exp Biol 2006, 209(11):2034-2041.
• [19]Shand J, Hart NS, Thomas N, Partridge JC: Developmental changes in the cone visual pigments of black bream Acanthopagrus butcheri. J Exp Biol 2002, 205(23):3661-3667.
• [20]Allen G, Steene G, Humann P, DeLoach N: Reef Fish Identificaton – Tropical Pacific. Jacksonville FL: New World Publications Inc; 2003.
• [21]Marshall NJ: Communication and camouflage with the same 'bright' colours in reef fishes. Philos T Roy Soc B 2000, 355(1401):1243-1248.
• [22]Haddock SHD, Dunn CW, Pugh PR, Schnitzler CE: Bioluminescent and red-fluorescent lures in a deep-sea siphonophore. Science 2005, 309(5732):263-263.
• [23]Siebeck UE: Communication in coral reef fish: the role of ultraviolet colour patterns in damselfish territorial behaviour. Anim Behav 2004, 68:273-282.
• [24]Mazel CH, Cronin TW, Caldwell RL, Marshall NJ: Fluorescent enhancement of signalling in a mantis shrimp. Science 2004, 303(5654):51.
• [25]Arnold KE, Owens IPF, Marshall NJ: Fluorescent signaling in parrots. Science 2002, 295(5552):92.
• [26]Odiorne JM: The Occurrence of guanophores in Fundulus. PNAS 1933, 19(7):750-754.
• [27]Mäthger LM, Land MF, Siebeck UE, Marshall NJ: Rapid colour changes in multilayer reflecting stripes in the paradise whiptail, Pentapodus paradiseus. J Exp Biol 2003, 206(20):3607-3613.
• [28]Herler J, Hilgers H: A synopsis of coral and coral-rock associated gobies (Pisces: Gobiidae) from the Gulf of Aqaba, northern Red Sea. Aqua 2005, 10(3):103-132.
• [29]Holleman W: Fishes of the genus Helcogramma (Blennioidei: Tripterygiidae) in the Western Indian Ocean, including Sri Lanka, with descriptions of four new species. Smithiana Bulletin 2007, 7:51-81.
• [30]Holleman W: A review of the triplefin fish genus Enneapterygius (Blennioidei: Tripterygiidae) in the western Indian Ocean, with descriptions of four new species. Smithiana Bulletin 2005, 5:1-25. + 22 plates
• [31]Hart NS: Microspectrophotometry of visual pigments and oil droplets in a marine bird, the wedge-tailed shearwater Puffinus pacificus: topographic variations in photoreceptor spectral characteristics. J Exp Biol 2004, 207(7):1229-1240.