Red fluorescence in marine fishes: Functions, mechanisms and consequences for visual communication on reefs
Final Report Abstract
After discovering red fluorescence in marine fishes this project explored and tested possible visual functions of fluorescence, resulting in three research avenues. First, we planned to collect and characterize the presence and expression of (red) fluorescence in a large sample of phylogenetically diverse marine fish species. Using these, we wanted to generate hypotheses of possible adaptive functions. The data set would then be used to test these hypotheses using phylogenetically corrected associations between the expression of fluorescence and the characteristics of a species’ behavioral and ecological properties. Second, we aimed at developing methods to characterize the detailed properties of fluorescence in live fish, and to describe the histological and cellular characteristics of fluorescence when expressed in situ in fish tissue. We also hoped to be able to characterize the pigments themselves and wanted to address the mechanisms associated with fluorescence modulation and detection of fluorescence. This included studies of the spectral sensitivity and eye anatomy of selected cases. We also planned to investigate whether fluorescence may stem from a microbial source. Third, promising functional hypotheses were to be addressed experimentally in selected model systems in the laboratory and in the field. Important questions we focused on in this context were: - Fluorescence is relevant for vision. It can be perceived by the own or other species and is regulated in an adaptive manner. - Fluorescence is used for intra-specific communication in a sexual selection context. - Cases of particularly strong fluorescence around the eyes may represent a short-distance "Illumination" property for assisted visual detection. - Lateral light redirection (beyond fluorescence) is indeed sufficient to facilitate detection of the reflective eyes of cryptic predatory fish. We call it "diurnal active photolocation". Lessons from innovative research: Ever since we started to mention "active photolocation" in manuscripts, it has met with unusually harsh, in part inappropriate, personal criticism from anonymous reviewers from some anonymous reviewers from the small visual ecology community. Most of this criticism was not based on facts or specific problems with our experimental designs, data collection or analysis methods, but by the "disbelief" that diurnal active photolocation works or even exists. Consequently, any experimental indication that we provided therefore “had to be flawed”. It appeared as if our reviewers may extrapolate own experience from their (usually larger, free-swimming) model species to our “small-world” system, where relevant distances and sizes are measured in millimetres and centimetres rather than metres. This resulted in unnecessary rejections and delays of up to year or more for some manuscripts. It showed us that the anonymous reviewing system that is characteristic for many journals prevents fruitful scientific discussion between reviewers and authors to improve their work and promote rather than prevent progress in science. We were surprised to learn that anonymous reviewing is sometimes misused by "apparent experts" to prevent the spread of new ideas. There are unfortunately only few options available to authors to counteract "disbelief". One option is to publish in open reviewing journals, which publish the reviewers’ names and their evaluations after publication. In such cases, we have indeed received "normal" critical reviews that were constructive and polite, and that directly improved our work. We will advocate and use such opportunities more in the future. The ultimate paper resulting from this project is the Santon et al. 2020 Proc. roy. Soc. B paper. It contains work from > 5 years of method development and data collection that would normally fill 3 papers (a visual model, a laboratory experiment and two field experiments using a new method to manipulation light redirection). Without the open and fair reviewing policy of the Royal Society, it probably would not have been published. It represents a breakthrough in visual ecology.
Publications
- 2012 A fluorescent chromatophore changes the level of fluorescence in a reef fish. PLoS ONE. 7, e37913
Wucherer, M. F., Michiels, N. K.
(See online at https://doi.org/10.1371/journal.pone.0037913) - 2014 Fairy wrasses perceive and respond to their deep red fluorescent coloration. Proceedings of the Royal Society B 281, 7
Gerlach, T., Sprenger, D., Michiels, N. K.
(See online at https://doi.org/10.1098/rspb.2014.0787) - 2014 Red fluorescence increases with depth in reef fishes, supporting a visual function, not UV protection. Proceedings of the Royal Society B 281, 20141211
Meadows, M. G., Anthes, N., Dangelmayer, S., Alwany, M. A., Gerlach, T., Schulte, G., Sprenger, D., Theobald, J., Michiels, N. K.
(See online at https://doi.org/10.1098/rspb.2014.1211) - 2014 Regulation of red fluorescent light emission in a cryptic marine fish. Frontiers in Zoology 11, 1
Wucherer, M. F., Michiels, N. K.
(See online at https://doi.org/10.1186/1742-9994-11-1) - 2015 The Red-Fluorescing Marine Fish Tripterygion delaisi can Perceive its Own Red Fluorescent Colour. Ethology. 121, 566-576
Kalb, N., Schneider, R. F., Sprenger, D., Michiels, N. K.
(See online at https://doi.org/10.1111/eth.12367) - Diversity and Ecological Correlates of Red Fluorescence in Marine Fishes. Frontiers in Ecology and Evolution, Vol. 4. 2016, 00126.
Anthes, N., Theobald, J., Gerlach, T., Meadows, M. G., Michiels, N. K.
(See online at https://doi.org/10.3389/fevo.2016.00126) - Fluorescence characterisation and visual ecology of pseudocheilinid wrasses. Frontiers in Zoology 13. 2016, 13.
Gerlach, T., Theobald, J., Hart, N. S., Collin, S. P., Michiels, N. K.
(See online at https://doi.org/10.1186/s12983-016-0145-1) - Successful operant conditioning of marine fish in their natural environment. Copeia, Vol. 104. 2016, Issue 2, pp. 380-386.
Haderer, I. K., Michiels, N. K.
(See online at https://doi.org/10.1643/CE-14-185) - The consistent difference in red fluorescence in fishes across a 15 m depth gradient is triggered by ambient brightness, not by ambient spectrum. BMC Research Notes, Vol. 9.2016, 107.
Harant, U. K., Michiels, N. K., Anthes, N., Meadows, M. G.
(See online at https://doi.org/10.1186/s13104-016-1911-z) - Anatomical analysis of the retinal specializations to a cryptobenthic,
micro-predatory lifestyle in the Mediterranean triplefin blenny Tripterygion delaisi. Frontiers in Neuroanatomy, Vol. 11.2017, 122.
Fritsch R., Collin S.P., Michiels N.K.
(See online at https://doi.org/10.3389/fnana.2017.00122) - Fish with red fluorescent eyes forage more efficiently under dim, blue- green light conditions. BMC Ecology, Vol. 17. 2017, Article number: 18.
Harant, U. K., Michiels, N. K.
(See online at https://doi.org/10.1186/s12898-017-0127-y) - Optic-nerve-transmitted eyeshine, a new type of light emission from fish eyes. Frontiers in Zoology, Vol. 14. 2017, Article number: 14.
Fritsch, R., Ullmann, J. F. P., Bitton, P.-P., Collin, S. P., Michiels, N. K.
(See online at https://doi.org/10.1186/s12983-017-0198-9) - Red fluorescence of the triplefin Tripterygion delaisi is increasingly visible against background light with increasing depth. Royal Society Open Science, Volume 4. 2017, Issue 3, Article ID:161009.
Bitton, P.-P., Harant, U. K., Fritsch, R., Champ, C. M., Temple, S. E., Michiels, N. K.
(See online at https://doi.org/10.1098/rsos.161009) - Daytime eyeshine contributes to pupil camouflage in a cryptobenthic marine fish. Scientific Reports, Vol. 8. 2018, Issue 1, Article number: 7368.
Santon M., Bitton P.P., Harant U.K., Michiels N.K.
(See online at https://doi.org/10.1038/s41598-018-25599-y) - Do the fluorescent red eyes of the marine fish Tripterygion delaisi stand out? In situ and in vivo measurements at two depths. Ecology and Evolution, Vol. 8. 2018, Issue 9, pp. 4685-4694.
Harant U.K., Santon M., Bitton P.-P., Wehrberger F., Griessler T., Meadows M.G., Champ C.M., Michiels N.K.
(See online at https://doi.org/10.1002/ece3.4025) - The contrast sensitivity function of a small cryptobenthic marine fish. Journal of Vision, Vol. 19. 2019, Issue 2: 1.
Santon M., Münch T.A., Michiels N.K.
(See online at https://doi.org/10.1167/19.2.1) - Visual modelling supports the potential for prey detection by means of diurnal active photolocation in a small cryptobenthic fish. Scientific Reports, Vol. 9. 2019, Article number: 8089.
Bitton P.-P., Christmann S.A.Y., Santon M., Harant U.K., Michiels N.K.
(See online at https://doi.org/10.1038/s41598-019-44529-0) - Redirection of ambient light improves predator detection in a diurnal fish. Proceedings of the Royal Society B, Vol. 287. 2020, Issue 1919: 20192292.
Santon M., Bitton P.-P., Dehm J., Fritsch R., Harant U.K., Anthes N., Michiels N.K.
(See online at https://doi.org/10.1098/rspb.2019.2292)
