The consistent difference in red fluorescence in fishes across a 15 m depth gradient is triggered by ambient brightness, not by ambient spectrum

Abstract

Background: Organisms adapt to fluctuations or gradients in their environment by means of genetic change or phenotypic plasticity. Consistent adaptation across small spatial scales measured in meters, however, has rarely been reported. We recently found significant variation in fluorescence brightness in six benthic marine fish species across a 15 m depth gradient. Here, we investigate whether this can be explained by phenotypic plasticity alone, using the triplefin Tripterygion delaisi as a model species. In two separate experiments, we measure change in red fluorescent brightness to spectral composition and ambient brightness, two central parameters of the visual environment that change rapidly with depth.

Results: Changing the ambient spectra simulating light at -5 or -20 m depth generated no detectable changes in mean fluorescence brightness after 4-6 weeks. In contrast, a reduction in ambient brightness generated a significant and reversible increase in mean fluorescence, most of this within the first week. Although individuals can quickly up- and down-regulate their fluorescence around this mean value using melanosome aggregation and dispersal, we demonstrate that this range around the mean remained unaffected by either treatment.

Conclusion: We show that the positive association between fluorescence and depth observed in the field can be fully explained by ambient light brightness, with no detectable additional effect of spectral composition. We propose that this change is achieved by adjusting the ratio of melanophores and fluorescent iridophores in the iris.

Fig. 1

Iris fluorescence regulation mechanisms of Tripterygion delaisi. Melanophore state modulation is fast and covers or uncovers fluorescence as an instant response to a current chance in conditions [24]. Chromophore number and pigmentation change is much slower and is the presumed mechanism behind the relationship between depth and fluorescence [10]

Fig. 2

Iris fluorescence brightness at deep and shallow capture depths. Iris fluorescence brightness of Tripterygion delaisi measured as total photon radiance (photons s⁻¹ sr⁻¹ m⁻²) (n = 40) in the field. Boxplots show median (horizontal line), upper and lower quartiles (boxes) and ranges (whiskers)

Fig. 3

Iris fluorescence in response to spectral composition. Iris fluorescence brightness of Tripterygion delaisi measured as total photon radiance (photons s⁻¹ sr⁻¹ m⁻²) in the spectrum experiment. Fish group 1 (n = 20) started with the −20 m spectrum (phase I) and changed to the −5 m spectrum after 6 weeks (phase II), whereas group 2 (n = 20) received the opposite treatment. Fish were checked for another 4 weeks after the light switch. Lines represent mean total photon radiance for group 1 (dashed) and 2 (solid)

Fig. 4

Iris fluorescence measured during the brightness experiment. Iris fluorescence of Tripterygion delaisi measured as total photon radiance (photons s⁻¹ sr⁻¹ m⁻²) throughout the brightness treatment. Group 1 (n = 10) started with the dark light treatment (phase I) and changed to the bright light treatment (phase II) after 3 weeks. Group 2 (n = 9) received the reverse treatment. Lines represent mean photon radiance of group 1 (dashed) and 2 (solid)

Fig. 5

Daily change in eye fluorescence brightness measured in the last week of the brightness experiment. Iris fluorescence measured as total photon radiance (photons s⁻¹ sr⁻¹ m⁻²) in Tripterygion delaisi after the final reversal of the light conditions (n = 19). Experimental day 0 is identical to the measurement taken during week 6 in Fig. 5. Lights were changed in the morning of the first experimental day. Fish previously held under dark light conditions (group 1) received the bright light treatment for the following 7 days whereas fish deriving from bright light conditions (group 2) changed to the dark light treatment

Fig. 6

Maximum and minimum fluorescence brightness of Tripterygion delaisi eyes. Iris fluorescence brightness measured as total photon radiance (photon s⁻¹ sr⁻¹ m⁻²), based on 20 freshly caught fish at euryspectral (−5 m) and stenospectral (−20 m) depths, 20 fish measured after the spectrum experiment, and 19 fish measured after the brightness experiment. Cross lines represent significant differences between groups with significance level indicated (*p < 0.05, **p < 0.01). Note that measurements cannot be directly compared between experiments due to non-standardized measuring conditions

Fig. 7

Comparison of overall brightness (a, b) and spectral shape (c, d) between field and lab measurements. Spectral curves are given as total photon irradiance (photon s⁻¹ m⁻² nm⁻¹). Note that c and d represent area-normalized curves

Fig. 8

Comparison of spectral shapes between the 100 % and 1 % brightness treatment. Spectral curves are given as photon radiance (photon s⁻¹ sr⁻¹ m⁻² nm⁻¹)