Diversity and Ecological Correlates of Red Fluorescence in Marine Fishes

Abstract

Marine environments at depths below −10 to −25 m are almost devoid of ambient red sunlight because water quickly attenuates long wavelengths. This stenospectral light environment presents unique opportunities for organisms that can transform ambient blue-green light into red light by fluorescence. Numerous marine fish species display intricate patterns of fluorescence. Because color vision is a key component of fish sensory ecology, several putative visual functions of red fluorescence have been proposed but are difficult to test experimentally. Here, we follow a comparative approach to assess the consistency between the phylogenetic distribution of red fluorescence with its presumed functions. We collected and analyzed the largest data set of red fluorescence in fishes to date, consisting of confirmed cases in 272 primarily diurnal fish species from 49 out of 90 surveyed fish families and 12 out of 21 surveyed fish orders, contrasted to 393 fish species with confirmed absence of red fluorescence. Based on a priori hypotheses on adaptive function, we compare the prevalence of red fluorescence among pre-defined sets of species based on ecological or biological characteristics while controlling for shared ancestry. When comparing between species, we find no evidence that red fluorescence is more prevalent in deep-water species, contrasting with our recent finding that fluorescence brightness increases with depth within species. There is also no evidence for a role in group-driven communication. Phylogenetic patterns are consistent, however, with three other predictions. First, fluorescence with a rather patchy distribution across the body occurred significantly more often among sit-and-wait predators or otherwise sedentary fish than in more mobile species, consistent with background matching for camouflage. Second, small, predatory fishes tended to show red fluorescent irides disproportionally often consistent with a proposed function in prey localization. Finally, sexually dimorphic species showed fluorescent fins more often, as predicted if relevant in sexual communication. From these findings, we derive predictions for experimental investigations of the presumed functions of red fluorescence.

Fish with red fluorescent eyes forage more efficiently under dim, blue-green light conditions

“…We define the euryspectral zone as the depth range close to the surface, with an ambient spectrum that is broader than the visual spectrum of most animals. The stenospectral zone, in contrast, describes the depth range below this, where most of the UV and longer wavelengths have been absorbed by the water column [16, 17], resulting in a spectrum that is narrower than the perception limits of most fish [9, 10]. The transition between the two can be between 5 and 25 m, depending on light conditions and variation in light attenuation by the water column.…”

Do the fluorescent red eyes of the marine fish Tripterygion delaisi stand out? In situ and in vivo measurements at two depths

“…Although Anthes et al. () did not find a correlation between increasing depth and red fluorescence across species, it is safe to assume that red fluorescence is more likely to contribute to visual signaling in deeper water rather than in shallow water. In fact, when analyzing individuals collected at 5 and 20 m within single species (including T. delaisi .…”

“…They transform absorbed photons of a given range of wavelength (e.g., in the blue‐green range) and re‐emit light at longer, less energetic, wavelengths (e.g., yellow or red). Although fluorescent pigments are widespread in benthic marine organisms (Alieva et al., ; Eyal et al., ; Marshall & Johnsen, ; Sparks et al., ), their presence in fish living in shallow water (0–40 m) has only recently been confirmed (Anthes et al, ; Gerlach et al, ; Michiels et al., ; Sparks et al., ). To date, several studies investigated potential functions of red fluorescence in fish, including intraspecific communication, camouflage, and prey detection (Anthes et al., ; Detecting the Detector; Harant & Michiels, ; Meadows et al., ).…”

“…The black‐faced triplefin Tripterygion delaisi possesses remarkably red fluorescent irides. Its fluorescence is among the strongest of all fish measured thus far (Anthes et al., ) and can be perceived by the human eye without the aid of an excitation source or the use of long‐pass viewing filters (Figure ). Yet, its fluorescence appears still weak relative to the ambient light.…”

Controlled iris radiance in a diurnal fish looking at prey

“…Rather than involving chemiluminescence, light emission originates from reflective and / or fluorescent irides [16][17][18][19]. Previously, we found that red fluorescent irides are most prevalent in small fish feeding on small, eyed prey [20], hinting at the possibility that light emission from the iris may constitute a visual aid in detection [21]. Indeed, one of those species captured more prey under "fluorescent-friendly" conditions in a subsequent experiment [22], even though the contribution of active photolocation to this finding remains to be shown.…”