Redirection of ambient light improves predator detection in a diurnal fish

Cases where animals use controlled illumination to improve vision are rare and thus far limited to chemiluminescence, which only functions in darkness. This constraint was recently relaxed by studies on Tripterygion delaisi , a small triplefin that redirects sunlight instead. By reflecting light sideways with its iris, it has been suggested to induce and detect eyeshine in nearby micro-prey. Here, we test whether ‘diurnal active photolocation’ also improves T. delaisi 's ability to detect the cryptobenthic sit-and-wait predator Scorpaena porcus, a scorpionfish with strong daytime retroreflective eyeshine. Three independent experiments revealed that triplefins in which light redirection was artificially suppressed approached scorpionfish significantly closer than two control treatments before moving away to a safer distance. Visual modelling confirmed that ocular light redirection by a triplefin is sufficiently strong to generate a luminance increase in scorpionfish eyeshine that can be perceived by the triplefin over 6–8 cm under average conditions. These distances coincide well with the closest approaches observed. We conclude that light redirection by small, diurnal fish significantly contributes to their ability to visually detect cryptic predators, strongly widening the conditions under which active sensing with light is feasible. We discuss the consequences for fish eye evolution.

Visual modelling supports the potential for prey detection by means of diurnal active photolocation in a small cryptobenthic fish

Active sensing has been well documented in animals that use echolocation and electrolocation. Active photolocation, or active sensing using light, has received much less attention, and only in bioluminescent nocturnal species. However, evidence has suggested the diurnal triplefin Tripterygion delaisi uses controlled iris radiance, termed ocular sparks, for prey detection. While this form of diurnal active photolocation was behaviourally described, a study exploring the physical process would provide compelling support for this mechanism. In this paper, we investigate the conditions under which diurnal active photolocation could assist T. delaisi in detecting potential prey. In the field, we sampled gammarids (genus Cheirocratus) and characterized the spectral properties of their eyes, which possess strong directional reflectors. In the laboratory, we quantified ocular sparks size and their angle-dependent radiance. Combined with environmental light measurements and known properties of the visual system of T. delaisi, we modeled diurnal active photolocation under various scenarios. Our results corroborate that diurnal active photolocation should help T. delaisi detect gammarids at distances relevant to foraging, 4.5 cm under favourable conditions and up to 2.5 cm under average conditions. Because ocular sparks are widespread across fish species, diurnal active photolocation for micro-prey may be a common predation strategy.

Controlled iris radiance in a diurnal fish looking at prey

Active sensing using light, or active photolocation, is only known from deep sea and nocturnal fish with chemiluminescent ‘search’ lights. Bright irides in diurnal fish species have recently been proposed as a potential analogue. Here, we contribute to this discussion by testing whether iris radiance is actively modulated. The focus is on behaviourally controlled iris reflections, called ‘ocular sparks’. The triplefin Tripterygion delaisi can alternate between red and blue ocular sparks, allowing us to test the prediction that spark frequency and hue depend on background hue and prey presence. In a first experiment, we found that blue ocular sparks were significantly more often ‘on’ against red backgrounds, and red ocular sparks against blue backgrounds, particularly when copepods were present. A second experiment tested whether hungry fish showed more ocular sparks, which was not the case. However, background hue once more resulted in a significant differential use of ocular sparks. We conclude that iris radiance through ocular sparks in T. delaisi is not a side effect of eye movement, but adaptively modulated in response to the context under which prey are detected. We discuss the possible alternative functions of ocular sparks, including an as yet speculative role in active photolocation.

Retinal specializations to a micro-predatory and crypto-benthic life-style in the Mediterranean triplefin blenny Tripterygion delaisi

The environment and lifestyle of a species are known to exert selective pressure on the visual system, often demonstrating a tight link between visual morphology and ecology. Many studies have predicted the visual requirements of a species by examining the anatomical features of the eye. However, among the vast number of studies on visual specializations in aquatic animals, only a few have focused on small benthic fishes that occupy a heterogeneous and spatially complex visual environment. This study investigates the general retinal anatomy including the topography of both the photoreceptor and ganglion cell populations and estimates the spatial resolving power of the eye of the Mediterranean triplefin Tripterygion delaisi. Retinal wholemounts were prepared to systematically and quantitatively analyze photoreceptor and retinal ganglion cell densities using design-based stereology. To further examine the retinal structure, we also used magnetic resonance imaging and histological examination of retinal cross sections. Observations of the triplefin's eyes revealed them to be highly mobile, allowing them to view the surroundings without body movements. A rostral aphakic gap and the elliptical shape of the eye extend its visual field rostrally and allow for a rostro-caudal accommodatory axis, enabling this species to focus on prey at close range. Single and twin cones dominate the retina and are consistently arranged in one of two regular patterns, which may enhance motion detection and color vision. The retina features a prominent, dorso-temporal, convexiclivate fovea with an average density of 104,400 double and 30,800 single cones per mm2, and 81,000 retinal ganglion cells per mm2. Based on photoreceptor spacing, spatial resolving power was calculated to be between 6.7 and 9.0 cycles per degree. Location and resolving power of the fovea would benefit the detection and identification of small prey in the lower frontal region of the visual field.

Controlled iris radiance in a diurnal fish looking at prey

1.SummaryActive sensing using light, or active photolocation, is only known from deep sea and nocturnal fish with chemiluminescent “search” lights. Bright irides in diurnal fish species have recently been proposed as a potential analogue. Here, we contribute to this discussion by testing whether iris radiance is actively modulated. The focus is on behaviourally controlled iris reflections, called “ocular sparks”. The triplefin Tripterygion delaisi can alternate between red and blue ocular sparks, allowing us to test the prediction that spark frequency and hue depend on background hue and prey presence. In a first experiment, we found that blue ocular sparks were significantly more often “on” against red backgrounds, and red ocular sparks against blue backgrounds, particularly when copepods were present. A second experiment tested whether hungry fish showed more ocular sparks, which was not the case. Again, background hue resulted in differential use of ocular spark types. We conclude that iris radiance through ocular sparks in T. delaisi is not a side effect of eye movement, but adaptively modulated in response to the context under which prey are detected. We discuss the possible alternative functions of ocular sparks, including an as yet speculative role in active photolocation.

Red fluorescence of the triplefin Tripterygion delaisi is increasingly visible against background light with increasing depth

The light environment in water bodies changes with depth due to the absorption of short and long wavelengths. Below 10 m depth, red wavelengths are almost completely absent rendering any red-reflecting animal dark and achromatic. However, fluorescence may produce red coloration even when red light is not available for reflection. A large number of marine taxa including over 270 fish species are known to produce red fluorescence, yet it is unclear under which natural light environment fluorescence contributes perceptively to their colours. To address this question we: (i) characterized the visual system of Tripterygion delaisi, which possesses fluorescent irides, (ii) separated the colour of the irides into its reflectance and fluorescence components and (iii) combined these data with field measurements of the ambient light environment to calculate depth-dependent perceptual chromatic and achromatic contrasts using visual modelling. We found that triplefins have cones with at least three different spectral sensitivities, including differences between the two members of the double cones, giving them the potential for trichromatic colour vision. We also show that fluorescence contributes increasingly to the radiance of the irides with increasing depth. Our results support the potential functionality of red fluorescence, including communicative roles such as species and sex identity, and non-communicative roles such as camouflage.

Rocky reef fish community structure in two Azorean islands (Portugal) central North Atlantic

The community structure of shallow rocky reef fish fauna of the Azores Archipelago is described from underwater visual censuses carried out at eight areas (Terceira and Corvo Islands). A total of 52 fish species from 26 different families was observed, and the ten most abundant fish corresponded to 82.7% of all fish. Trophic categories are given for observed species with comments on distribution and densities along sampled depth strata. Mean densities along sampled strata were tested for significant differences. Sparidae, Labridae and Carangidae were the most speciose families being Diplodus sargus, Pagellus acarne, Coris julis, Thalassoma pavo and Tripterygion delaisi the most abundant species that consequently also accounted for the highest densities.