Biology subjects

Michiels, N. K.

Publications and source records attributed to Michiels, N. K..

7 recordsLinked to original sources

bioRxiv2018

Visual modelling validates 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. Recently, 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 complete physical and theoretical process would provide a more compelling case supporting this mechanism. In this paper, we investigate the conditions under which diurnal active photolocation could assist T. delaisi in detecting potential prey items. In the field, we sampled prey gammarids (Genus Cheirocratus) from foraging substrates, and characterized the spectral properties of their body and eyes, which possess strong reflectors between the ommatidia. In the laboratory, we quantified ocular spark sizes and the angular dependence of their radiance. Together with environmental light measurements and the visual properties of T. delaisi, we modeled diurnal active photolocation under various scenarios. Our results corroborate that diurnal active photolocation can 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 many different fish species, diurnal active photolocation for micro-prey may be a common predation strategy.

zoology↗

bioRxiv2018

Diurnal active photolocation enhances predator detection in a marine fish

Active sensing by means of light is rare. In vertebrates, it is known only from chemiluminescent fish with light organs below their pupils, an anatomical arrangement that is ideal to generate eyeshine in the pupils of nearby organisms. Here, we test whether diurnal fish can achieve the same by redirecting sunlight through reflection instead. We recently showed that small (< 5 cm), benthic, marine triplefin fish actively redirect downwelling light using their iris. We hypothesized that this mechanism allows triplefins to improve detection of a cryptic organism by generating eyeshine in its pupil. Here, we tested this by attaching small dark hats to triplefins to shade their iris from downwelling light. Two controls consisted of triplefins with a clear or no hat. These treatments test the prediction that light redirection increases the visual detection ability of triplefins. To this end, we placed treated fish in a tank with a display compartment containing either a stone as the control stimulus, or a scorpionfish, i.e. a cryptic, motionless triplefin predator with retroreflective eyes. After overnight acclimatization, we determined the average distance triplefins kept from the display compartment over two days. Both in the laboratory (n = 15 replicates per treatment) and in a similar field experiment at 15 m depth (n = 43 replicates per treatment) fish kept longer distances from the scorpionfish than from the stone. This response varied between hat treatments: shaded triplefins stayed significantly closer to the scorpionfish in the laboratory and in one of two orientations tested in the field. A follow-up field experiment at 10 m depth revealed the immediate response of triplefins to a scorpionfish. At first, many individuals (n = 80) moved towards it, with shaded triplefins getting significantly closer. All individuals then gradually moved to a safer distance at the opposite half of the tank. Visual modelling supported the experimental results by showing that triplefins can redirect enough light with their iris to increase a scorpionfishs pupil brightness above detection threshold at a distance of 7 cm under average field conditions and at more than 12 cm under favorable conditions. We conclude that triplefins are generally good in the visual detection of a cryptic predator, but can significantly improve this ability when able to redirect downwelling light with their iris and induce eyeshine in the predators pupil. We discuss the consequences of \"diurnal active photolocation\" for visual detection and camouflage among fish species.

zoology↗

bioRxiv2018

Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton

Ciliary and rhabdomeric photoreceptor cells represent two main lines of photoreceptor evolution in animals. The two photoreceptor-cell types coexist in some animals, however how they functionally integrate is unknown. We used connectomics to map synaptic paths between ciliary and rhabdomeric photoreceptors in the planktonic larva of the annelid Platynereis and found that ciliary photoreceptors are presynaptic to the rhabdomeric circuit. The behaviors mediated by the ciliary and rhabdomeric cells also interact hierarchically. The ciliary photoreceptors are UV-sensitive and mediate downward swimming to non-directional UV light, a behavior absent in ciliary-opsin knockouts. UV avoidance antagonizes positive phototaxis mediated by the rhabdomeric eyes so that vertical swimming direction is determined by the ratio of blue/UV light. Since this ratio increases with depth, Platynereis larvae may use it as a depth gauge during planktonic migration. Our results revealed a functional integration of ciliary and rhabdomeric photoreceptors with implications for eye and photoreceptor evolution.

neuroscience↗

bioRxiv2017

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.

animal behavior and cognition↗

bioRxiv2017

Controlled ocular radiance in a diurnal fish looking at prey

1.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. 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.

animal behavior and cognition↗

bioRxiv2017

Does red eye fluorescence in marine fish stand out? In situ and in vivo measurements at two depths

Since the discovery of red fluorescence in fish, much effort has been made to elucidate its potential contribution to vision. However, whatever that function might be, it always implies that the combination of red fluorescence and reflectance of the red iris is sufficient to generate a visual contrast. Here, we present in vivo iris radiance measurements of T. delaisi under natural light fields at 5 and 20 m depth. We also took substrate radiance measurements of shaded and exposed foraging sites at those depths. To assess the visual contrast that can be generated by the red iris, we then calculated iris brightness in the 600-650 nm \"red\" waveband relative to substrate radiance. At 20 m depth, T. delaisi iris radiance substantially exceeded substrate radiance in the red waveband, regardless of exposure, and despite substrate fluorescence. Given that downwelling light in the 600-650 nm range is negligible at this depth, we can attribute this effect to iris fluorescence. As expected, contrasts were much weaker in 5 m - despite the added contribution of iris reflectance, but we identified specific substrates and conditions under which the pooled radiance caused by red reflectance and fluorescence still exceeded substrate radiance in the same waveband. Due to the negative effect of anesthesia on iris fluorescence these estimates are conservative. We conclude that the requirements to create visual brightness contrasts are fulfilled for a wide range of conditions in the natural environment of T. delaisi.

ecology↗

bioRxiv2017

Daytime eyeshine contributes to pupil camouflage in a cryptobenthic marine fish

Ocular reflectors enhance eye sensitivity in dim light, but can produce reflected eyeshine when illuminated. Most teleost fish occlude their reflectors during the day. The opposite is observed in cryptic sit-and-wait predators such as scorpionfish and toadfish, where reflectors are occluded at night and exposed during the day. This results in daytime eyeshine, proposed to enhance pupil camouflage by reducing the contrast between the otherwise black pupil and the surrounding tissue. In this study, we test this hypothesis in the scorpionfish Scorpaena porcus and show that eyeshine is the result of two mechanisms: the previously described Stratum Argenteum Reflected (SAR) eyeshine, and Pigment Epithelium Transmitted (PET) eyeshine, a newly described mechanism for this species. We confirm that the ocular reflector is exposed only when the eye is light-adapted, and present field measurements to show that eyeshine reduces pupil contrast against the iris. We then estimate the relative contribution of SAR and PET eyeshine to pupil brightness. Visual models for different light scenarios in the field show that daytime eyeshine enhances pupil camouflage from the perspective of a prey fish. We propose that the reversed occlusion mechanism of some cryptobenthic predators has evolved as a compromise between camouflage and vision.

evolutionary biology↗