Hiding opaque eyes in transparent organisms: a potential role for larval eyeshine in stomatopod crustaceans

Abstract

Opaque screening pigments are a fundamental requisite for preserving resolution in image-forming eyes. Possession of any type of image-forming eye in a transparent, pelagic animal will thus undermine the ability of that animal to be invisible in the water column. Transparent, pelagic animals must therefore deal with the trade-off between the ability to see and the ability of other animals to see them. Stomatopod larvae, like many transparent crustaceans, possess specialized optics in their compound eyes that minimize the volume of the opaque retina. Though the volumes of these retinas are reduced, their opacity remains conspicuous to an observer. The light reflected from structures overlying the retinas of stomatopod crustacean larval eyes, referred to here as eyeshine, is hypothesized to further reduce the visibility of opaque retinas. Blue or green wavelengths of light are most strongly reflected in stomatopod larval eyeshine, suggesting a putative spectral matching to the light environment against which the larval eyes are viewed. We tested the efficacy of stomatopod crustacean larval eyeshine as an ocular camouflaging mechanism by photographing larvae in their natural light environment and analysing the contrast of eyes with the background light. To test for spectral matching between stomatopod larval eyeshine and the background light environment, we characterized the spectrum of eyeshine and calculated its performance using radiometric measurements collected at the time of each photographic series. These results are the first to demonstrate an operative mirror camouflage matched in both spectrum and radiance to the pelagic background light environment.

Evolution of crab eye structures and the utility of ommatidia morphology in resolving phylogeny

“…Larval apposition optics are specialized for open water habitats, and are thought to provide as much camouflage (predator avoidance) to the larva as possible by decreasing the pigmented portion of the retina to minimize its diameter. This results in a 'clear zone' between the cones and the rhabdom, thus the larval apposition eye functionally mimics a superposition eye (Gaten, 1998;Feller and Cronin, 2014). At metamorphosis into the 745!…”

Selection of the intrinsic polarization properties of animal optical materials creates enhanced structural reflectivity and camouflage

“…Typically the high, n o , refractive index values are orientated in the broad planes of the crystal (Type 1), but sometimes the n e value is orientated in the broad plane (Type 2).[48,51,52]chitin—beetlesThe chitin fibrils embedded in a protein matrix are uniaxial with refractive indices of n o = 1.70 and n e = 1.54[2,28,53,54] intrinsic anisotropy —chiralitychitin—beetles[2,25,28,55–57]chitin—crustaceansHelical progression of chitin layers found in arthropod cuticles—an oblique cut demonstrates the nested arcs / Bouligand planes[58,59]chitin—butterflyIn many lepidopteron scales Chitin can also form a variety of minimum energy surfaces such as single gyroids.[60–63] form birefringence Form anisotropy occurs when the length scale of individual components is less than the wavelength of the light but the overall size is much greater than the wavelength.chitin—butterflies[64]chitin—OrthopteranThe assembly behaves as a positive uniaxial crystal where the optic axis is perpendicular to the plane of the plates.[65] Structural anisotropy Structural anisotropy occurs when the length scale of anisotropy is comparable to the wavelength of light. At this scale, the polarization of reflected light is controlled by asymmetric scattering and interference/diffraction (rather than anisotropy in the refractive index).anisotropic vesicles—stomatopodsHollow ovoid vesicles with aspect ratios of 2–3 found in the maxilliped cuticle[44]diffraction gratings—insectsDiffraction grating is periodic in the x-direction.[2,4,66]…”

“…Animals use structural optics to produce highly reflective coloration [1–4]. Many of these optical structures follow well-understood physics [5]; however, there are also several examples where no synthetic analogues exist [6].…”

Controlled iris radiance in a diurnal fish looking at prey

“…The anatomical location of the light organ next to the pupil is optimal to induce reflective eyeshine (bright pupils or "cat's eyes" effect) in nearby organisms [2]. Reflective eyeshine is a side-effect of the presence of a reflective layer at the back of the eye [10] (ESM 1), which improves vision under dim light [11,12] or plays a role in camouflage [13]. With such a reflective layer present, focusing eyes in particular backscatter or reflect the incoming light directly back to the source [14].…”

“…Many fish show bright eyes due to luminescent mechanisms such as chemiluminescence in nocturnal fish(1) or fluorescence in diurnal fish(2). Many more species show forms of reflection off the iris(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16) or cornea(17)(18). This study focuses on so-called "ocular sparks", a mechanism where fish focus downwelling light onto their own iris(19-22, see figure 2) (species names in ESM 2, photos by N.K.M.).…”