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Three-dimensional Midwater Camouflage From a Novel Two-Component Photonic Structure in Hatchetfish Skin

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Three-dimensional Midwater Camouflage From a Novel Two-Component Photonic Structure in Hatchetfish Skin

Eric I Rosenthal et al. J R Soc Interface.

Abstract

The largest habitat by volume on Earth is the oceanic midwater, which is also one of the least understood in terms of animal ecology. The organisms here exhibit a spectacular array of optical adaptations for living in a visual void that have only barely begun to be described. We describe a complex pattern of broadband scattering from the skin of Argyropelecus sp., a hatchetfish found in the mesopelagic zone of the world's oceans. Hatchetfish skin superficially resembles the unpolished side of aluminium foil, but on closer inspection contains a complex composite array of subwavelength-scale dielectric structures. The superficial layer of this array contains dielectric stacks that are rectangular in cross-section, while the deeper layer contains dielectric bundles that are elliptical in cross-section; the cells in both layers have their longest dimension running parallel to the dorsal-ventral axis of the fish. Using the finite-difference time-domain approach and photographic radiometry, we explored the structural origins of this scattering behaviour and its environmental consequences. When the fish's flank is illuminated from an arbitrary incident angle, a portion of the scattered light exits in an arc parallel to the fish's anterior-posterior axis. Simultaneously, some incident light is also scattered downwards through the complex birefringent skin structure and exits from the ventral photophores. We show that this complex scattering pattern will provide camouflage simultaneously against the horizontal radially symmetric solar radiance in this habitat, and the predatory bioluminescent searchlights that are common here. The structure also directs light incident on the flank of the fish into the downwelling, silhouette-hiding counter-illumination of the ventral photophores.

Keywords: bioluminescence; biophotonics; camouflage; midwater ecology; optical modelling.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1.
Figure 1.
Images of hatchetfish and photonic skin structures. (a) Photograph of the lateral aspect of a hatchetfish showing the general anatomy including ventral photophores, and appearance of the fish in diffuse lighting. (b) Darkfield reflected-light micrograph of hatchetfish skin and diagram of cell types within the skin. Individual skin cells appear as reflective wire-like structures with long axes running vertically. Exploded view shows the relative orientation of the two distinct layers and cell types within the skin, and also with respect to the X- and Y-planes used to describe and model this structure. (c) Overview transmission electron micrograph (TEM) showing both layers of skin cells sectioned in the X-plane. (d) Detail TEM of the elliptical-bundle cells of the deeper layer, sectioned in the X-plane. (e) Detail TEM of the rectangular-bundle cells of the superficial skin layer. (f) Detail TEM of both layers of the skin sectioned in the Y-plane, showing that both cell types shown in cross-section in the X-plane are tens of microns long when sectioned along their longest axis.
Figure 2.
Figure 2.
Reflectance distribution functions for hatchetfish skin and related structures. (a) Bidirectional reflectance distribution function (BRDF) of hatchetfish skin and definition of incident and scattering angles, as measured by Haag et al. [14]. Units along the intensity axis are arbitrary, and remain arbitrary in all panels in this figure. Small black circle shows the direction of the incident beam. (b) Reflectance distributions of hatchetfish skin along planes parallel and perpendicular to the ‘scattering arc’ where most reflected energy is directed by the fish skin, approximately described by θo = −20° to 20° and φo = 0° or 180° (blue line), and θo = −20° to 20° and φo = 90° or 270° (red line). (c) Backscattering from ellipses similar in size and shape to the X cross-sectional planes of cells found in hatchetfish skin. Dashed lines show backscatter from 2 µm long ellipses, analogous to backscatter from the cells in the deeper layer. Solid lines show backscatter from 7 µm long ellipses, analogous to backscatter from superficial-layer cells. (d) Backscattering from rectangles similar in size and shape to the X cross-sectional planes of cells found in hatchetfish skin. Dashed lines show backscatter from 2 µm long ellipses, analogous to backscatter from the cells in the deeper layer. Solid lines show backscatter from 7 µm long ellipses, analogous to backscatter from superficial-layer cells in the top layer. Integrated backscatter is roughly the same intensity as in panel (c). (e) Backscattering from rectangles and ellipses similar in size and shape to the cells sectioned along the Y-plane in both superficial and deep layers. Dashed lines show backscatter from 25 µm long rectangles, and solid lines show backscatter from 25 µm long ellipses.
Figure 3.
Figure 3.
FDTD calculations of scattering as a function of wavelength from cross-sections of ellipses and complex cells from the superficial and deep layers of hatchetfish skin. (a) Snapshots of electric fields as calculated by FDTD interacting with cross-sections of shapes, analogous to the cells in hatchetfish skin and with cross-sections of the subwavelength structures present in these cells. Arrows show the angle of incidence of the plane-wave source. From left to right: elliptical cross-section analogous to deep-layer cells in the X-plane; elliptical cross-section analogous to superficial-layer cells in the X-plane; cross-section of the subcellular structure of a deep-layer cell; cross-section of the subcellular structure of a superficial-layer cell. (b) Wavelength-dependent phase functions of the structures in (a). Curves show radial coordinates of scattering intensity as calculated by the FDTD method at 750 nm (red), 650 nm (orange), 550 nm (green), and 450 nm (blue).
Figure 4.
Figure 4.
Three-dimensional FDTD analysis of the full complexity hatchetfish skin structure. (a) Schematic showing TEM images, binary image representations of hatchetfish skin structure, and spatial dimensions of the coordinates used in our FDTD model. In the model, a Gaussian source (width 1 µm) was incident on the plane indicated. (b) Flux calculated along detection planes placed parallel to the X-axis as defined in (a) (blue line) and along the Y-axis as defined in (a) (red line). Even in the near field, flux is more widely distributed along the X-axis than along the Y-axis, and is in general consistent with multiple scattering from the two-dimensional structures examined above.
Figure 5.
Figure 5.
Visibility of hatchetfish skin in the oceanic midwater. (a) Ratio of BRDFs for a metallic mirror and the hatchetfish. The pattern in the plane of the page is defined in the same manner as figure 2a, while the intensity axis represents the ratio of the BRDF intensity of a metallic mirror versus that of the hatchetfish skin. The ratio of the brightest point in the hatchetfish BRDF compared with the mirror BRDF represents the relative brightness of light returning to a searchbeam predator's eye. (b) Relationship of sighting distance as a function of number of photons emitted from a searchlight, shown for both a completely collimated searchbeam (red curve) and a hemi-isotropic searchbeam (blue curve). The circle at the intersection of the two curves represents the sighting distance of a mirror given a searchlight intensity of 1010 photons. The red and blue circles show the sighting distance of the hatchetfish given a 20-fold reduction in intensity of the directly reflected beam, as shown in (a). The orange and blue bars represent absolute reduction in sighting distance of the hatchetfish relative to a mirror for a searchlight intensity of 1010 photons.
Figure 6.
Figure 6.
Visibility of various non-absorbing surfaces illuminated by a collimated searchbeam. (a) Bar graphs showing average intensities of pixels in exposure-normalized images of a set of non-absorbing surfaces of different BRDF. Left set shows images and average pixel intensities of the surfaces with the source incident normal to the surface and the detector viewing at a 30° angle from normal to the surface. Right set shows the image that is formed when both the detector and the source are pointed normal to the surface. Hatchetfish is shown in dark blue, dull aluminium is shown in light blue, a mirror is shown in green, and Spectralon is in yellow. Central section shows enlarged detail of images in the bar graphs. Surface types are indicated by the colours of the image borders as in left section. (b) Top, schematic of overall fish scattering showing how a searchbeam (red arrow) is backscattered lateral to the fish (blue wedge) as well as ventrally through the photophores (blue circles). Bottom, photograph with inset detail (orange box) of a beam incident on the lateral flank of the fish exiting the fish through the ventral photophores.

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