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Sponges are animals that inhabit many aquatic environments while filtering small particles and ejecting metabolic wastes. They are composed of cells in a bulk extracellular matrix, often with an embedded scaffolding of stiff, siliceous spicules. We hypothesize that the mechanical response of this heterogeneous tissue to hydrodynamic flow influences cell proliferation in a manner that generates the body of a sponge. Towards a more complete picture of the emergence of sponge morphology, we dissected a set of species and subjected discs of living tissue to physiological shear and uniaxial deformations on a rheometer. Various species exhibited rheological properties such as anisotropic elasticity, shear softening and compression stiffening, negative normal stress, and non-monotonic dissipation as a function of both shear strain and frequency. Erect sponges possessed aligned, spicule-reinforced fibres which endowed three times greater stiffness axially compared with orthogonally. By contrast, tissue taken from shorter sponges was more isotropic but time-dependent, suggesting higher flow sensitivity in these compared with erect forms. We explore ecological and physiological implications of our results and speculate about flow-induced mechanical signalling in sponge cells.

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., (© 2017 The Authors.)

Galiteuthis, a midwater squid, has photophores on the ventral surfaces of its eyes. These photophores emit bioluminescence to counter-illuminate the shadows cast by the eyes in downwelling sunlight, thereby hiding the eyes from upward-looking predators. The photophores consist of laminated fibre-like cells with semi-coaxial protein-dense layers around axial cytoplasm. These cells have been suggested to function as light guides: bioluminescence is an isotropic process used to hide in an anisotropic light environment, so any emission must be reshaped to be effective. We found a wide variation in cross-sectional geometries of photophore cells; some were more efficient at light guiding than others. We used a set of optical models to place these photophores in the context of the radiance where Galiteuthis lives and discovered a possible adaptive reason for this variation. In Galiteuthis's horizontal and vertical range, ocean radiance is also quite variable. For complete camouflage, photophores must reproduce this variation in radiance using an isotropic source. Our models show that variation in the geometry of the photophore light guides reproduces the predicted variation in ocean radiance experienced by this species. By selectively activating geometrically distinct populations of photophore cells, the animal may reproduce the angular distribution of light at all positions in its habitat., (© 2016 The Author(s).)

'Giant' tridacnid clams have evolved a three-dimensional, spatially efficient, photodamage-preventing system for photosymbiosis. We discovered that the mantle tissue of giant clams, which harbours symbiotic nutrition-providing microalgae, contains a layer of iridescent cells called iridocytes that serve to distribute photosynthetically productive wavelengths by lateral and forward-scattering of light into the tissue while back-reflecting non-productive wavelengths with a Bragg mirror. The wavelength- and angle-dependent scattering from the iridocytes is geometrically coupled to the vertically pillared microalgae, resulting in an even re-distribution of the incoming light along the sides of the pillars, thus enabling photosynthesis deep in the tissue. There is a physical analogy between the evolved function of the clam system and an electric transformer, which changes energy flux per area in a system while conserving total energy. At incident light levels found on shallow coral reefs, this arrangement may allow algae within the clam system to both efficiently use all incident solar energy and avoid the photodamage and efficiency losses due to non-photochemical quenching that occur in the reef-building coral photosymbiosis. Both intra-tissue radiometry and multiscale optical modelling support our interpretation of the system's photophysics. This highly evolved 'three-dimensional' biophotonic system suggests a strategy for more efficient, damage-resistant photovoltaic materials and more spatially efficient solar production of algal biofuels, foods and chemicals.

Cephalopods possess a sophisticated array of mechanisms to achieve camouflage in dynamic underwater environments. While active mechanisms such as chromatophore patterning and body posturing are well known, passive mechanisms such as manipulating light with highly evolved reflectors may also play an important role. To explore the contribution of passive mechanisms to cephalopod camouflage, we investigated the optical and biochemical properties of the silver layer covering the eye of the California fishery squid, Loligo opalescens. We discovered a novel nested-spindle geometry whose correlated structure effectively emulates a randomly distributed Bragg reflector (DBR), with a range of spatial frequencies resulting in broadband visible reflectance, making it a nearly ideal passive camouflage material for the depth at which these animals live. We used the transfer-matrix method of optical modelling to investigate specular reflection from the spindle structures, demonstrating that a DBR with widely distributed thickness variations of high refractive index elements is sufficient to yield broadband reflectance over visible wavelengths, and that unlike DBRs with one or a few spatial frequencies, this broadband reflectance occurs from a wide range of viewing angles. The spindle shape of the cells may facilitate self-assembly of a random DBR to achieve smooth spatial distributions in refractive indices. This design lends itself to technological imitation to achieve a DBR with wide range of smoothly varying layer thicknesses in a facile, inexpensive manner.

Many cephalopods exhibit remarkable dermal iridescence, a component of their complex, dynamic camouflage and communication. In the species Euprymna scolopes, the light-organ iridescence is static and is due to reflectin protein-based platelets assembled into lamellar thin-film reflectors called iridosomes, contained within iridescent cells called iridocytes. Squid in the family Loliginidae appear to be unique in which the dermis possesses a dynamic iridescent component with reflective, coloured structures that are assembled and disassembled under the control of the muscarinic cholinergic system and the associated neurotransmitter acetylcholine (ACh). Here we present the sequences and characterization of three new members of the reflectin family associated with the dynamically changeable iridescence in Loligo and not found in static Euprymna iridophores. In addition, we show that application of genistein, a protein tyrosine kinase inhibitor, suppresses ACh- and calcium-induced iridescence in Loligo. We further demonstrate that two of these novel reflectins are extensively phosphorylated in concert with the activation of iridescence by exogenous ACh. This phosphorylation and the correlated iridescence can be blocked with genistein. Our results suggest that tyrosine phosphorylation of reflectin proteins is involved in the regulation of dynamic iridescence in Loligo.

A lens with a graded refractive index is required for vision in aquatic animals with camera-type eyes. This optical design entails a radial gradient of protein density, with low density in external layers and high density in internal layers. To maintain the optical stability of the eye, different material properties are required for proteins in different regions of the lens. In low-density regions of the lens where slight protein aggregation causes significant light scattering, aggregation must be minimized. Squid lens S-crystallin proteins are evolutionarily derived from the glutathione S-transferase protein family. We used biochemistry, optical modelling and phylogenetics to study the evolution and material properties of S-crystallins. S-crystallins are differentially expressed in a radial gradient, suggesting a role in refractive index. This gradient in S-crystallin expression is correlated with their evolutionary history and biochemistry. S-crystallins have been under positive selection. This selection appears to have resulted in stabilization of derived S-crystallins via mutations in the dimer interface and extended electrostatic fields. These derived S-crystallins probably cause the glassy organization and stability of low refractive index lens layers. Our work elucidates the molecular and evolutionary mechanisms underlying the production and maintenance of camera-like optics in squid lenses.