Functional differences between the extraordinary eyes of deep-sea hyperiid amphipods.

The ocean's midwater is a uniquely challenging yet predictable and simple visual environment. The need to see without being seen in this dim, open habitat has led to extraordinary visual adaptations. To understand these adaptations, we compared the morphological and functional differences between the eyes of three hyperiid amphipods-Hyperia galba, Streetsia challengeri and Phronima sedentaria. Combining micro-CT data with computational modelling, we mapped visual field topography and predicted detection distances for visual targets viewed in different directions through mesopelagic depths. Hyperia's eyes provide a wide visual field optimized for spatial vision over short distances, while Phronima's and Streetsia's eyes have the potential to achieve greater sensitivity and longer detection distances using spatial summation. These improvements come at the cost of smaller visual fields, but this loss is compensated for by a second pair of eyes in Phronima and by behaviour in Streetsia. The need to improve sensitivity while minimizing visible eye size to maintain crypsis has likely driven the evolution of hyperiid eye diversity. Our results provide an integrative look at how these elusive animals have adapted to the unique visual challenges of the mesopelagic.

Composite material in the sea urchin Cidaris rugosa: ordered and disordered micrometre-scale bicontinuous geometries.

The sponge-like biomineralized calcite materials found in echinoderm skeletons are of interest in terms of both structure formation and biological function. Despite their crystalline atomic structure, they exhibit curved interfaces that have been related to known triply periodic minimal surfaces. Here, we investigate the endoskeleton of the sea urchin Cidaris rugosa that has long been known to form a microstructure related to the Primitive surface. Using X-ray tomography, we find that the endoskeleton is organized as a composite material consisting of domains of bicontinuous microstructures with different structural properties. We describe, for the first time, the co-occurrence of ordered single Primitive and single Diamond structures and of a disordered structure within a single skeletal plate. We show that these structures can be distinguished by structural properties including solid volume fraction, trabeculae width and, to a lesser extent, interface area and mean curvature. In doing so, we present a robust method that extracts interface areas and curvature integrals from voxelized datasets using the Steiner polynomial for parallel body volumes. We discuss these very large-scale bicontinuous structures in the context of their function, formation and evolution.

A new computational model illuminates the extraordinary eyes of Phronima.

Vision in the midwater of the open ocean requires animals to perform visual tasks quite unlike those of any other environment. These tasks consist of detecting small, low contrast objects and point sources against a relatively dim and uniform background. Deep-sea animals have evolved many extraordinary visual adaptations to perform these tasks. Linking eye anatomy to specific selective pressures, however, is challenging, not least because of the many difficulties of studying deep-sea animals. Computational modelling of vision, based on detailed morphological reconstructions of animal eyes, along with underwater optics, offers a chance to understand the specific visual capabilities of individual visual systems. Prior to the work presented here, comprehensive models for apposition compound eyes in the mesopelagic, the dominant eye form of crustaceans, were lacking. We adapted a model developed for single-lens eyes and used it to examine how different parameters affect the model's ability to detect point sources and extended objects. This new model also allowed us to examine spatial summation as a means to improve visual performance. Our results identify a trade-off between increased depth range over which eyes function effectively and increased distance at which extended objects can be detected. This trade-off is driven by the size of the ommatidial acceptance angle. We also show that if neighbouring ommatidia have overlapping receptive fields, spatial summation helps with all detection tasks, including the detection of bioluminescent point sources. By applying our model to the apposition compound eyes of Phronima, a mesopelagic hyperiid amphipod, we show that the specialisations of the large medial eyes of Phronima improve both the detection of point sources and of extended objects. The medial eyes outperformed the lateral eyes at every modelled detection task. We suggest that the small visual field size of Phronima's medial eyes and the strong asymmetry between the medial and lateral eyes reflect Phronima's need for effective vision across a large depth range and its habit of living inside a barrel. The barrel's narrow aperture limits the usefulness of a large visual field and has allowed a strong asymmetry between the medial and lateral eyes. The model provides a useful tool for future investigations into the visual abilities of apposition compound eyes in the deep sea.

Photoreceptors and diurnal variation in spectral sensitivity in the fiddler crab Gelasimus dampieri.

Colour signals, and the ability to detect them, are important for many animals and can be vital to their survival and fitness. Fiddler crabs use colour information to detect and recognise conspecifics, but their colour vision capabilities remain unclear. Many studies have attempted to measure their spectral sensitivity and identify contributing retinular cells, but the existing evidence is inconclusive. We used electroretinogram (ERG) measurements and intracellular recordings from retinular cells to estimate the spectral sensitivity of Gelasimus dampieri and to track diurnal changes in spectral sensitivity. G. dampieri has a broad spectral sensitivity and is most sensitive to wavelengths between 420 and 460 nm. Selective adaptation experiments uncovered an ultraviolet (UV) retinular cell with a peak sensitivity shorter than 360 nm. The species' spectral sensitivity above 400 nm is too broad to be fitted by a single visual pigment and using optical modelling, we provide evidence that at least two medium-wavelength sensitive (MWS) visual pigments are contained within a second blue-green sensitive retinular cell. We also found a ∼25 nm diurnal shift in spectral sensitivity towards longer wavelengths in the evening in both ERG and intracellular recordings. Whether the shift is caused by screening pigment migration or changes in opsin expression remains unclear, but the observation shows the diel dynamism of colour vision in this species. Together, these findings support the notion that G. dampieri possesses the minimum requirement for colour vision, with UV and blue/green receptors, and help to explain some of the inconsistent results of previous research.

A new method for mapping spatial resolution in compound eyes suggests two visual streaks in fiddler crabs.

Visual systems play a vital role in guiding the behaviour of animals. Understanding the visual information animals are able to acquire is therefore key to understanding their visually mediated decision making. Compound eyes, the dominant eye type in arthropods, are inherently low-resolution structures. Their ability to resolve spatial detail depends on sampling resolution (interommatidial angle) and the quality of ommatidial optics. Current techniques for estimating interommatidial angles are difficult, and generally require in vivo measurements. Here, we present a new method for estimating interommatidial angles based on the detailed analysis of 3D micro-computed tomography images of fixed samples. Using custom-made MATLAB software, we determined the optical axes of individual ommatidia and projected these axes into the 3D space around the animal. The combined viewing directions of all ommatidia, estimated from geometrical optics, allowed us to estimate interommatidial angles and map the animal's sampling resolution across its entire visual field. The resulting topographic representations of visual acuity match very closely the previously published data obtained from both fiddler and grapsid crabs. However, the new method provides additional detail that was not previously detectable and reveals that fiddler crabs, rather than having a single horizontal visual streak as is common in flat-world inhabitants, probably have two parallel streaks located just above and below the visual horizon. A key advantage of our approach is that it can be used on appropriately preserved specimens, allowing the technique to be applied to animals such as deep-sea crustaceans that are inaccessible or unsuitable for in vivo approaches.