Colour vision in stomatopod crustaceans.

The stomatopod crustaceans, or mantis shrimps, are colourful marine invertebrate predators. Their unusual compound eyes have dorsal and ventral regions resembling typical crustacean apposition designs separated by a unique region called the midband that consists of from two to six parallel rows of ommatidia. In species with six-row midbands, the dorsal four rows are themselves uniquely specialized for colour analysis. Rhabdoms of ommatidia in these rows are longitudinally divided into three distinct regions: an apical ultraviolet (UV) receptor, a shorter-wavelength middle tier receptor and a longer-wavelength proximal tier receptor. Each of the total of 12 photoreceptors has a different spectral sensitivity, potentially contributing to a colour-vision system with 12 channels. Mantis shrimps can discriminate both human-visible and UV colours, but with limited precision compared to other colour-vision systems. Here, we review the structure and function of stomatopod colour vision, examining the types of receptors present in a species, the spectral tuning of photoreceptors both within and across species, the neural analysis of colour and the genetics underlying the multiple visual pigments used for colour vision. Even today, after many decades of research into the colour vision of stomatopods, much of its operation and its use in nature remain a mystery. This article is part of the theme issue 'Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods'.

Polarisation signals: a new currency for communication.

Most polarisation vision studies reveal elegant examples of how animals, mainly the invertebrates, use polarised light cues for navigation, course-control or habitat selection. Within the past two decades it has been recognised that polarised light, reflected, blocked or transmitted by some animal and plant tissues, may also provide signals that are received or sent between or within species. Much as animals use colour and colour signalling in behaviour and survival, other species additionally make use of polarisation signalling, or indeed may rely on polarisation-based signals instead. It is possible that the degree (or percentage) of polarisation provides a more reliable currency of information than the angle or orientation of the polarised light electric vector (e-vector). Alternatively, signals with specific e-vector angles may be important for some behaviours. Mixed messages, making use of polarisation and colour signals, also exist. While our knowledge of the physics of polarised reflections and sensory systems has increased, the observational and behavioural biology side of the story needs more (and more careful) attention. This Review aims to critically examine recent ideas and findings, and suggests ways forward to reveal the use of light that we cannot see.

A shape-anisotropic reflective polarizer in a stomatopod crustacean.

Many biophotonic structures have their spectral properties of reflection 'tuned' using the (zeroth-order) Bragg criteria for phase constructive interference. This is associated with a periodicity, or distribution of periodicities, parallel to the direction of illumination. The polarization properties of these reflections are, however, typically constrained by the dimensional symmetry and intrinsic dielectric properties of the biological materials. Here we report a linearly polarizing reflector in a stomatopod crustacean that consists of 6-8 layers of hollow, ovoid vesicles with principal axes of ~550 nm, ~250 nm and ~150 nm. The reflection of unpolarized normally incident light is blue/green in colour with maximum reflectance wavelength of 520 nm and a degree of polarization greater than 0.6 over most of the visible spectrum. We demonstrate that the polarizing reflection can be explained by a resonant coupling with the first-order, in-plane, Bragg harmonics. These harmonics are associated with a distribution of periodicities perpendicular to the direction of illumination, and, due to the shape-anisotropy of the vesicles, are different for each linear polarization mode. This control and tuning of the polarization of the reflection using shape-anisotropic hollow scatterers is unlike any optical structure previously described and could provide a new design pathway for polarization-tunability in man-made photonic devices.

Behavior and Body Patterns of the Larger Pacific Striped Octopus.

Over thirty years ago anecdotal accounts of the undescribed Larger Pacific Striped Octopus suggested behaviors previously unknown for octopuses. Beak-to-beak mating, dens shared by mating pairs, inking during mating and extended spawning were mentioned in publications, and enticed generations of cephalopod biologists. In 2012-2014 we were able to obtain several live specimens of this species, which remains without a formal description. All of the unique behaviors listed above were observed for animals in aquaria and are discussed here. We describe the behavior, body color patterns, and postures of 24 adults maintained in captivity. Chromatophore patterns of hatchlings are also shown.

Out of the blue: the evolution of horizontally polarized signals in Haptosquilla (Crustacea, Stomatopoda, Protosquillidae).

The polarization of light provides information that is used by many animals for a number of different visually guided behaviours. Several marine species, such as stomatopod crustaceans and cephalopod molluscs, communicate using visual signals that contain polarized information, content that is often part of a more complex multi-dimensional visual signal. In this work, we investigate the evolution of polarized signals in species of Haptosquilla, a widespread genus of stomatopod, as well as related protosquillids. We present evidence for a pre-existing bias towards horizontally polarized signal content and demonstrate that the properties of the polarization vision system in these animals increase the signal-to-noise ratio of the signal. Combining these results with the increase in efficacy that polarization provides over intensity and hue in a shallow marine environment, we propose a joint framework for the evolution of the polarized form of these complex signals based on both efficacy-driven (proximate) and content-driven (ultimate) selection pressures.

A dynamic broadband reflector built from microscopic silica spheres in the 'disco' clam Ctenoides ales.

The 'disco' or 'electric' clam Ctenoides ales (Limidae) is the only species of bivalve known to have a behaviourally mediated photic display. This display is so vivid that it has been repeatedly confused for bioluminescence, but it is actually the result of scattered light. The flashing occurs on the mantle lip, where electron microscopy revealed two distinct tissue sides: one highly scattering side that contains dense aggregations of spheres composed of silica, and one highly absorbing side that does not. High-speed video confirmed that the two sides act in concert to alternate between vivid broadband reflectance and strong absorption in the blue region of the spectrum. Optical modelling suggests that the diameter of the spheres is nearly optimal for scattering visible light, especially at shorter wavelengths which predominate in their environment. This simple mechanism produces a striking optical effect that may function as a signal.

Filtering and polychromatic vision in mantis shrimps: themes in visible and ultraviolet vision.

Stomatopod crustaceans have the most complex and diverse assortment of retinal photoreceptors of any animals, with 16 functional classes. The receptor classes are subdivided into sets responsible for ultraviolet vision, spatial vision, colour vision and polarization vision. Many of these receptor classes are spectrally tuned by filtering pigments located in photoreceptors or overlying optical elements. At visible wavelengths, carotenoproteins or similar substances are packed into vesicles used either as serial, intrarhabdomal filters or lateral filters. A single retina may contain a diversity of these filtering pigments paired with specific photoreceptors, and the pigments used vary between and within species both taxonomically and ecologically. Ultraviolet-filtering pigments in the crystalline cones serve to tune ultraviolet vision in these animals as well, and some ultraviolet receptors themselves act as birefringent filters to enable circular polarization vision. Stomatopods have reached an evolutionary extreme in their use of filter mechanisms to tune photoreception to habitat and behaviour, allowing them to extend the spectral range of their vision both deeper into the ultraviolet and further into the red.

The evolution of complexity in the visual systems of stomatopods: insights from transcriptomics.

Stomatopod crustaceans have complex visual systems containing up to 16 different spectral classes of photoreceptors, more than described for any other animal. A previous molecular study of this visual system focusing on the expression of opsin genes found many more transcripts than predicted on the basis of physiology, but was unable to fully document the expressed opsin genes responsible for this diversity. Furthermore, questions remain about how other components of phototransduction cascades are involved. This study continues prior investigations by examining the molecular function of stomatopods' visual systems using new whole eye 454 transcriptome datasets from two species, Hemisquilla californiensis and Pseudosquilla ciliata. These two species represent taxonomic diversity within the order Stomatopoda, as well as variations in the anatomy and physiology of the visual system. Using an evolutionary placement algorithm to annotate the transcriptome, we identified the presence of nine components of the stomatopods' G-protein-coupled receptor (GPCR) phototransduction cascade, including two visual arrestins, subunits of the heterotrimeric G-protein, phospholipase C, transient receptor potential channels, and opsin transcripts. The set of expressed transduction genes suggests that stomatopods utilize a Gq-mediated GPCR-signaling cascade. The most notable difference in expression between the phototransduction cascades of the two species was the number of opsin contigs recovered, with 18 contigs found in retinas of H. californiensis, and 49 contigs in those of P. ciliata. Based on phylogenetic placement and fragment overlap, these contigs were estimated to represent 14 and 33 expressed transcripts, respectively. These data expand the known opsin diversity in stomatopods to clades of arthropod opsins that are sensitive to short wavelengths and ultraviolet wavelengths and confirm the results of previous studies recovering more opsin transcripts than spectrally distinct types of photoreceptors. Many of the recovered transcripts were phylogenetically placed in an evolutionary clade of crustacean opsin sequences that is rapidly expanding as the visual systems from more species are investigated. We discuss these results in relation to the emerging pattern, particularly in crustacean visual systems, of the expression of multiple opsin transcripts in photoreceptors of the same spectral class, and even in single photoreceptor cells.

Microdistribution of tetrodotoxin in two species of blue-ringed octopuses (Hapalochlaena lunulata and Hapalochlaena fasciata) detected by fluorescent immunolabeling.

Blue-ringed octopuses (genus Hapalochlaena) possess the potent neurotoxin tetrodotoxin (TTX). We examined the microdistribution of TTX in ten tissues of Hapalochlaena lunulata and Hapalochlaena fasciata by immunolabeling for fluorescent light microscopy (FLM). We visualized TTX throughout the posterior salivary gland, but the toxin was concentrated in cells lining the secretory tubules within the gland. Tetrodotoxin was present just beneath the epidermis of the integument (mantle and arms) and also concentrated in channels running through the dermis. This was suggestive of a TTX transport mechanism in the blood of the octopus, which would also explain the presence of the toxin in the blood-rich brachial hearts, gills, nephridia, and highly vascularized Needham's sac (testes contents). We also present the first report of TTX in any cephalopod outside of the genus Hapalochlaena. A specimen of Octopus bocki from French Polynesia contained a small amount of TTX in the digestive gland.

A novel function for a carotenoid: astaxanthin used as a polarizer for visual signalling in a mantis shrimp.

Biological signals based on color patterns are well known, but some animals communicate by producing patterns of polarized light. Known biological polarizers are all based on physical interactions with light such as birefringence, differential reflection or scattering. We describe a novel biological polarizer in a marine crustacean based on linear dichroism of a carotenoid molecule. The red-colored, dichroic ketocarotenoid pigment astaxanthin is deposited in the antennal scale of a stomatopod crustacean, Odontodactylus scyllarus. Positive correlation between partial polarization and the presence of astaxanthin indicates that the antennal scale polarizes light with astaxanthin. Both the optical properties and the fine structure of the polarizationally active cuticle suggest that the dipole axes of the astaxanthin molecules are oriented nearly normal to the surface of the antennal scale. While dichroic retinoids are used as visual pigment chromophores to absorb and detect polarized light, this is the first demonstration of the use of a carotenoid to produce a polarizing signal. By using the intrinsic dichroism of the carotenoid molecule and orienting the molecule in tissue, nature has engineered a previously undescribed form of biological polarizer.

Ontogeny of tetrodotoxin levels in blue-ringed octopuses: maternal investment and apparent independent production in offspring of Hapalochlaena lunulata.

Many organisms provision offspring with antipredator chemicals. Adult blue-ringed octopuses (Hapalochlaena spp.) harbor tetrodotoxin (TTX), which may be produced by symbiotic bacteria. Regardless of the ultimate source, we find that females invest TTX into offspring and offspring TTX levels are significantly correlated with female TTX levels. Because diversion of TTX to offspring begins during the earliest stages of egg formation, when females are still actively foraging and looking for mates, females may face an evolutionary tradeoff between provisioning larger stores of TTX in eggs and retaining that TTX for their own defense and offense (venom). Given that total TTX levels appear to increase during development and that female TTX levels correlate with those of offspring, investment may be an active adaptive process. Even after eggs have been laid, TTX levels continue to increase, suggesting that offspring or their symbionts begin producing TTX independently. The maternal investment of TTX in offspring of Hapalochlaena spp. represents a rare examination of chemical defenses, excepting ink, in cephalopods.

Evolution of anatomical and physiological specialization in the compound eyes of stomatopod crustaceans.

Stomatopod crustaceans have complex and diverse visual systems. Among their many unique features are a specialized ommatidial region (the midband) that enables the eye to have multiple overlapping visual fields, as well as sets of spectral filters that are intercalated at two levels between tiers of photoreceptors involved in polychromatic color vision. Although the physiology and visual function of stomatopod eyes have been studied for many years, how these unique visual features originated and diversified is still an open question. In order to investigate how stomatopods have attained the current complexity in visual function, we have combined physiological and morphological information (e.g. number of midband rows, number of filters in the retina, and the spectral properties of filters) with new phylogenetic analyses of relationships among species based on nucleotide sequence data from two nuclear (18S and 28S rDNA) and two mitochondrial [16S and cytochrome oxidase I (COI)] genes. Based on our recovered phylogenetic relationships among species, we propose two new superfamilies within the Stomatopoda: Hemisquilloidea and Pseudosquillodea. Maximum likelihood ancestral state reconstructions indicate that ancestral stomatopod eyes contained six midband rows and four intrarhabdomal filters, illustrating that the visual physiological complexity originated early in stomatopod evolutionary history. While the two distal filters contain conservative sets of filter pigments, the proximal filters show more spectral diversity in filter types, particularly in midband row 2, and are involved in tuning the color vision system to the photic environment. In particular, a set of related gonodactyloid families (Gonodactylidae, Protosquillidae, Takuidae) inhabiting shallow, brightly lit coral reef waters contain the largest diversity of filter pigments, which are spectrally placed relative to the underlying photoreceptors to take advantage of the broad spectrum of light available in the environment.

Male-male and male-female aggression may influence mating associations in wild octopuses (Abdopus aculeatus).

Abdopus aculeatus engages in frequent aggression and copulation, exhibits male mate-choice, and employs multiple mating tactics. Here we draw upon established hypotheses to compare male-male aggression (MMA) and male-female aggression (MFA), as they relate to their mating behavior in the wild. When contesting for females, males appear to balance mate preference (resource value) with perceived chances of winning contests (resource holding potential). Although males spent more time mating with and contesting for large "Adjacent Guarded" females (those occupying a den within arm's reach of a large "Adjacent Guarding" male), they exhibited higher rates of aggression over nonadjacent "Temporarily Guarded" females that may be more accessible. The major determinant of male-male aggressive success was size, and this factor may dictate the expression of conditional mating tactics in males. "Adjacent Guarding" males were the largest and most aggressively successful males, earning the most time copulating with females. They are considered to have the highest resource holding potential (RHP) in MMA. By contrast, in MFA, some larger individuals fled from smaller individuals, indicating that RHP appears to be a function of both size and sex in intersexual aggression. This result suggests variation in aggressiveness, or potential for severe injury-even sexual cannibalism during MFA. Male-female aggression may also be influenced by the sexual nonreceptivity of some individuals, or attempts by both sexes to increase foraging behavior by delaying mate-guarding activity.

Intra-organismal distribution of tetrodotoxin in two species of blue-ringed octopuses (Hapalochlaena fasciata and H. lunulata).

In-depth studies on the intra-organismal distribution of toxin may yield valuable clues about potential ecological functions. The distribution of tetrodotoxin (TTX) in previously unexamined tissues of two species of blue-ringed octopuses, wild-caught Hapalochlaena fasciata and Hapalochlaena lunulata from the aquarium industry, was surveyed. Tissues from each individual were examined separately. Tetrodotoxin was detected in posterior salivary gland (PSG), arm, mantle, anterior salivary glands, digestive gland, testes contents, brachial heart, nephridia, gill, and oviducal gland of H. fasciata. By contrast TTX was found only in the PSG, mantle tissue, and ink of H. lunulata. The highest concentrations of TTX resided in the PSG of both species; however, the arms and mantle contained the greatest absolute amounts of TTX. Minimum total amounts of TTX per octopus ranged from 60 to 405 microg in H. fasciata and from 0 to 174 microg in H. lunulata and correlated well with the amounts in the PSG. Transport of TTX in the blood is loosely suggested by the presence of the toxin in blood-rich organs such as the gill and brachial hearts. The distributional data also suggest both offensive and defensive functions of TTX.

Behaving in the dark: locomotor, chromatic, postural, and bioluminescent behaviors of the deep-sea squid Octopoteuthis deletron young 1972.

Visual behaviors are prominent components of intra- and interspecific communication in shallow-water cephalopods. Meso- and bathypelagic cephalopods were believed to have limited visual communication, other than bioluminescence, due to the reduced illumination at depth. To explore potential visual behaviors in mesopelagic squid, we used undersea vehicles to observe 76 individuals of Octopoteuthis deletron. In contrast to predictions, we found this species capable of a variety of visually linked behaviors not previously reported for a deep-ocean cephalopod. The resultant ethogram describes numerous chromatic, postural, locomotor, and bioluminescent behavioral components. A few common body patterns-the whole appearance of the individual involving multiple components-are characterized. The behaviors observed from individual squid were compared using a Non-metric Multi-Dimensional Scaling (NMDS) ordination, onto which hydrographic and observation parameters were mapped. Observation length, specimen collection, and contact with the vehicle affected which behaviors were performed. A separate NMDS, analyzing the body patterns, indicated that these sets of behavioral components could be visualized as groups within the NMDS ordination. While the functional roles of the behaviors described are not yet known, our findings of numerous behaviors in O. deletron clearly indicate that bioluminescence is not the sole method of visual communication by deep-sea squid.

Individually unique body color patterns in octopus (Wunderpus photogenicus) allow for photoidentification.

Studies on the longevity and migration patterns of wild animals rely heavily on the ability to track individual adults. Non-extractive sampling methods are particularly important when monitoring animals that are commercially important to ecotourism, and/or are rare. The use of unique body patterns to recognize and track individual vertebrates is well-established, but not common in ecological studies of invertebrates. Here we provide a method for identifying individual Wunderpus photogenicus using unique body color patterns. This charismatic tropical octopus is commercially important to the underwater photography, dive tourism, and home aquarium trades, but is yet to be monitored in the wild. Among the adults examined closely, the configurations of fixed white markings on the dorsal mantle were found to be unique. In two animals kept in aquaria, these fixed markings were found not to change over time. We believe another individual was photographed twice in the wild, two months apart. When presented with multiple images of W. photogenicus, volunteer observers reliably matched photographs of the same individuals. Given the popularity of W. photogenicus among underwater photographers, and the ease with which volunteers can correctly identify individuals, photo-identification appears to be a practical means to monitor individuals in the wild.

Recovery from blast fishing on coral reefs: a tale of two scales.

Dynamite or "blast" fishing is one of the most immediate and destructive threats to coral reefs worldwide. However, little is known about the long-term ecosystem effects of such blasts or the dynamics of recovery. Here, we examine coral reef recovery in the simplest case of acute single blasts of known age, as well as recovery from chronic blasting over greater spatial and temporal scales. Rubble resulting from single blasts slowly stabilized, and craters filled in with surrounding coral and new colonies. After five years, coral cover within craters no longer differed significantly from control plots. In contrast, extensively bombed areas showed no significant recovery over the six years of this study, despite adequate supply of coral larvae. After extensive blasting, the resulting coral rubble shifts in ocean currents, forming unstable "killing fields" for new recruits. While recently tested rehabilitation methods might be feasible on a small scale, human intervention is unlikely to be effective on large spatial scales, highlighting the need for effective management to prevent blast fishing in the first place.

Recovery in rubble fields: long-term impacts of blast fishing.

This paper presents initial results from a study of factors that inhibit or enhance hard coral recovery in rubble fields created by blast fishing in Komodo National Park and Bunaken National Park, Indonesia. Within nine sites monitored since 1998, there was no significant natural recovery. Levels of potential source coral larvae were assessed with settlement tiles in the rubble fields and in nearby high coral cover sites. Rubble movement was measured and shown to be detrimental to small scleractinians, especially in high current areas. In shallow water (2-6 m deep), rubble is often overgrown by soft corals and corallimorpharians, which inhibit hard coral survival. There is increased scleractinian recruitment in quadrats cleared of soft coral, and Acropora nubbins transplanted into soft coral fields suffer greater mortality than those transplanted above the soft coral canopy. Gaining an understanding of the prognosis for coral recovery is essential not only in order to assess the long-term impacts of blast fishing, but also to improve management decisions about protection of intact reefs and potential restoration of damaged areas.

Adaptive color vision in Pullosquilla litoralis (Stomatopoda, Lysiosquilloidea) associated with spectral and intensity changes in light environment.

Some stomatopod crustacean species that inhabit a range of habitat depths have color vision systems that adapt to changes in ambient light conditions. To date, this change in retinal function has been demonstrated in species within the superfamily Gonodactyloidea in response to varying the spectral range of light. Intrarhabdomal filters in certain ommatidia within the specialized midband of the eye change spectrally, modifying the sensitivity of underlying photoreceptors to match the spectrum of available light. In the present study, we utilized Pullosquilla litoralis, a member of the superfamily Lysiosquilloidea that also has a wide depth range. Individuals were placed within one of three light treatments: (1) full-spectrum, high-intensity 'white' light, (2) narrow-spectrum 'blue' light and (3) full-spectrum, reduced-intensity 'gray' light. After 3 months, the intrarhabdomal filters in Row 3 ommatidia of the midband in blue- and gray-light-treated animals were short-wavelength shifted by 10-20 nm compared with homologous filters in animals in white-light treatments. These spectral changes increase the relative sensitivity of associated photoreceptors in animals that inhabit environments where light spectral range or intensity is reduced. The adaptable color vision system of stomatopods may allow animals to make the best use of the ambient light occurring at their habitat regardless of depth. The major controlling element of the plasticity in lysiosquilloid stomatopod color vision appears to be light intensity rather than spectral distribution.

Polarization vision and its role in biological signaling.

Visual pigments, the molecules in photoreceptors that initiate the process of vision, are inherently dichroic, differentially absorbing light according to its axis of polarization. Many animals have taken advantage of this property to build receptor systems capable of analyzing the polarization of incoming light, as polarized light is abundant in natural scenes (commonly being produced by scattering or reflection). Such polarization sensitivity has long been associated with behavioral tasks like orientation or navigation. However, only recently have we become aware that it can be incorporated into a high-level visual perception akin to color vision, permitting segmentation of a viewed scene into regions that differ in their polarization. By analogy to color vision, we call this capacity polarization vision. It is apparently used for tasks like those that color vision specializes in: contrast enhancement, camouflage breaking, object recognition, and signal detection and discrimination. While color is very useful in terrestrial or shallow-water environments, it is an unreliable cue deeper in water due to the spectral modification of light as it travels through water of various depths or of varying optical quality. Here, polarization vision has special utility and consequently has evolved in numerous marine species, as well as at least one terrestrial animal. In this review, we consider recent findings concerning polarization vision and its significance in biological signaling.