Fluorescent enhancement of signaling in a mantis shrimp.
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Animal Communication↗
Biomedical subjects
T W Cronin
Publications and source records attributed to T W Cronin.
Sensory adaptation. Tunable colour vision in a mantis shrimp.
Systems of colour vision are normally identical in all members of a species, but a single design may not be adequate for species living in a diverse range of light environments. Here we show that in the mantis shrimp Haptosquilla trispinosa, which occupies a range of depths in the ocean, long-wavelength colour receptors are individually tuned to the local light environment. The spectral sensitivity of specific classes of photoreceptor is adjusted by filters that vary between individuals.
Adaptation, Physiological↗
The linearly polarized light field in clear, tropical marine waters: spatial and temporal variation of light intensity, degree of polarization and e-vector angle.
Sensitivity to polarized light is widespread among marine animals, including crustaceans, cephalopods and some fishes. They use this ability to orient and find prey, and possibly for a number of other visual tasks. Unlike the ultraviolet-sensitive polarization receptors of most insects, the polarization receptors of marine invertebrates tend to be maximally sensitive near 500 nm, suggesting that polarized light in water differs from that in air. The underwater field of partially linearly polarized light has been studied for nearly 50 years, but data are still limited and sparse. We measured the submarine polarized light field from 350 to 600 nm throughout the day on a coral reef in the Florida Keys at a depth of 15m using the underwater laboratory Aquarius as a research platform. Our results show that the angle of polarization as viewed along any given line of sight at this depth is a relatively simple function of solar position and that the degree of polarization is greatest 60-90 degrees from the sun. Both e-vector angle and degree of polarization vary only slightly with wavelength, although light is sometimes less polarized in the ultraviolet. Since light is most intense at medium wavelengths and polarization is nearly maximal at these wavelengths, invertebrate polarization photoreceptors are spectrally well placed. Also, the relative spectral constancy of the angle and degree of polarization supports fish polarization sensitivity, which relies on spectrally diverse photoreceptor sets.
Animals↗
Parallel processing and image analysis in the eyes of mantis shrimps.
The compound eyes of mantis shrimps, a group of tropical marine crustaceans, incorporate principles of serial and parallel processing of visual information that may be applicable to artificial imaging systems. Their eyes include numerous specializations for analysis of the spectral and polarizational properties of light, and include more photoreceptor classes for analysis of ultraviolet light, color, and polarization than occur in any other known visual system. This is possible because receptors in different regions of the eye are anatomically diverse and incorporate unusual structural features, such as spectral filters, not seen in other compound eyes. Unlike eyes of most other animals, eyes of mantis shrimps must move to acquire some types of visual information and to integrate color and polarization with spatial vision. Information leaving the retina appears to be processed into numerous parallel data streams leading into the central nervous system, greatly reducing the analytical requirements at higher levels. Many of these unusual features of mantis shrimp vision may inspire new sensor designs for machine vision.
Animals↗
Spectral tuning and the visual ecology of mantis shrimps.
The compound eyes of mantis shrimps (stomatopod crustaceans) include an unparalleled diversity of visual pigments and spectral receptor classes in retinas of each species. We compared the visual pigment and spectral receptor classes of 12 species of gonodactyloid stomatopods from a variety of photic environments, from intertidal to deep water (> 50 m), to learn how spectral tuning in the different photoreceptor types is modified within different photic environments. Results show that receptors of the peripheral photoreceptors, those outside the midband which are responsible for standard visual tasks such as spatial vision and motion detection, reveal the well-known pattern of decreasing lambdamax with increasing depth. Receptors of midband rows 5 and 6, which are specialized for polarization vision, are similar in all species, having visual lambdamax-values near 500nm, independent of depth. Finally, the spectral receptors of midband rows 1 to 4 are tuned for maximum coverage of the spectrum of irradiance available in the habitat of each species. The quality of the visual worlds experienced by each species we studied must vary considerably, but all appear to exploit the full capabilities offered by their complex visual systems.
Adaptation, Physiological↗
Spectral tuning of avian violet- and ultraviolet-sensitive visual pigments.
The violet- and ultraviolet-sensitive visual pigments of birds belong to the same class of pigments as the violet-sensitive (so-called blue) pigments of mammals. However, unlike the pigments from mammals and other vertebrate taxa which, depending on species, have lambda(max) values of either around 430 nm or around 370 nm, avian pigments are found with lambda(max) values spread across this range. In this paper, we present the sequences of two pigments isolated from Humbolt penguin and pigeon with intermediate lambda(max) values of 403 and 409 nm, respectively. By comparing the amino acid sequences of these pigments with the true UV pigments of budgerigar and canary and with chicken violet with a lambda(max) value of 420 nm, we have been able to identify five amino acid sites that show a pattern of substitution between species that is consistent with differences in lambda(max). Each of these substitutions has been introduced into budgerigar cDNA and expressed in vitro in COS-7 cells. Only three resulted in spectral shifts in the regenerated pigment; two had relatively small effects and may account for the spectral shifts between penguin, pigeon, and chicken whereas one, the replacement of Ser by Cys at site 90 in the UV pigments, produced a 35 nm shortwave shift that could account for the spectral shift from 403 nm in penguin to around 370 nm in budgerigar and canary.
Amino Acid Sequence↗
Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae).
Sexual communication between male and female fireflies involves the visual detection of species-specific bioluminescent signals. Firefly species vary spectrally in both their emitted light and in the sensitivity of the eye, depending on the time when each is active. Tuning of spectral sensitivity in three firefly species that occupy different photic niches was investigated using light and electron microscopy, microspectrophotometry, and intracellular recording to characterize the location and spectral absorption of the screening pigments that filter incoming light, the visual pigments that receive this filtered light, and the visual spectral sensitivity. Twilight-active species had similar pink screening pigments, but the visual pigment of Photinus pyralis peaked near 545 nm, while that of P. scintillans had a lambdamax near 557 nm. The night-active Photuris versicolo, had a yellow screening pigment that was uniquely localized, while its visual pigment was similar to that of P. pyralis. These results show that both screening and visual pigments vary among species. Modeling of spectral tuning indicates that the combination of screening and visual pigments found in the retina of each species provides the best possible match of sensitivity to bioluminescent emission. This combination also produced model sensitivity spectra that closely resemble sensitivities measured either with electroretinographic or intracellular techniques. Vision in both species of Photinus appears to be evolutionarily tuned for maximum discrimination of conspecific signals from spectrally broader backgrounds. Ph. versicolor, on the other hand, appears to have a visual system that offers a compromise between maximum sensitivity to, and maximum discrimination of, their signals.
Animal Communication↗
Spectral tuning of dichromats to natural scenes.
Multispectral images of natural scenes were collected from both forests and coral reefs. We varied the wavelength position of receptors in hypothetical dichromatic visual systems and, for each receptor pair estimated the percentage of discriminable points in natural scenes. The optimal spectral tuning predicted by this model results in photoreceptor pairs very like those of forest dwelling, dichromatic mammals and of coral reef fishes. Variations of the natural illuminants in forests have little or no effect on optimal spectral tuning, but variations of depth in coral reefs have moderate effects on the spectral placement of S and L cones. The ratio of S and L cones typically found in dichromatic mammals reduces the discriminability of forest scenes; in contrast, the typical ratio of S and L cones in coral reef fishes achieves nearly the optimal discrimination in coral reef scenes.
Animals↗
Microspectrophotometric analysis of intact chromatophores of the Japanese medaka, Oryzias latipes.
To investigate the possible photoprotective role of chromatophores in fish, the absorbances of four types of intact chromatophores in adult and larval Japanese medaka were analyzed using microspectrophotometric techniques. The absorbance spectrum of each chromatophore class was obtained from 300 to 550 nm. The absorbance spectra of intact leucophores, melanophores and xanthophores were very similar to the published absorbance spectra of the isolated pure pigments contained in each chromatophore type, pteridines, melanin and carotenoids or pteridines, respectively. Based on these absorbance spectra, leucophores and melanophores should provide the most ultraviolet (UV) photoprotection to fish since the compounds they contain, pteridines and melanin, correspondingly, have strong absorbances in the UV region of the spectrum. Xanthophores containing carotenoids are not likely to provide much protection to fish from UV-induced damage since carotenoids have low absorbances in the UV range. Xanthophores containing colored pteridines, however, may provide somewhat greater UV protection to fish, since pteridines absorb more light than carotenoids in the UV portion of the spectrum. The relative frequency, coverage and thickness of these two types of xanthophores should determine how much protection xanthophores as a chromatophore type would provide against UV-induced damage.
Age Factors↗
Eye design and color signaling in a stomatopod crustacean Gonodactylus smithii.
Many species of stomatopod crustaceans have multiple spectral classes of photoreceptors in their retinas. Behavioral evidence also indicates that stomatopods are capable of discriminating objects by their spectral differences alone. Most animals use only two to four different types of photoreceptors in their color vision systems, typically with broad sensitivity functions, but the stomatopods apparently include eight or more narrowband photoreceptor classes for color recognition. It is also known that stomatopods use several colored body regions in social interactions. To examine why stomatopods may be so 'concerned' with color, we measured the absorption spectra of visual pigments and intrarhabdomal filters, and the reflectance spectra from different parts of the bodies of several individuals of the gonodactyloid stomatopod species, Gonodactylus smithii. We then applied a model of multiple dichromatic channels for color encoding to examine whether the finely tuned color vision was specifically co-evolved with their complex color signals. Although the eye design of stomatopods seems suitable for detecting color signals of their own, the detection of color signals from other animals, such as reef fishes, can be enhanced as well. Color vision in G. smithii is therefore not exclusively adapted to detect its own color signals, but the spectral tuning of some photoreceptors (e.g. midband Rows 2 and 3) enhances the contrast of certain color signals to a large enough degree to make co-evolution between color vision and these rather specific color signals likely.
Animals↗
Color signals in natural scenes: characteristics of reflectance spectra and effects of natural illuminants.
Multispectral images of natural scenes were collected from both forests and coral reefs to represent typical, complex scenes that might be viewed by modern animals. Both reflectance spectra and modeled visual color signals in these scenes were decorrelated spectrally by principal-component analysis. Nearly 98% of the variance of reflectance spectra and color signals can be described by the first three principal components for both forest and coral reef scenes, which implies that three well-designed visual channels can recover almost all of the spectral information of natural scenes. A variety of natural illuminants affects color signals of forest scenes only slightly, but the variation in ambient irradiance spectra that is due to the absorption of light by water has dramatic influences on the spectral characteristics of coral reef scenes.
Animals↗
Characterization of natural illuminants in forests and the use of digital video data to reconstruct illuminant spectra.
We describe illumination spectra in forests and show that they can be accurately recovered from recorded digital video images. Natural illuminant spectra of 238 samples measured in temperate forests were characterized by principal-component analysis. The spectra can be accurately approximated by the mean and the first two principal components. Compared with illumination under open skies, the loci of forest illuminants are displaced toward the green region in the chromaticity plots, and unlike open sky illumination they cannot be characterized by correlated color temperature. We show that it is possible to recover illuminant spectra accurately from digital video images by a linear least-squares-fit estimation technique. The use of digital video data in spectral analysis provides a promising new approach to the studies of the spatial and temporal variation of illumination in natural scenes and the understanding of color vision in natural environments.
Color↗
Behavioural evidence for polarisation vision in stomatopods reveals a potential channel for communication.
Polarisation sensitivity (PS) - the ability to detect the orientation of polarised light - occurs in a wide variety of invertebrates [1] [2] and vertebrates [3] [4] [5], many of which are marine species [1]. Of these, the crustacea are particularly well documented in terms of their structural [6] and neural [7] [8] adaptations for PS. The few behavioural studies conducted on crustaceans demonstrate orientation to, or local navigation with, polarised sky patterns [9]. Aside from this, the function of PS in crustaceans, and indeed in most animals, remains obscure. Where PS can be shown to allow perception of polarised light as a 'special sensory quality' [1], separate from intensity or colour, it has been termed polarisation vision (PV). Here, within the remarkable visual system of the stomatopod crustaceans (mantis shrimps) [10], we provide the first demonstration of PV in the crustacea and the first convincing evidence for learning the orientation of polarised light in any animal. Using new polarimetric [11] and photographic methods to examine stomatopods, we found striking patterns of polarisation on their antennae and telson, suggesting that one function of PV in stomatopods may be communication [12]. PV may also be used for tasks such as navigation [5] [9] [13], location of reflective water surfaces [14] and contrast enhancement [1] [15] [16] [17] [18]. It is possible that the stomatopod PV system also contributes to some of these functions.
Animals↗
Estimation of errors in luminance signals encoded by primate retina resulting from sampling of natural images with red and green cones.
Both long-wavelength-sensitive (L) and medium-wavelength-sensitive (M) cones contribute to luminance mechanisms in human vision. This means that luminance and chromatic signals may be confounded. We use power spectra from natural images to estimate the magnitude of the corruption of luminance signals encoded by an array of retinal ganglion cells resembling the primate magnocellular neurons. The magnitude of this corruption is dependent on the cone lattice and is most severe where cones form clumps of a single spectral type. We find that chromatic corruption may equal or exceed the amplitude of other sources of noise and so could impose constraints on visual performance and on eye design.
Animals↗
The molecular evolution of visual pigments of freshwater crayfishes (Decapoda: Cambaridae).
This study examines the diverse maximum wavelength absorption (lambdamax) found in crayfishes (Decapoda: Cambaridae and Parastacidae) and the associated genetic variation in their opsin locus. We measured the wavelength absorption in the photoreceptors of six species that inhabit environments of different light intensities (i.e., burrows, streams, standing waters, and subterranean waters). Our results indicate that there is relatively little variation in lambdamax (522-530 nm) among species from different genera and families. The existing variation did not correlate with the habitat differences of the crayfishes studied. We simultaneously sequenced the rhodopsin gene to identify the amino acid replacements that affect shifts in maximum wavelength absorption. We then related these to changes that correlated with shifts in lambdamax by reconstructing ancestral character states using a maximum-likelihood approach. Using amino acid sequences obtained from five species (all were 301 amino acids in length), we identified a number of candidates for producing shifts of 4 to 8 nm in lambdamax. These amino acid replacements occurred in similar regions to those involved in spectral shifts in vertebrates.
Amino Acid Sequence↗
Corneal curvatures and refractions of central American frogs.
We employed neutralizing infrared videophotorefraction and photokeratometry to examine the manifest refractions and corneal curvatures of 21 species of anurans (frogs and toads) in five families (Dendrobatidae, Bufonidae, Centrolenidae, Leptodactylidae, and Hylidae) resident in Central America. We found that all of the anurans exhibited hyperopic refractions in air, but that the observed hyperopia was not totally explained by the small eye artefact (Glickstein & Millodot, 1970). An allometric comparison of the corneal radii of these small anurans with those of a large number of other vertebrates, inferred from ocular axial lengths, showed that their corneal radii increased significantly more rapidly with increasing body size than that of other vertebrates generally (allometric slope constants: anurans: 0.270 +/- 0.032; other vertebrates: 0.151 +/- 0.004). Among the anurans examined, nocturnal Hylids had significantly larger eyes than diurnal Dendrobatid frogs and Bufonid toads.
Animals↗
Stomatopod photoreceptor spectral tuning as an adaptation for colour constancy in water.
Where colour is used in communication absolute judgement of signalling spectra is important, and failures of colour constancy may limit performance. Stomatopod crustaceans have unusual eyes in which the midband contains ten or more classes of photoreceptor. For constancy based on receptor adaptation to a fixed background, elementary theory predicts and we confirm by modelling, that stomatopods' narrow-band receptors outperform more broadly tuned receptors. Similar considerations could account for the small spectral separation of receptors in each midband row. Thus, stomatopods seem to trade-off sensitivity and signal-to-noise ratio for increased colour constancy.
Adaptation, Ocular↗
Polarization contrast vision in Octopus.
While the ability to analyze polarized light is widespread among animals, its contribution to form vision has not yet been documented. We tested the hypothesis that polarization vision can be used for object discrimination, by training octopuses to distinguish between targets on the basis of the presence or absence of a pattern produced by a 90 degrees polarization contrast within the target. Octopuses recognized a 90 degrees contrast pattern within a single target, when presented either on a horizontal/vertical axis or on a 45 degrees/135 degrees axis. They were able to transfer their learning to new situations and to detect a polarization contrast when the orientations of the e-vector of light passing through the target center and background differed by as little as 20 degrees. Polarization vision may provide information similar to that available from color vision and thus serve to enhance the detection and recognition of objects.
Animals↗