ORCID Profile
0000-0002-4540-6683
Current Organisation
University of Bristol
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Biological Physics | Evolutionary Biology | Biological Adaptation
Publisher: The Company of Biologists
Date: 04-2021
DOI: 10.1242/JEB.240812
Abstract: Polarization vision is widespread in nature, mainly among invertebrates, and is used for a range of tasks including navigation, habitat localization and communication. In marine environments, some species such as those from the Crustacea and Cephalopoda that are principally monochromatic, have evolved to use this adaptation to discriminate objects across the whole visual field, an ability similar to our own use of colour vision. The performance of these polarization vision systems varies, and the few cephalopod species tested so far have notably acute thresholds of discrimination. However, most studies to date have used artificial sources of polarized light that produce levels of polarization much higher than found in nature. In this study, the ability of octopuses to detect polarization contrasts varying in angle of polarization (AoP) was investigated over a range of different degrees of linear polarization (DoLP) to better judge their visual ability in more ecologically relevant conditions. The ‘just-noticeable-differences’ (JND) of AoP contrasts varied consistently with DoLP. These JND thresholds could be largely explained by their ‘polarization distance’, a neurophysical model that effectively calculates the level of activity in opposing horizontally and vertically oriented polarization channels in the cephalopod visual system. Imaging polarimetry from the animals’ natural environment was then used to illustrate the functional advantage that these polarization thresholds may confer in behaviourally relevant contexts.
Publisher: Springer Science and Business Media LLC
Date: 19-01-2022
DOI: 10.1038/S41598-021-04702-W
Abstract: The sensitivity of animal photoreceptors to different wavelengths of light strongly influence the perceived visual contrast of objects in the environment. Outside of the human visual wavelength range, ultraviolet sensitivity in many species provides important and behaviourally relevant visual contrast between objects. However, at the opposite end of the spectrum, the potential advantage of red sensitivity remains unclear. We investigated the potential benefit of long wavelength sensitivity by modelling the visual contrast of a wide range of jewel beetle colours against flowers and leaves of their host plants to hypothetical insect visual systems. We find that the presence of a long wavelength sensitive photoreceptor increases estimated colour contrast, particularly of beetles against leaves. Moreover, under our model parameters, a trichromatic visual system with ultraviolet (λ max = 355 nm), short (λ max = 445 nm) and long (λ max = 600 nm) wavelength photoreceptors performed as well as a tetrachromatic visual system, which had an additional medium wavelength photoreceptor (λ max = 530 nm). When we varied λ max for the long wavelength sensitive receptor in a tetrachromatic system, contrast values between beetles, flowers and leaves were all enhanced with increasing λ max from 580 nm to at least 640 nm. These results suggest a potential advantage of red sensitivity in visual discrimination of insect colours against vegetation and highlight the potential adaptive value of long wavelength sensitivity in insects.
Publisher: The Royal Society
Date: 06-12-2014
Abstract: Multilayer optical reflectors constructed from ‘stacks’ of alternating layers of high and low refractive index dielectric materials are present in many animals. For ex le, stacks of guanine crystals with cytoplasm gaps occur within the skin and scales of fish, and stacks of protein platelets with cytoplasm gaps occur within the iridophores of cephalopods. Common to all these animal multilayer reflectors are different degrees of random variation in the thicknesses of the in idual layers in the stack, ranging from highly periodic structures to strongly disordered systems. However, previous discussions of the optical effects of such thickness disorder have been made without quantitative reference to the propagation of light within the reflector. Here, we demonstrate that Anderson localization provides a general theoretical framework to explain the common coherent interference and optical properties of these biological reflectors. Firstly, we illustrate how the localization length enables the spectral properties of the reflections from more weakly disordered ‘coloured’ and more strongly disordered ‘silvery’ reflectors to be explained by the same physical process. Secondly, we show how the polarization properties of reflection can be controlled within guanine–cytoplasm reflectors, with an interplay of birefringence and thickness disorder explaining the origin of broadband polarization-insensitive reflectivity.
Publisher: The Company of Biologists
Date: 15-08-2022
DOI: 10.1242/JEB.243927
Abstract: All species within the conch snail family Strombidae possess large camera-type eyes that are surprisingly well-developed compared with those found in most other gastropods. Although these eyes are known to be structurally complex, very little research on their visual function has been conducted. Here, we use isoluminant expanding visual stimuli to measure the spatial resolution and contrast sensitivity of a strombid, Conomurex luhuanus. Using these stimuli, we show that this species responds to objects as small as 1.06 deg in its visual field. We also show that C. luhuanus responds to Michelson contrasts of 0.07, a low contrast sensitivity between object and background. The defensive withdrawal response elicited by visual stimuli of such small angular size and low contrast suggests that conch snails may use spatial vision for the early detection of potential predators. We support these findings with morphological estimations of spatial resolution of 1.04 deg. These anatomical data therefore agree with the behavioural measures and highlight the benefits of integrating behavioural and morphological approaches in animal vision studies. Using contemporary imaging techniques [serial block-face scanning electron microscopy (SBF-SEM), in conjunction with transmission electron microscopy (TEM)], we found that C. luhuanus have more complex retinas, in terms of cell type ersity, than expected based on previous studies of the group using TEM alone. We find the C. luhuanus retina comprises six cell types, including a newly identified ganglion cell and accessory photoreceptor, rather than the previously described four cell types.
Publisher: Elsevier BV
Date: 06-2014
Publisher: The Company of Biologists
Date: 2015
DOI: 10.1242/JEB.122507
Abstract: Polarization sensitivity (PS) is a common feature of invertebrate visual systems. In insects, PS is well known for its use in several different visually guided behaviours, particularly navigation and habitat search. Adult dragonflies use the polarization of light to find water but a role for PS in aquatic dragonfly larvae, a stage that inhabits a very different photic environment to the adults, has not been investigated. The optomotor response of the larvae of the Emperor dragonfly, Anax imperator, was used to determine whether these larvae use PS to enhance visual contrast underwater. Two different light scattering conditions were used to surround the larval animals: a naturalistic horizontally polarized light field and non-naturalistic weakly polarized light field. In both cases these scattering light fields obscured moving intensity stimuli that provoke an optokinetic response in the larvae. Animals were shown to track the movement of a square-wave grating more closely when it was viewed through the horizontally polarized light field, equivalent to a similar increase in tracking ability observed in response to an 8% increase in the intensity contrast of the stimuli. Our results suggest that larval PS enhances the intensity contrast of a visual scene under partially polarized lighting conditions that occur naturally in freshwater environments.
Publisher: Institute of Electrical and Electronics Engineers (IEEE)
Date: 10-2014
Publisher: SPIE
Date: 26-04-2012
DOI: 10.1117/12.915153
Publisher: Springer Science and Business Media LLC
Date: 12-07-2016
DOI: 10.1038/NCOMMS12140
Abstract: Gaze stabilization is an almost ubiquitous animal behaviour, one that is required to see the world clearly and without blur. Stomatopods, however, only fix their eyes on scenes or objects of interest occasionally. Almost uniquely among animals they explore their visual environment with a series pitch, yaw and torsional (roll) rotations of their eyes, where each eye may also move largely independently of the other. In this work, we demonstrate that the torsional rotations are used to actively enhance their ability to see the polarization of light. Both Gonodactylus smithii and Odontodactylus scyllarus rotate their eyes to align particular photoreceptors relative to the angle of polarization of a linearly polarized visual stimulus, thereby maximizing the polarization contrast between an object of interest and its background. This is the first documented ex le of any animal displaying dynamic polarization vision, in which the polarization information is actively maximized through rotational eye movements.
Publisher: Springer Science and Business Media LLC
Date: 21-10-2012
Publisher: Springer Science and Business Media LLC
Date: 16-05-2019
Publisher: American Physical Society (APS)
Date: 11-07-2013
Publisher: SPIE-Intl Soc Optical Eng
Date: 25-06-2013
Publisher: Cold Spring Harbor Laboratory
Date: 22-12-2021
DOI: 10.1101/2021.12.21.473630
Abstract: All species within the conch snail family Strombidae possess large camera-type eyes that are surprisingly well-developed compared to those found in most other gastropods. Although these eyes are known to be structurally complex, very little research on their visual function has been conducted. Here, we use isoluminant expanding visual stimuli to measure the spatial resolution and contrast sensitivity of a strombid, Conomurex luhuanus . Using these stimuli, we show that this species responds to objects as small as 1.06° in its visual field. We also show that C. luhuanus responds to Michelson contrasts of 0.07, a low contrast sensitivity between object and background. The defensive withdrawal response elicited by visual stimuli of such small angular size and low contrast suggests that conch snails may use spatial vision for the early detection of potential predators. We support these findings with morphological estimations of spatial resolution of 1.04 ± 0.14°. These anatomical data therefore agree with the behavioural measures and highlight the benefits of integrating morphological and behavioural approaches in animal vision studies. Furthermore, using contemporary imaging techniques including serial block-face scanning electron microscopy (SBF-SEM), in conjunction with transmission electron microscopy (TEM), we found that C. luhuanus have more complex retinas, in terms of cell type ersity, than previous studies of the group have discovered using TEM alone. We found the C. luhuanus retina is comprised of six cell types, including a newly identified ganglion cell and accessory photoreceptor, rather than the previously described four cell types. Behavioural trials indicate the eyes of conch snail species Conomurex luhuanus provide high-resolution spatial vision, and morphological examination reveals the retina contains more cell types than those of other gastropods.
Publisher: Elsevier BV
Date: 2009
DOI: 10.1016/J.CUB.2008.11.061
Abstract: Sunlight is attenuated rapidly in the ocean, resulting in little visually useful light reaching deeper than approximately 1000 m in even the clearest water. To maximize sensitivity to the relatively brighter downwelling sunlight, to view the silhouette of animals above them, and to increase the binocular overlap of their eyes, many mesopelagic animals have developed upward-pointing tubular eyes. However, these sacrifice the ability to detect bioluminescent and reflective objects in other directions. Thus, some mesopelagic fish with tubular eyes extend their visual fields laterally and/or ventrally by lensless ocular erticula, which are thought to provide unfocused images, allowing only simple detection of objects, with little spatial resolution. Here, we show that a medial mirror within the ventrally facing ocular erticulum of the spookfish, Dolichopteryx longipes, consisting of a multilayer stack derived from a retinal tapetum, is used to reflect light onto a lateral retina. The reflective plates are not orientated parallel to the surface of the mirror. Instead, plate angles change progressively around the mirror, and computer modeling indicates that this provides a well-focused image. This is the first report of an ocular image being formed in a vertebrate eye by a mirror.
Publisher: The Royal Society
Date: 27-06-2018
Publisher: The Royal Society
Date: 02-05-2018
Abstract: Almost all animals, regardless of the anatomy of the eyes, require some level of gaze stabilization in order to see the world clearly and without blur. For the mantis shrimp, achieving gaze stabilization is unusually challenging as their eyes have an unprecedented scope for movement in all three rotational degrees of freedom: yaw, pitch and torsion. We demonstrate that the species Odontodactylus scyllarus performs stereotypical gaze stabilization in the yaw degree of rotational freedom, which is accompanied by simultaneous changes in the pitch and torsion rotation of the eye. Surprisingly, yaw gaze stabilization performance is unaffected by both the torsional pose and the rate of torsional rotation of the eye. Further to this, we show, for the first time, a lack of a torsional gaze stabilization response in the stomatopod visual system. In the light of these findings, we suggest that the neural wide-field motion detection network in the stomatopod visual system may follow a radially symmetric organization to compensate for the potentially disorientating effects of torsional eye movements, a system likely to be unique to stomatopods.
Publisher: Institute of Electrical and Electronics Engineers (IEEE)
Date: 10-2014
Publisher: Public Library of Science (PLoS)
Date: 21-04-2016
Publisher: American Association for the Advancement of Science (AAAS)
Date: 04-08-2017
Abstract: Animals live in a colorful world, but we rarely stop to think about how this color is produced and perceived, or how it evolved. Cuthill et al. review how color is used for social signals between in idual animals and how it affects interactions with parasites, predators, and the physical environment. New approaches are elucidating aspects of animal coloration, from the requirements for complex cognition and perception mechanisms to the evolutionary dynamics surrounding its development and ersification. Science , this issue p. eaan0221
Publisher: Public Library of Science (PLoS)
Date: 27-03-2017
Publisher: The Royal Society
Date: 22-09-2021
Abstract: The sun is the most reliable celestial cue for orientation available to daytime migrants. It is widely assumed that diurnal migratory insects use a ‘time-compensated sun compass’ to adjust for the changing position of the sun throughout the day, as demonstrated in some butterfly species. The mechanisms used by other groups of diurnal insect migrants remain to be elucidated. Migratory species of hoverflies (Diptera: Syrphidae) are one of the most abundant and beneficial groups of diurnal migrants, providing multiple ecosystem services and undergoing directed seasonal movements throughout much of the temperate zone. To identify the hoverfly navigational strategy, a flight simulator was used to measure orientation responses of the hoverflies Scaeva pyrastri and Scaeva selenitica to celestial cues during their autumn migration. Hoverflies oriented southwards when they could see the sun and shifted this orientation westward following a 6 h advance of their circadian clocks. Our results demonstrate the use of a time-compensated sun compass as the primary navigational mechanism, consistent with field observations that hoverfly migration occurs predominately under clear and sunny conditions.
Publisher: The Company of Biologists
Date: 04-2017
DOI: 10.1242/JEB.153692
Abstract: Stomatopods have an extraordinary visual system, incorporating independent movement of their eyes in all three degrees of rotational freedom. In this work, we demonstrate that in the peacock mantis shrimp, Odontodactylus scyllarus, the level of ocular independence is task dependent. During gaze stabilization in the context of optokinesis, there is weak but significant correlation between the left and right eyes in the yaw degree of rotational freedom, but not in pitch and torsion. When one eye is completely occluded, the uncovered eye does not drive the covered eye during gaze stabilization. However, occluding one eye does significantly affect the uncovered eye, lowering its gaze stabilization performance. There is a lateral asymmetry, with the magnitude of the effect depending on the eye (left or right) combined with the direction of motion of the visual field. In contrast, during a startle saccade, the uncovered eye does drive a covered eye. Such disparate levels of independence between the two eyes suggest that responses to in idual visual tasks are likely to follow different neural pathways.
Publisher: The Company of Biologists
Date: 02-2019
DOI: 10.1242/JEB.134213
Abstract: Most polarisation vision studies reveal elegant ex les 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.
Publisher: Elsevier BV
Date: 12-2015
DOI: 10.1016/J.CUB.2015.09.073
Abstract: We are constantly surprised by the ability of relatively simple animals to perform precise visually guided movements within complex visual scenes, often using eyes with limited resolution. Exceptional ex les include the capture of airborne prey by dragonflies, the learning flights of bees and wasps, and the tracking of conspecifics by crabs on intertidal mudflats. Most studies have focused on how animals do this using sensitivity to intensity or color. However, it is increasingly evident that a third ability, polarization vision, may contribute to such tasks. In many insects, polarization-sensitive photoreceptors are confined within an area of the eye known as the dorsal rim, which detects the polarized sky pattern specifically for navigation. However, some animals, including fiddler crabs, are sensitive to the polarization of light across the majority of their image-forming eyes, potentially allowing them to use polarization information to increase perceived contrast for general visual tasks. Investigations into the use of polarization image-parsing by animals have largely been confined to laboratory settings under artificial lighting. This approach can occasionally mislead if the lighting conditions are different from natural. This study presents the first behavioral evidence from the natural context for a function of polarization image parsing. Using experimental manipulations in wild populations of the fiddler crab Uca stenodactylus, we provide evidence that these animals use their polarization vision to enhance contrast in their visual environment, thereby increasing their ability to detect and respond to objects on the mudflat surface.
Publisher: Elsevier BV
Date: 12-2016
DOI: 10.1016/J.YMPEV.2016.08.007
Abstract: Understanding the link between how proteins function in animals that live in extreme environments and selection on specific properties of amino acids has proved extremely challenging. Here we present the discovery of how the compressibility of opsin proteins in two evolutionarily distinct animal groups, teleosts and cephalopods, appears to be adapted to the high-pressure environment of the deep-sea. We report how in both groups, opsins in deeper living species are calculated to be less compressible. This is largely due to a common set of amino acid sites (bovRH# 159, 196, 213, 275) undergoing positive destabilizing selection in six of the twelve amino acid physiochemical properties that determine protein compressibility. This suggests a common evolutionary mechanism to reduce the adiabatic compressibility of opsin proteins. Intriguingly, the sites under selection are on the proteins' outer faces at locations known to be involved in opsin-opsin dimer interactions.
Location: United Kingdom of Great Britain and Northern Ireland
Start Date: 05-2019
End Date: 12-2022
Amount: $340,000.00
Funder: Australian Research Council
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