Electrophysiological evidence for linear polarization sensitivity in the compound eyes of the stomatopod crustacean <i>Gonodactylus chiragra</i>

Kleinlogel, Sonja; Marshall, N. Justin

doi:10.1242/jeb.02499

Cited by 41 publications

(42 citation statements)

References 40 publications

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“…Electrophysiological evidence for LP sensitivity in Gonodactylus chiragra was presented by Kleinlogel and Marshall (2006). This study supported previous structural evidence showing the areas of the eye that are potentially involved in polarization vision , highlighting the hemispheres which sample four e-vector orientations for LPL (-45, +45, 0, 90º).…”

Section: Evidence For Linear Polarization Visionsupporting

confidence: 85%

Circular polarization vision in stomatopod crustaceans

Templin¹

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Perhaps due to relative speed and reliability, the information that light provides is useful to many animals. As a result, visual systems are a major, sensory system in several animal groups. Various aspects of vision become tuned by the environment and behavioural need, including relative sensitivity, speed, colour, and in some species, polarization. The stomatopod crustaceans (mantis shrimps) are remarkable in that they possess, at the retinal level, the most complex colour system known including 12 spectral sensitivities. However, like other crustaceans their lifestyles may also rely on the information they can receive from polarization. This is evident from the range of polarization sensitive areas of their subdivided eye. The hemispheric regions of the stomatopod eye are linear polarization sensitive, in a total of four different e-vector orientations. Additionally, stomatopods are able to rotate their eyes making the actual angle of polarization sensitivity to the outside world arbitrary.Perhaps most interesting in the context of polarization vision is the function of the eighth retinular cells, known as R8, of rows 5 and 6 of the midband region. These birefringent cells act as quarter-wave retarders allowing stomatopods to be sensitive to circularly polarized light (CPL). This ability has yet to be demonstrated in other animals and compared to linear polarization vision (LPV), circular polarization vision (CPV) is not well understood.The aim of this thesis was to further investigate rows 5 and 6 of the midband in a range of stomatopod species, using both behavioural and anatomical techniques. Firstly, through modelling the birefringent properties of the R8 in six species, it is revealed that the ability to discriminate CPL is shared among many stomatopods (Chapter 2). Adaptive pressure to maintain the size of the R8 cell, achieving quarter-wave retardance, suggests that it provides an important role for stomatopods. However, one species included in this study, Haptosquilla trispinosa, is likely sensitive to a different ellipticity of polarized light than circular.Since its discovery in 2008, it was hypothesized that circular polarization vision could provide a covert communication system for stomatopods. Chapter 3 uses behavioural paradigms to examine the discrimination abilities of Gonodactylaceus falcatus, a species of stomatopod with extensive polarization patterns on their bodies, and demonstrates that they use circular polarization as a signal for burrow occupancy. However, as variation in body patterns exist between species, with some species having none at all, other roles for CPL need to be The research presented in this thesis provides evidence contrary to the assumption that row 5 and 6 of the midband provide all species with CPV, despite appearing anatomically identical. We present a number of alternative hypotheses for the function of these rows, highlighting the likelihood that for different species specific roles exist.iv

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Section: Evidence For Linear Polarization Visionsupporting

confidence: 85%

Circular polarization vision in stomatopod crustaceans

Templin¹

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“…Electrophysiological studies have detailed the spatial variation of polarization sensitivity in the different photoreceptor classes in the eye (Kleinlogel and Marshall, 2006;Chiou et al, 2008). Optical measurements Chiou et al, 2008), optical modeling ) and molecular methods (Porter et al, 2009;Roberts et al, 2011) have provided additional information on the underlying mechanisms of polarization sensitivity.…”

Section: Research Articlementioning

confidence: 99%

Out of the blue: the evolution of horizontally polarized signals inHaptosquilla(Crustacea, Stomatopoda, Protosquillidae)

How

Porter

Radford

et al. 2014

Journal of Experimental Biology

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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 multidimensional 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. KEY WORDS: Stomatopod, Mantis shrimp, Polarization vision, Signal evolution, Sensory bias, Multi-modal signal INTRODUCTIONPolarization sensitivity is a common visual specialization that has evolved in both terrestrial and aquatic animals, and is particularly prevalent in invertebrates (Wehner and Labhart, 2006). On land, many insects use the celestial polarization pattern for navigation (Wehner, 1976;Rossel and Wehner, 1986;Labhart and Meyer, 1999;Dacke et al., 2003), while in the ocean, some crustaceans and cephalopod molluscs use polarization information to detect prey and possibly as a means of conspecific communication (Shashar et al., 1996;Cronin et al., 2003a;Chiou et al., 2007;Mäthger et al., 2009;Cronin et al., 2009;Chiou et al., 2011). In the context of communication, polarization often forms composite signals with other visual dimensions, such as hue and brightness (Cronin et al., 2003a;Cronin et al., 2009).The term polarization is used to define several properties of light. The angle of polarization describes the predominant direction in which the electric field of the light oscillates, while the degree of polarization defines the extent to which waves oscillate at the same angle. Underwater, differential sensitivity to either angle or degree of polarization has several fundamental advantages over other forms of visual information (Cronin et al., 2003a;Cronin et al., 2003b;Cronin et al., 2009;Shashar et al., 2011). For instance, in shallow, clear marine waters, the intensity and spectral composition of the downwelling light can vary dramatically, both as a function of the time of day, and because of environmental factors such as turbidity (Cronin et al., 2014). In such changing conditions, the polarization of light remains more constant than other visual dimensions over short ranges (Waterman, 1954;Cronin, 2001), which renders it a reliable provider of information (Shashar et al., 2011;Johnsen et al., 2011). Previous research in this field has fo...

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“…Many species possess at least 16 spectral classes of photoreceptors in their retinas. Included in these are eight color-specialist photoreceptors sensitive to narrow ranges of 'human-visible' light (Cronin and Marshall, 1989a,b;Marshall, 1988), three polarization receptors sensitive to linearly or circularly polarized light (Chiou et al, 2008;Cronin et al, 1994b;Kleinlogel and Marshall, 2006;Marshall, 1988;Marshall et al, 1991a) and at least five receptors sensitive to various spectral ranges of ultraviolet (UV) light (Kleinlogel and Marshall, 2009;Marshall and Oberwinkler, 1999). Underlying these diverse visual sensitivities is an array of optical and retinal structural modifications (Horridge, 1978;Marshall et al, 1991a;Schiff et al, 1986), the expression of a great number of opsins resulting in the most visual pigments yet described in a single eye (Cronin and Marshall, 1989b;Cronin et al, 1993;Porter et al, 2009Porter et al, , 2013, and the tuning of spectral sensitivity via serial filtering effects due to more distal visual pigments as well as photostable colored pigments (Cronin and Marshall, 1989a;Cronin et al, 1994aCronin et al, ,b, 2014Marshall, 1988;Marshall et al, 1991b;Porter et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Ultraviolet filters in stomatopod crustaceans: diversity, ecology, and evolution

Bok

Porter

Cronin

2015

Journal of Experimental Biology

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Stomatopod crustaceans employ unique ultraviolet (UV) optical filters in order to tune the spectral sensitivities of their UV-sensitive photoreceptors. In the stomatopod species Neogonodactylus oerstedii, we previously found four filter types, produced by five distinct mycosporine-like amino acid pigments in the crystalline cones of their specialized midband ommatidial facets. This UV-spectral tuning array produces receptors with at least six distinct spectral sensitivities, despite expressing only two visual pigments. Here, we present a broad survey of these UV filters across the stomatopod order, examining their spectral absorption properties in 21 species from seven families in four superfamilies. We found that UV filters are present in three of the four superfamilies, and evolutionary character reconstruction implies that at least one class of UV filter was present in the ancestor of all modern stomatopods. Additionally, postlarval stomatopods were observed to produce the UV filters simultaneously alongside development of the adult eye. The absorbance properties of the filters are consistent within a species; however, between species we found a great deal of diversity, both in the number of filters and in their spectral absorbance characteristics. This diversity correlates with the habitat depth ranges of these species, suggesting that species living in shallow, UV-rich environments may tune their UV spectral sensitivities more aggressively. We also found additional, previously unrecognized UV filter types in the crystalline cones of the peripheral eye regions of some species, indicating the possibility for even greater stomatopod visual complexity than previously thought.

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Electrophysiological evidence for linear polarization sensitivity in the compound eyes of the stomatopod crustacean Gonodactylus chiragra

Cited by 41 publications

References 40 publications

Circular polarization vision in stomatopod crustaceans

Circular polarization vision in stomatopod crustaceans

Out of the blue: the evolution of horizontally polarized signals inHaptosquilla(Crustacea, Stomatopoda, Protosquillidae)

Ultraviolet filters in stomatopod crustaceans: diversity, ecology, and evolution

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