Optics, range-finding, and neuroanatomy of the eye of a mantis shrimp, Squilla mantis Linnaeus

Schiff, H.; Abbott, Bill; Manning, Raymond B.

doi:10.5479/si.00810282.440

Cited by 27 publications

(31 citation statements)

References 26 publications

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“…Despite previous investigations into the stomatopod visual system (Schönenberger, 1977, Manning et al, 1984, Schiff et al, 1986 it was not until 1988 that researchers discovered exactly how intricate their eyes are , Cronin and Marshall, 1989a, Cronin and Marshall, 1989b provides a recent review)…”

Section: Bathysquilloidea Lysiosquilloidea Erythrosquilloidea and Gmentioning

confidence: 99%

“…Previously Schiff, Strausfeld and Nässel have described some of the general features of stomatopod optic neuropils and made some comparisons to other arthropods (Strausfeld and Nässel, 1981, Schiff et al, 1986, 1987. A few studies have described properties of the photoreceptor projections to the first optic neuropil, the lamina (Kleinlogel et al, , 2005, but detailed investigations of the other optic lobes (the medulla and lobula) have not been carried out.…”

Section: Introductionmentioning

confidence: 99%

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Colour vision in mantis shrimps: understanding one of the most complex visual systems in the world

Thoen¹

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Stomatopods (commonly known as mantis shrimps) have one of the most complex visual systems in the animal kingdom with up to 20 different photoreceptor types and the ability to see both linear and circular polarized light. The eye of a stomatopod is divided into three different parts; a dorsal and a ventral hemisphere divided up by 6 distinct rows of specialised ommatidia (visual units) termed the midband. The midband contains a complex array of up to 12 spectral receptors with maximum sensitivities ranging from the ultraviolet (UV) to the far-red (300-700 nm), in addition to achromatic receptors of which several are sensitive to different forms of polarized light. The abundance of spectral receptors has puzzled researchers, as it seemed excessive even for an animal living in a spectrally rich environment such as the coral reef. Furthermore, theoretical analyses suggest that there is really no need to have more than 4-7 receptors to have satisfactory colour vision in the 300-400 nm spectral range. Our increasing knowledge of polarization sensitivity is rapidly expanding the theme of photoreceptor proliferation with up to six channels of polarization information from a combination of midband and hemisphere receptors.The aim of this thesis was to investigate how stomatopods process and analyse chromatic and polarization information using a complementary approach of behavioural, electrophysiological and neuroanatomical techniques. A comparison of spectral sensitivities across species in the superfamily Gonodactyloidea was carried out in Chapter 2. This study showed that their spectral sensitivities remain very similar between species, with narrow, steeply shaped sensitivity curves spread evenly throughout the spectrum, suggesting there is a benefit of having uniform sampling of all wavelengths. Behavioural experiments were performed to test stomatopod spectral discrimination in Chapter 3, and this was found to be surprisingly poor, both compared to other animals and to theoretical modelling. To investigate if the poor discrimination was due to the spectral shape of the stimuli, more natural-shaped stimuli (with step-shaped spectra instead of the conventional peakshaped spectra) were tested in similar experiments (Chapter 4). However, these experiments yielded similar results to the ones obtained in Chapter 3. The electrophysiological and behavioural results suggest that the stomatopod visual system may use a simpler, serial processing system unlike the "conventional" opponency system known from other animals and may be the reason for why the spectral and polarization space must be covered by several channels.While such as system may appear exceptional, there are similarities between this system and they way primates process colour, only at different steps in the processing pathway (Chapter 5). Using an interval-decoding scheme coupled with the narrow, binned spectral sensitivities of stomatopods could allow quick and precise colour judgements but at the cost of very fine discrimination. 3As very little wa...

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Section: Bathysquilloidea Lysiosquilloidea Erythrosquilloidea and Gmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Colour vision in mantis shrimps: understanding one of the most complex visual systems in the world

Thoen¹

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“…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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“…Like other arthropods, stomatopods have three nested optical neuropils, termed the lamina, medulla and lobula (Strausfeld and Nassel, 1981, Schiff et al, 1986, Schiff, 1987, Kleinlogel et al, 2003, Kleinlogel and Marshall, 2005, Thoen et al, 2017 (Fig 1.5 A, B), which are located in the eye stalk. Beneath the lobula lies the lateral protocerebrum which is composed of several smaller structures, many of which are yet to be named.…”

Section: The Optic Neuropils Of Stomatopodsmentioning

confidence: 99%

“…While many studies have concentrated on the complex retina of stomatopods, which is also the focus of the previous chapters of this thesis, few have aimed to decode what happens in the eyestalk. Some studies have concentrated on the first steps in the processing pathway ,with particular focus on the projection pattern from the retina to lamina (Kleinlogel et al, 2003, Kleinlogel and Marshall, 2005, Schiff et al, 1986, and the lamina itself (Thoen et al, 2017). Thoen et al, (2017) also presented an overview of the eyestalk neuropils, including more detailed morphological descriptions of the second optic neuropil, the medulla.…”

Section: Introductionmentioning

confidence: 99%

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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Optics, range-finding, and neuroanatomy of the eye of a mantis shrimp, Squilla mantis Linnaeus

Cited by 27 publications

References 26 publications

Colour vision in mantis shrimps: understanding one of the most complex visual systems in the world

Colour vision in mantis shrimps: understanding one of the most complex visual systems in the world

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

Circular polarization vision in stomatopod crustaceans

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