Spatial vision in the echinoid genus<i>Echinometra</i>

Blevins, Erin; Johnsen, Sönke

doi:10.1242/jeb.01286

Cited by 71 publications

(71 citation statements)

References 13 publications

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“…We found them to be primarily arranged in two clusters in the numerous tube feet and to fulfill the minimal requirements for directional vision by deploying the sea urchin opaque skeleton as a screening device. Taken together, our data support a model of "compound-eye"-like vision in sea urchins contrasting to those proposed for echinoderms by other authors in the past (3,12,13). Our findings furthermore constitute unique documentation of a deuterostome animal deploying r-opsinexpressing PRCs for vision.…”

supporting

confidence: 83%

“…The spatial resolution of the PRC system would then depend on the spacing of spines that function, similarly to pigment cells in insect ommatidia, by shading defined parts of the sea urchin's skin. In contrast, our findings of distinct PRCs contradict the prerequisite of the model proposed by Johnsen and colleagues (3,13) and are supported by the findings of Millott and Coleman (35), who demonstrated that the podial bases in sea urchins comprise the most photosensitive part of their skin. Our finding that the basal PRC cluster is embedded in a considerable depression of the tube foot pore, resulting in a smaller angular width of the light reaching the PRCs (Fig.…”

Section: Different Compound Eye Models In Echinodermssupporting

confidence: 72%

“…Our finding that the basal PRC cluster is embedded in a considerable depression of the tube foot pore, resulting in a smaller angular width of the light reaching the PRCs (Fig. 4E), may constitute one component of a detector system accounting for the behavioral results presented by Johnsen and associates (3,13). Nevertheless, a new model implementing our structural findings and additional parameters like (species-dependent) number and arrangement of tube feet will have to show if and how different spacing of spines relative to the discovered tube foot basal PRCs might influence spatial resolution of the echinoid PRC system.…”

Section: Different Compound Eye Models In Echinodermsmentioning

confidence: 64%

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Unique system of photoreceptors in sea urchin tube feet

Ullrich-Lüter

Dupont

Arboleda

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

134

160

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Different sea urchin species show a vast variety of responses to variations in light intensity; however, despite this behavioral evidence for photosensitivity, light sensing in these animals has remained an enigma. Genome information of the recently sequenced purple sea urchin (Strongylocentrotus purpuratus) allowed us to address this question from a previously unexplored molecular perspective by localizing expression of the rhabdomeric opsin Spopsin4 and Sp-pax6, two genes essential for photoreceptor function and development, respectively. Using a specifically designed antibody against Sp-Opsin4 and in situ hybridization for both genes, we detected expression in two distinct groups of photoreceptor cells (PRCs) located in the animal's numerous tube feet. Specific reactivity of the Sp-Opsin4 antibody with sea star optic cushions, which regulate phototaxis, suggests a similar visual function in sea urchins. Ultrastructural characterization of the sea urchin PRCs revealed them to be of a microvillar receptor type. Our data suggest that echinoderms, in contrast to chordates, deploy a microvillar, r-opsinexpressing PRC type for vision, a feature that has been so far documented only in protostome animals. Surprisingly, sea urchin PRCs lack any associated screening pigment. Indeed, one of the tube foot PRC clusters may account for directional vision by being shaded through the opaque calcite skeleton. The PRC axons connect to the animal internal nervous system, suggesting an integrative function beyond local short circuits. Because juveniles display no phototaxis until skeleton completion, we suggest a model in which the entire sea urchin, deploying its skeleton as PRC screening device, functions as a huge compound eye.evolution | electron microscopy | immunogold

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supporting

confidence: 83%

Section: Different Compound Eye Models In Echinodermssupporting

confidence: 72%

Section: Different Compound Eye Models In Echinodermsmentioning

confidence: 64%

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Unique system of photoreceptors in sea urchin tube feet

Ullrich-Lüter

Dupont

Arboleda

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

134

160

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“…Orientation to visual stimuli in echinoderms occurs in one species of starfish, L. laevigata (Garm and Nilsson 2014) and two species of sea urchins (Blevins and Johnsen 2004;Yerramilli and Johnsen 2010). In addition, physiological studies have reported phototactic movements in the northern Pacific seastar, Asterias amurensis Ohtsuki 1966, 1968).…”

Section: Introductionmentioning

confidence: 99%

Visual orientation by the crown-of-thorns starfish (Acanthaster planci)

et al. 2016

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Photoreception in echinoderms has been known for over 200 years, but their visual capabilities remain poorly understood. As has been reported for some asteroids, the crown-of-thorns starfish (Acanthaster planci) possess a seemingly advanced eye at the tip of each of its 7-23 arms. With such an array of eyes, the starfish can integrate a wide field of view of its surroundings. We hypothesise that, at close range, orientation and directional movements of the crown-of-thorns starfish are visually guided. In this study, the eyes and vision of A. planci were examined by means of light microscopy, electron microscopy, underwater goniometry, electroretinograms and behavioural experiments in the animals' natural habitat. We found that only animals with intact vision could orient to a nearby coral reef, whereas blinded animals, with olfaction intact, walked in random directions. The eye had peak sensitivity in the blue part (470 nm) of the visual spectrum and a narrow, horizontal visual field of approximately 100°wide and 30°high. With approximately 250 ommatidia in each adult compound eye and average interommatidial angles of 8°, crown-of-thorns starfish have the highest spatial resolution of any starfish studied to date. In addition, they have the slowest vision of all animals examined thus far, with a flicker fusion frequency of only 0.6-0.7 Hz. This may be adaptive as fast vision is not required for the detection of stationary objects such as reefs. In short, the eyes seem optimised for detecting large, dark, stationary objects contrasted against an ocean blue background. Our results show that the visual sense of the crown-of-thorns starfish is much more elaborate than has been thus far appreciated and is essential for orientation and localisation of suitable habitats.

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“…Blevins and Johnsen tested this hypothesis using echinoids of the genus Echinometra and found that their visual resolution was on the order of that predicted by the spacing of their spines (~30deg.) (Blevins and Johnsen, 2004).This paper examines the visual resolution of S. purpuratus. Like Echinometra, it exhibits shelter-seeking behavior and is known to have a photosensitive test.…”

mentioning

confidence: 99%

Spatial vision in the purple sea urchinStrongylocentrotus purpuratus(Echinoidea)

Yerramilli

Johnsen

2010

Journal of Experimental Biology

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Echinoderm photoreception is a well-studied but puzzling phenomenon. Light-mediated behaviors are ubiquitous in this phylum, including simple phototaxis, covering reactions, UV avoidance, homing, polarization sensitivity, color changes, shelter seeking, diurnal migrations and movement towards small dark objects (Millot, 1954;Millot, 1955;Thornton, 1956;Yoshida, 1966;Millot and Yoshida, 1960;Scheibling, 1980;Hendler, 1984;Johnsen, 1994;Johnsen and Kier, 1999;Adams, 2001;Blevins and Johnsen, 2004). However, the underlying architecture and abilities of this system have remained mysterious.With the exception of the ocelli found at the tips of the arms of certain asteroids and the tentacular nerves of the holothurian Opheodesoma spectabilis, echinoderms have no discrete visual organs (reviewed by Yoshida et al., 1983). Instead, neurological and behavioral evidence suggests that their photosensitivity is diffuse and located above, below and even within the calcitic endoskeleton (Yoshida, 1979;Moore and Cobb, 1985;Aizenberg, 2001). More recently, Burke et al. (Burke et al., 2006) and Raible et al. (Raible et al., 2006) independently analyzed the genome of the echinoid Strongylocentrotus purpuratus and found six opsins from at least three pan-bilaterian families (r-opsin, c-opsin, G o -opsin) that were most strongly expressed in the tube feet and the globiferous and tridentate pedicellariae (expression in the endoskeleton was not measured). While other recent work has found some remarkable adaptations in the endoskeleton of echinoderms, including polarizing filters, migrating pigments and arrays of microscopic lenses (Hendler, 1984;Johnsen, 1994;Aizenberg et al., 2001), no regional specialization akin to cephalization has been found, leaving open the question of the neurological and structural bases of these photobehaviors.Woodley (Woodley, 1982) attempted to reconcile the ability of the tropical urchin Diadema antillarum to move towards small, dark objects with its apparent lack of an image-forming eye by suggesting that the entire animal functions as a compound eye, with the spines screening off-axis light, much like screening pigments optically separate ommatidia in insect eyes (Land and Nilsson, 2002). Blevins and Johnsen tested this hypothesis using echinoids of the genus Echinometra and found that their visual resolution was on the order of that predicted by the spacing of their spines (~30deg.) (Blevins and Johnsen, 2004).This paper examines the visual resolution of S. purpuratus. Like Echinometra, it exhibits shelter-seeking behavior and is known to have a photosensitive test. However, the angular density of its spines is roughly double-triple that of Echinometra. We therefore performed similar experiments to those described by Blevins and Johnsen (Blevins and Johnsen, 2004) to determine whether S. purpuratus had correspondingly higher visual resolution. ; Monte Carlo simulation), showing that each urchin, whether it moved towards or away from the target, did so with high consistency. These results strongly sug...

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Spatial vision in the echinoid genusEchinometra

Cited by 71 publications

References 13 publications

Unique system of photoreceptors in sea urchin tube feet

Unique system of photoreceptors in sea urchin tube feet

Visual orientation by the crown-of-thorns starfish (Acanthaster planci)

Spatial vision in the purple sea urchinStrongylocentrotus purpuratus(Echinoidea)

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