Brigitte Schoenemann

Exceptional preservation of eye structure in arthropod visual predators from the Middle Jurassic

Vision has revolutionized the way animals explore their environment and interact with each other and rapidly became a major driving force in animal evolution. However, direct evidence of how ancient animals could perceive their environment is extremely difficult to obtain because internal eye structures are almost never fossilized. Here, we reconstruct with unprecedented resolution the three-dimensional structure of the huge compound eye of a 160-million-year-old thylacocephalan arthropod from the La Voulte exceptional fossil biota in SE France. This arthropod had about 18,000 lenses on each eye, which is a record among extinct and extant arthropods and is surpassed only by modern dragonflies. Combined information about its eyes, internal organs and gut contents obtained by X-ray microtomography lead to the conclusion that this thylacocephalan arthropod was a visual hunter probably adapted to illuminated environments, thus contradicting the hypothesis that La Voulte was a deep-water environment.

Discovery of some 400 million year-old sensory structures in the compound eyes of trilobites

Fossilised arthropod compound eyes have frequently been described. Among the oldest known are those from the lower Cambrian of the Chengjiang Lagerstätte (China, c 525 Ma). All these compound eyes, though often excellently preserved, however, represent just the outer shells, because soft tissues, or even individual cells, usually do not fossilise. Using modern techniques, including μct-scanning and synchrotron radiation analysis we present the discovery of the sensory cell system of compound eyes, belonging to trilobites around 400 million years old, which allows their description and analysis. They are interpreted as forming part of an apposition-like ommatidium, which is a basic functional type of compound eye present in arthropods of today. Considered in greater detail, it is similar to the compound eye of the horseshoe crab Limulus, generally regarded as a ‘living fossil’, which probably retained this ancient basal system successfully until today.

The sophisticated visual system of a tiny Cambrian crustacean: analysis of a stalked fossil compound eye

Fossilized compound eyes from the Cambrian, isolated and three-dimensionally preserved, provide remarkable insights into the lifestyle and habitat of their owners. The tiny stalked compound eyes described here probably possessed too few facets to form a proper image, but they represent a sophisticated system for detecting moving objects. The eyes are preserved as almost solid, mace-shaped blocks of phosphate, in which the original positions of the rhabdoms in one specimen are retained as deep cavities. Analysis of the optical axes reveals four visual areas, each with different properties in acuity of vision. They are surveyed by lenses directed forwards, laterally, backwards and inwards, respectively. The most intriguing of these is the putatively inwardly orientated zone, where the optical axes, like those orientated to the front, interfere with axes of the other eye of the contralateral side. The result is a three-dimensional visual net that covers not only the front, but extends also far laterally to either side. Thus, a moving object could be perceived by a two-dimensional coordinate (which is formed by two axes of those facets, one of the left and one of the right eye, which are orientated towards the moving object) in a wide three-dimensional space. This compound eye system enables small arthropods equipped with an eye of low acuity to estimate velocity, size or distance of possible food items efficiently. The eyes are interpreted as having been derived from individuals of the early crustacean Henningsmoenicaris scutula pointing to the existence of highly efficiently developed eyes in the early evolutionary lineage leading towards the modern Crustacea.

Vision in fossilised eyes

This paper presents a review of recent developments in the study of vision in fossil arthropods, beginning with a discussion of the origin of visual systems. A report of the eyes of Cambrian arthropods from different Lagerstatten, especially the compound and median arthropod eyes from the Chengjiang fauna of China, is given. Reference is made also to compound eyes from the lower Cambrian Emu Bay Shale fauna of Australia and the Sirius Passet fauna of Greenland; also to the three-dimensionally preserved ‘Orsten’ fauna of Sweden. An understanding of how these eyes functioned is possible by reference to living arthropods and by using physical tools developed by physiologists. The eyes of trilobites (lower Cambrian to Upper Permian) are often very well preserved, and the structure and physiology of their calcite lenses, and the eye as a whole, are summarised here, based upon recent literature. Two main kinds of trilobite eyes have been long known. Firstly, there is the holochroal type, in which the lenses are usually numerous, small and closely packed together; this represents the ancestral kind, first found in lowermost Cambrian trilobites. The second type is the schizochroal eye, in which the lenses are relatively much larger and each is separated from its neighbours. Such eyes are confined to the single suborder Phacopina (Lower Ordovician to Upper Devonian). This visual system has no real equivalents in the animal kingdom. In this present paper, the origin of schizochroal eyes, by paedomorphosis from holochroal precursors, is reviewed, together with subsequent evolutionary transitions in the Early Ordovician. A summary of new work on the structure and mineralogy of phacopid lenses is presented, as is a discussion of the recent discovery of sublensar sensory structures in Devonian phacopids, which has opened up new dimensions in the study of trilobite vision.

Traces of an ancient immune system – how an injured arthropod survived 465 million years ago

This report of a severely injured trilobite from the Middle Ordovician (~465 Ma) accords with a number of similar observations of healed lesions observed in trilobites. The uniqueness of the specimen described here is that the character of the repair-mechanisms is reflected by the secondarily built structures, which form the new surface of the ruptured compound eye. Smooth, repaired areas inside the visual surface advert to a clotting principle, rather similar to those of today, and the way in which broken parts of the exoskeleton fused during restoration seem to simulate modern samples. The irregularity and variance of newly inserted visual units indicate the severity of the injury, which, most probably, was caused by a predatory attack, presumably by a cephalopod; these were most likely, the top predators of the Ordovician. Furthermore, the state of the moulted cephalon tells the dramatic struggle of an organism that lived in the Palaeozoic, to survive. In sum the specimen analysed here is evidence of an ancient clotting mechanism not dissimilar to those of today, rapidly preventing any exsanguination and the breakdown of osmoregulation of this marine arthropod.

An Unusual Cornea from a Well Preserved ('Orsten') Cambrian Compound Eye

Abstract. The tiny marine Cambrian ‘Orsten’ Cambropachycope clarksoni Walossek and Müller, 1990 (ca. 500 Ma), a derivative of the stem lineage toward Eucrustacea (= crown group), bore an unusual anterior projection of the head that has been designated a single compound eye. The cornea only of this eye has been preserved in three dimensions and in fine detail - unprecedented for a non-trilobite, Cambrian arthropod eye. Here we investigate the ultrastructure of this cornea. The cornea was found to be relatively thin and composed of three layers: an outermost and innermost layer of transparent material (a felt work of fibrils) and a hollow middle layer containing a dark material. This middle layer appears not to be an artefact of phosphatization or the consequence of moulting; probably it was present in the living, non-moulting-stage animal. The middle layer may have functioned as a filter - filled with pigmented oil that served to filter out the blue, scattered light from sunlight, thus enhancing the appearance of tiny light signals (i.e., potential prey). This adaptation would support the model lifestyle predicted from a study of the larger anatomy of C. clarksoni as a predator. However, the cornea of C. clarksoni remains enigmatic at this stage.

Structure and function of a compound eye, more than half a billion years old

Significance An exceptionally well-preserved arthropod fossil from near the base of the lower Cambrian shows the internal sensory structures of a compound eye, more than half a billion years old. The trilobite to which it belongs is found in a zone where the first complete organisms appear in the fossil record; thus, it is probably the oldest record of a visual system that ever will be available. This compound eye proved to possess the same kind of structure as the eyes of bees and dragonflies living today, but it lacks the lenses that are typical of modern eyes of this type. There is an elegant physical solution, however, of how to develop a quality image of modern type. Until now, the fossil record has not been capable of revealing any details of the mechanisms of complex vision at the beginning of metazoan evolution. Here, we describe functional units, at a cellular level, of a compound eye from the base of the Cambrian, more than half a billion years old. Remains of early Cambrian arthropods showed the external lattices of enormous compound eyes, but not the internal structures or anything about how those compound eyes may have functioned. In a phosphatized trilobite eye from the lower Cambrian of the Baltic, we found lithified remnants of cellular systems, typical of a modern focal apposition eye, similar to those of a bee or dragonfly. This shows that sophisticated eyes already existed at the beginning of the fossil record of higher organisms, while the differences between the ancient system and the internal structures of a modern apposition compound eye open important insights into the evolution of vision.

Form, Function and Palaeobiology: Preface

Form, Function and Palaeobiology: Preface Sergio F. Vizcaı́no, Euan N. K. Clarkson and Brigitte Schoenemann 1 CONICET, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Argentina. 2 División Paleontologı́a Vertebrados, Unidades de Investigación Anexo Museo FCNyM-UNLP, Av. 60 y 122, 1900, La Plata, Argentina. 3 Grant Institute, School of Geosciences, The King’s Buildings, University of Edinburgh, West Mains Road, Edinburgh EH9 3JW, Scotland, UK. 4 University of Cologne, Institute of Zoology, Department of Animal Physiology, Biocenter Cologne, Zülpicherstrasse 47b, D-50674 Köln, Germany. 5 University of Cologne, Institute of Biology Education (Zoology), Herbert-Lewinstrasse 10, D-50931 Cologne, Germany.

Colour Patterns in Devonian Trilobites

Many living marine animals exhibit striking colour patterns on their external skeletons or on exposed flesh. Such colour patterns surely existed in fossil animals, but usually have faded, partially or more often completely, or have been modified by diagenesis. Some reported patterns may indeed have resulted from diagenesis alone and thus are not original. Here we assess colour patterns in trilobites in Devonian specimens from North America and in new material from Germany. Specimens of Eldredgeops crassituberculata (Stumm, 1953) from the Middle Devonian Silica Shale, Sylvania, Ohio show spots on the pleurae, a brown band on the axial ribs and shadowy brown patches on the glabella. We advance reasons why these are most likely original. Distinctive patterns in the pygidia of Scutellum geesense Rud. & E. Richter 1956, Calycoscutellum sp., Scabriscutellum scabrum (Goldfuss, 1842) and Thysanopeltella acanthopeltis Barrande 1852 from the Devonian of Germany are illustrated here. Several specimens from different localities show a medium brown band fading to whitish towards the margin of the pygidium. These patterns are most unlikely to be random or, as argued here, diagenetic. They represent, in our opinion, original colour bands. We speculate that these colour patterns may have functioned as camouflage in a shallow-water visual world determined by ever-changing patterns of light.