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Cambrian view
Palaeoworld 15 (2006) 307–314
Research paper
Cambrian view Brigitte Schoenemann ∗ Pal¨aontologisches Institut der Universit¨at Bonn, Nussallee 8, 53115 Bonn, Germany Received 28 December 2005; received in revised form 14 July 2006; accepted 16 October 2006 Available online 3 November 2006
Abstract The analysis of visual systems is a valuable method of assessing phylogenetic processes. As in the present animal world, we find simple and complex systems in the Lower Cambrian. One may detect “simple eyes” for example with an advanced design in lobopodians, while the existence of even more simple “simple eyes” is very probable but still to be proved. More complex systems are to be found. In Leanchoilia illecebrosa Hou, 1987 and Leanchoilia superlata Walcott, 1912 there are probable dorsal median eyes and a pair of fine, stalked ventral eyes. Both systems may contribute to phylogenetic and systematic discussions. These presumably movable stalked eyes may be regarded as an adaptation to a mobile lifestyle. They suggest that the physiologic principle of nystagmus to stabilise the visual world of an animal in motion was already realised in Leanchoilia, perhaps for the first time. To analyse the surface of the early eyes from the Lower Cambrian – not only of Leanchoilia, but of any other forms as well – the number, shape and other parameters of the lenses could lead to further knowledge regarding vision in early invertebrates. © 2006 Nanjing Institute of Geology and Palaeontology, CAS. Published by Elsevier Ltd. All rights reserved. Keywords: Cambrian; Chengjiang Lagerst¨atte; Visual systems; Nystagmus; Leanchoilia; Luminescence
1. Introduction The earliest metazoan fossil record of the Lower Cambrian already reveals a high variety of eye systems, sometimes with quite sophisticated designs. These structures must have originated with unknown Proterozoic forms and their early development must have taken place long before. Parker (2003) developed the fascinating idea that the Cambrian explosion was triggered by the sudden evolution of vision in small successive singular steps. It is important to understand both, the structure and possible function of early visual systems, because the quality of vision depends on them. On the other hand the structure of eyes may characterise the affiliation to a systematic group and may even provide evidence
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for phylogenetic relationships. Two observations support this idea. First of all there is melanin, a black protein that persists in fossilisation, as we know from the black ink sacs of Jurassic squids. Melanin accompanies the essential structures of nearly all-visual systems. The other observation is selection that diminishes in importance where a visual system is ecologically well, so, once evolved, may remain to the present day. This allows a comparison of recent systems and ancient structures to be made. This analysis is based on photographs alone (photographs in Hou et al., 2004; Hou and Bergstr¨om, 1997), which are not greatly reliable in detail, but may be possible to observe the main structures and consequently it is worth formulating some hypotheses in order to give a concrete direction for more detailed investigations. A precondition for detailed work, however, is a clear definition of what is an eye. There is an excellent definition by the physiologists Land and Nilsson (2002): “Eyes supply information about the nature of light distribution
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in the environment.” This definition carries several implications, such as: (1) Vision is not necessarily coupled with an image, as we are used to in human vision. (2) Eyes are not restricted to a fixed design. 2. Early eyes Eyes in early Cambrian animals are common, but there have been no detailed investigations except of holochroal (Clarkson, 1973, 1975, 1979) and abathochroal (Jell, 1975; Zhang and Clarkson, 1990) eyes of trilobites. There are to be expected, however, much simpler systems. Even nerve cells may be light sensitive and light sensory cells may aggregate into small systems of different complexity, where each cell has its own pigment cup. In recent animals we find such simple eyes widely spread (e.g., in turbellarian flatworms, leeches, polychaetes, some molluscs and even prochordates; Land, 1981). The simplest structures are so-called “spot-eyes,” small flat aggregates that are characterised by a dark homogenous colour and a perfectly round shape with a sharp margin. These spot eyes are usually smaller than 1 mm2 . They may just perceive “light or no light,” but usually we find them as paired structures or even sequenced. In relation to each other, they may indicate a direction of the incident light or even allow the perception of movement in the environment (Fig. 1a and b). The spot eye may be recessed into a “pit eye” and it thus becomes possible to detect directions and motion even with one eye (see Fig. 1c and d). Even a slight closure of the pit leads to the potential for image formation. Each object point, however, is projected over a wide field and many receptors. The image points are not sharp and result in a blurred image. In the left example in Fig. 1f, the front and back of the object may be estimated, but no acuity is possible. As illustrated in Fig. 1f (right), the quality of the image, especially its sharpness, depends on the width of the opening of the pit. It improves when the hole becomes smaller. The sharper the image, however, the darker it becomes. In this example the front and back of the object may both be seen independently. But if these points become truly sharp as in this optimal “pinhole camera eye”, it would become very dark inside the eye as well. Animals with eyes of this kind need a bright environment. This situation in evolution led to the invention of lens eyes, with a large aperture and finally sharp image formation, such as we know in human eyes. In simpler organisms we find lenses, where the pit is filled with a blob of jelly or mucus, surrounded by a mul-
ticellular retina. These simple lenses are able to collect light and to converge the incident rays slightly. Among recent animals we find such systems widely distributed, for example in onychophorans, several annelid worms, molluscs and even cnidarians (Land and Nilsson, 2002). The characteristic patterns of flat, simple spot eyes can be recognised, if unexpectedly, in an illustration of a priapulid worm, smaller than 1 cm, Palaeopriapulites parvus Hou, Bergstr¨om, Wang, Feng et Chen, 1999, NIGPAS115446 (Hou et al., 2004, p. 65). It is a picture of excellent quality and of a very well preserved specimen, as very fine structures, for example the hooks of the proboscis, are to be seen. From the physiological point of view this specimen shows two conspicuous spoteyes as discussed above, because of their perfect round form, their sharp margin, their homogenous black colour, their symmetrical arrangement and their equal size (see Fig. 1g). In this respect they differ from all other dark patterns in this specimen that show an inhomogenous area, a random position and a shadowy indistinct contour. Priapulids have a very simple nervous system, concentrated in an anterior throat-ganglion, and eyes, if present, should be expected as other sensory organs close to this ganglion. A posterior position, however, makes sense. These worms belong to a group of priapulids that are mud-burrowers and predators. While the animal is moving, the proboscis, being the anterior part of the body (Kaestner, 1969), is pulled forward, anchored with its hooks into the ground and the stretched-out posterior part of the body follows. If the animal catches something to devour, the prey is skewered with these hooks of the proboscis and pulled completely back into the posterior part of the body. Thus, every part of the animal is constantly changing and in motion except for the very posterior end, where the assumed eyes are positioned. Being paired structures they may inform the worm of approaching danger and from which direction it comes, if one of the assumed spot eyes is suddenly shadowed; the animal may then react appropriately. There are other posterior sensory inputs, e.g. bristles. Like these, the signals of simple eyes may be directly switched onto the motor system, as in recent organisms, where they cause phototactic reactions, and no further complex processing is necessary. Another point should be discussed. Spot eyes are very common in different recent worms, but do not occur in extent priapulids (Kaestner, 1969). This loss, however, may be associated with a changing environment or life-style. The more turbid and muddy the water becomes, the less eyes, especially complex ones, become necessary, and they may disappear after a short period of evolution. Such simple structures especially may dwindle or may be changed to simple organs with
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Fig. 1. (a, b) Spot eye. (a) Turbellarian flatworm. Inset: paired spot eyes, scale bar ∼100 m. (b) Light sensitive cells (yellow) embedded into the epidermis (blue cells) forming a spot eye. (c, d) Pit eye. (c) Gieysztoria cuspidata Schmidt, 1861 (Turbellaria). Inset: left eye formed as a cup-like pit eye, scale bar ∼100 m. (d) Pit eyes allow detection of light from different directions. (e, f) Pinhole camera eye. (e) Stylaria lacustris Linnaeus, 1767 (Annelida). Inset: Left pinhole camera eye, scale bar ∼50 m. (f) Quality of vision, especially of sharpness, depends on the width of the opening of the pit. (g) Palaeopriapulites parvus Hou, Bergstr¨om, Wang, Feng et Chen, 1999 (see Hou et al., 2004, p. 65). White arrows: presumed simple spot eyes, scale bar ∼1 mm. Part (a, c) courtesy: Wim van Egmond, Rotterdam; (e) courtesy: Yuuji Tsukii, Tokyo, http://protist.i.hosei.ac.jp/; (g) reproduced from The Cambrian Fossils, by Hou et al. (2004, p. 27), by permission of Blackwell Publishing. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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Fig. 2. Simple lens eyes. (a) Luolishania longicruris Hou et Chen, 1989 (see Hou et al., 2004, p. 83), scale bar ∼1 mm. (b) Path of rays through a simple lens eye. Lens with two refracting surfaces resulting in an image far outside the eye. (c) Index gradient lens with a continuously changing refractive index refracting the light continuously, resulting in an image in the range of the eye region. Part (a) Reproduced from The Cambrian Fossils, by Hou et al. (2004 p. 27), by permission of Blackwell Publishing.
other sensory functions, e.g. mechanical. Accordingly an investigation of more specimens of a comparable quality will show whether we are dealing here with a regular structure that may be interpreted as a spot eye. If not, this illustrative example may be taken as a demonstration for the structure one has to look for in other quite simply organised, small-fossilised animals. A more advanced design of simple eyes is to be found in the lobopodian Luolishania longicruris Hou et Chen, 1989 ZCBYU10242 (Hou et al., 2004, p. 83). The paired eyes are positioned dorso-laterally (Fig. 2a). In the spherical dark eye in Miraluolishania haikouensis Liu et Shu, 2004, I observed a bright oval structure inside that may be interpreted as a lens embedded in a pigment layer of the former retina, because lens structures are known to mineralise differently from the rest of the eye or the entire animal. Thus the structure of this eye resembles that of present day onychophorans, an interesting comparison with phylogenetic consequences, that are to be discussed elsewhere. Such a lens may be inhomogenously dense and with a changing refractive index, arranged like onion skins. This can easily arise due to an inhomogenous secretion when it was being formed out, the light is refracted on and on continuously (Fig. 2b).
It may be calculated that the light rays can be refracted even sufficiently in this gradient refractive index lens to form a rough image, good enough to recognise patterns of the surroundings. Another example of an even more complex system of Early Cambrian eyes is that of Leanchoilia illecebrosa Hou, 1987 from Maotianshan, Chengjiang, China. In the “Treatise” of 1959 (Moore, 1959) Leanchoilia is regarded as probably missing lateral eyes. This opinion was shared by Bruton and Whittington (1983), Hou and Bergstr¨om (1997) and Hou et al. (2004), who considered it to be probably blind. However, Hou (1987) had discovered suspicious dark dorsal structures, possibly eyes, and Chen and Zhou (1997) described stalked eyes in Alalcomenaeus illecebrosus Simonetta, 1970 (later on reassigned by Hou and Bergstr¨om (1997) to Leanchoilia illecebrosa Hou, 1987). Because the structures seemed to have the large pendulous character that Briggs and Collins (1999) found in Alalcomenaeus cambricus Simonetta, 1970, these authors assumed that the Chinese “Leanchoilia” were Alalcomenaeus. Now it is clear that both forms, Leanchoilia and Alalcomenaeus, are present in the Chengjiang Biota. Consequently Leanchoilia itself became a blind form again.
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The systematic assignment of Leanchoilia has proved enigmatic. If one has to look for an eye, the systematic position of the investigated organism may be helpful, because naturally the structure of the eyes, their function and their systematical context are coupled. The early authors thought Leanchoilia to be a shrimp, a crustacean or a closely associated form (Walcott, 1912; Fedotov, 1925; Henriksen, 1928; Raymond, 1935; Simonetta and Delle Cave, 1975, 1980; Delle Cave and Simonetta, 1991). In the “Treatise” of 1959 it is to be found as a trilobitomorph animal among the subclass Merostomata of the class Trilobitoidea, forming an order Leanchoilida. More recent morphological information and cladistic analysis resolve Leanchoilia as an arachnomorph. A strong affiliation for Leanchoilia or the closely related Alalcomenaeus and the “great appendage animals” in general to the Arachnomorpha is seen for example in the work of Wills et al. (1994, 1995, 1998), Briggs and Collins (1999), Chen et al. (2004) and Cotton and Braddy (2004). This ambiguous situation was formulated by Bergstr¨om (1992) and Bergstr¨om and Hou (1998), who failed to see any similarity between this genus and chelicerates. Even in 1998, Bergstr¨om and Hou (1998, p. 161), had assigned the “Great Appendage Animals” previously to an individual clade, the Megacheira, where the Leanchoiliida constitute an order (Hou and Bergstr¨om, 1997). Budd (2002) finally considered Leanchoilia to be a stem group arthropod close to Alalcomenaeus. Leanchoilia does have eyes. In specimen CN 115363 of Leanchoilia illecebrosa Hou, 1987 a fine stalked eye is clearly to be seen (Fig. 3a and c). It sits on a thin, fine stalk, distally on a disc-like plate. This eye looks atypical for the megacheiran visual system, which has a characteristic large pendulous structure as is seen in Alalcomenaeus. We may observe such a form also in Tanglangia caudata Luo et Hu in Luo et al., 1997, Jianfengia multisegmentalis Hou, 1987 and others. Here we are dealing with a fine stalked eye, as we are accustomed to find in certain shrimps such as Lysmata seticaudata Risso, 1816. Even smaller but also fine penduculated eyes are to be found in the middle Cambrian Leanchoilia superlata Walcott, 1912 from the Burgess Shale as well (Fig. 3d), as to be seen in specimen USNM 83943b (Briggs et al., 1994). The architecture of these eyes indicates several different ecological adaptations. Stalked eyes, which are usually mobile by means of a basal joint, may point actively to a target that is to be looked at, although the head of the animal is not movable. The main task, however, is to keep the visual world constant. With a centre of gravity far distant, they may keep a constant posi-
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tion despite small, sudden, passive movements due to turbulence of the water. On the other hand, these finely structured eyes with a small resistance to the flowing water may fix one point of vision and while the animal is swimming forward, it holds this aspect, fixing its sight. If the eye has reached its extreme outermost position, the eye is very rapidly moved forward, fixing a new point and so on. This so-called nystagmus, in humans taking place in microseconds, occurs in stalked-eyed crustaceans as well. In this respect, the conspicuous finestructured stalked eyes of Leanchoilia with their physical characteristics enables the presumption, that these were the eyes of an active, maybe predatorial (Butterfield, 2002) animal. Leanchoilia may have been more lively than that Alalcomenaeus with its big lethargic pendulate eyes. Some morphological characters reveal that Leanchoilia was a good swimmer (Hou et al., 2004). One may even deduce that the use of nystagmus to stabilise the visual world arrived with Leanchoilia, because other Megacheira likewise possessed this large lethargic system. “Weak” stalked eyes like those of snails, comparable to these of many other Early Cambrian animals, seem to show no nystagmus (Penzlin, 1970). In these newly recognised stalked eyes it would be highly important to analyse the structure of the surface of the eyes, whether there are facets, and if there are, whether the facets are round, hexagonal or even square, whether the lenses are separated from each other or whether they are positioned closely together. Important assumptions concerning their function, system, phylogenetic context and performance could be made. Such characters as the number of facets could also be highly interesting, because by this feature the acuity of vision could be estimated as well as other optical characteristics. Besides these stalked eyes it seems to be highly possible that a dorsal eye system likewise exists (Fig. 3b and e), first described by Hou (1987, p. 254) and indicated by other publications such as Briggs and Collins (1999) or Hou et al. (2004). Because in Leanchoilia, as discussed before, stalked eyes are to be found as well, these structures may not be interpreted as eyes that really contribute to vision such as do the dorsally positioned eyes, e.g. in recent jumping spiders. It is more likely that these structures represent eyes that are comparable to socalled median eyes of crustaceans or hexapods (Fig. 3g). Among other functions they may work as “light meters”, and while they control the activity of the animal during the course of day, they may control the sensitivity of the main eye system or they may stabilise the position of the body with respect to the horizon in free-moving, especially flying animals. The number of these dorsal eyes as well as the surface structure should be investigated more
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Fig. 3. Eyes of Leanchoilia. (a) Leanchoilia illecebrosa Hou, 1987 CN 115363 (see Hou and Bergstr¨om, 1997, p. 27). White circle: right eye, stalked, scale bar ∼100 m. (b) Leanchoilia superlata (Walcott, 1912) ROM 54211 (see Butterfield, 2002, p. 157). White arrows indicate possible eye structures, scale bar ∼5 mm. (c) Stalked eye (the right) of Leanchoilia illecebrosa Hou, 1987 CN 115363 (see Hou and Bergstr¨om, 1998, p. 27). (d) Stalked eye of Leanchoilia superlata Walcott, 1912, drawn after USNM 83943 (see Briggs et al., 1994, p. 180). (For enhanced comparison to part (c) the drawing is a mirror image of the original.) (e) Leanchoilia superlata Walcott, 1912, drawn after ROM 54211 (see Butterfield, 2002, p. 157), position of the possible median eyes. (f) Shrimp eye. The mirror-like appearance is due to the reflecting superpositional mechanism. Was it already realised in Cambrian animals? (g) Median eyes of a hornet. Note that the median structure is larger than the outer structure. (h) Positions of eyes in Leanchoilia. (1) Leanchoilia illecebrosa Hou, 1987, in dorsal view, (2) Leanchoilia superlata Walcott, 1912, in dorsal view. (i) Positions of eyes in Leanchoilia. (1) Leanchoilia illecebrosa Hou, 1987, in lateral view, (2) Leanchoilia superlata Walcott, 1912, in lateral view. Part (a) Reproduced from Fossils and Strata, by Hou and Bergstr¨om (1997, p. 27), by permission of Taylor and Francis AS; (b) courtesy: Nicholas Butterfield, Cambridge; (f) courtesy: Jim Kasson; (g) © 1999, Dr. Elmar Billig.
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closely. In the illustration of Leanchoilia superlata Walcott, 1912 (Fig. 3b) (Butterfield, 2002) it appears as if there were two dorso-lateral and two very close, slightly diverging eye structures in the middle (Fig. 3e). Alalcomenaeus cambricus Simonetta, 1970 may have three (Briggs and Collins, 1999, p. 955), respectively five (Orr et al., 1998, p. 1173). If it is confirmed that there are really three, with the median one divided into two parts (compare Fig. 3b), thus resulting in four structures in total, they share an euarthropodean autapomorphic feature that has been retained among the recent Crustacea (Ax, 1999). Equally remarkable is an observation made in certain specimens of Leanchoilia illecebrosa Hou, 1987, for there is possibly to be recognised another type of dorsal eye, e.g. in specimen CN 115371, see Hou and Bergstr¨om (1997), or ELR C25001(MQ1), see Chen and Zhou (1997). Such eyes of a conspicuous comparable structure exist in today living Atlantic hydrothermal vent shrimps, living far from daylight in a depth of 2000–3000 m. The dorsal eyes of these vent shrimps are equipped with hypertrophic light perceptive structures. They are considered to be highly sensitive to detect dim light of special wavelengths, here produced by sonoluminescence at the top of the volcanic chimneys (O’Neill et al., 1995). Thus, forms of even higher specialised vision may have been possible in the Cambrian as well, currently being investigated more closely. 3. Conclusions (1) Simple eye systems exist in the early Cambrian and even advanced systems, as we have found in the lobopodians such as Luolishania longicruris Hou et Chen, 1989 respectively Miraluolishania haikouensis Liu et al., 2004. More simple designs than this one-lens system remain to be discovered. (2) Leanchoilia illecebrosa Hou, 1987 from Chengjiang as well as Leanchoilia superlata Walcott, 1912 from Burgess Shale are not blind. Contrary to the large, lethargic system of Alalcomenaeus, they have two fine penduculated ventral eyes, while the system of Leanchoilia superlata Walcott, 1912 is smaller than that of the older Leanchoilia illebrosa Hou, 1987. (3) Leanchoilia is presumed to possess two separate eye systems: stalked (compound?) eyes and 2+(2?) dorsal median eyes. Even if this stalked eye is actually being seen as convergent in different groups (due to their kind of mobility and their agile life-style), this combination of ventral stalked eyes and the dorsal median eyes suggests a crustacean context.
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(4) That big pendulous eyes exist in the Chengjiang Fauna is confirmed by a specimen illustrated by Chen (2004, p. 462). Considering previous investigations and the high number of specimens studied there may exist blind forms as well. Thus it seems to be worthwhile to re-study the Leanchoilia forms, especially these from Chengjiang. If one tries to imagine, what these ancient animals may have seen, in specimen RCCBYU 10217 Maotianoascus octonarius Chen et Zhou, 1997 dark structures in the flap regions are obvious. It is very likely that these symmetrically arranged patterns are also the results of melanin. They may be interpreted as structural elements, essential to all photophores, except of cnidarians (Ladd Prosser, 1991). The assignment of Maotianoascus octonarius Chen et Zhou, 1997 to cnidarians is still disputed and this feature may give an additional argument. These dark structures, however, lie in the same position as the photophores in recent luminescent organisms like modern Deiopeas. One may conclude from this, that photoluminescence is an ancient phenomenon, to be observed in and by the Early Cambrian animals, if their eye systems had allowed it. If not, it may have been an evolutionary incentive to improve. Acknowledgements I am indebted to my reviewers Euan N.K. Clarkson (Edinburgh, Great Britain) and Joachim Reitner (G¨ottingen, Germany) for their excellent advice, to JiAn Han (Xi‘an, China) and Di-Ying Huang (Nanjing, China), who opened my eyes to other specimens of Palaeopriapulites parvus (Hou, Bergstr¨om, Wang, Feng et Chen, 1999) and its preferred life-style, to Nick Butterfield (Cambridge, Great Britain), who advised me to handle the eyes of Leanchoilia with care while being discussed and to Ulrike Falckenberg-Bongarts (Bonn, Germany) as to Bernhard R. Schoenemann (Bonn, Germany) for their great help in preparing the figures. References Ax, P., 1999. Das System der Metazoa II. Gustav Fischer Verlag, Stuttgart, Jena, L¨ubeck, Ulm, 384 p. Bergstr¨om, J., 1992. The oldest arthropods and the origin of the Crustacea. Acta Zool. (Stockholm) 73 (5), 287–291. Bergstr¨om, J., Hou, X.G., 1998. Chengjiang arthropods and their bearing on early arthropod evolution. In: Edgecombe, G.D. (Ed.), Arthropod Fossils and Phylogeny. Columbia University Press, New York, pp. 151–184.
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Research paper
Cambrian view Brigitte Schoenemann ∗ Pal¨aontologisches Institut der Universit¨at Bonn, Nussallee 8, 53115 Bonn, Germany Received 28 December 2005; received in revised form 14 July 2006; accepted 16 October 2006 Available online 3 November 2006
Abstract The analysis of visual systems is a valuable method of assessing phylogenetic processes. As in the present animal world, we find simple and complex systems in the Lower Cambrian. One may detect “simple eyes” for example with an advanced design in lobopodians, while the existence of even more simple “simple eyes” is very probable but still to be proved. More complex systems are to be found. In Leanchoilia illecebrosa Hou, 1987 and Leanchoilia superlata Walcott, 1912 there are probable dorsal median eyes and a pair of fine, stalked ventral eyes. Both systems may contribute to phylogenetic and systematic discussions. These presumably movable stalked eyes may be regarded as an adaptation to a mobile lifestyle. They suggest that the physiologic principle of nystagmus to stabilise the visual world of an animal in motion was already realised in Leanchoilia, perhaps for the first time. To analyse the surface of the early eyes from the Lower Cambrian – not only of Leanchoilia, but of any other forms as well – the number, shape and other parameters of the lenses could lead to further knowledge regarding vision in early invertebrates. © 2006 Nanjing Institute of Geology and Palaeontology, CAS. Published by Elsevier Ltd. All rights reserved. Keywords: Cambrian; Chengjiang Lagerst¨atte; Visual systems; Nystagmus; Leanchoilia; Luminescence
1. Introduction The earliest metazoan fossil record of the Lower Cambrian already reveals a high variety of eye systems, sometimes with quite sophisticated designs. These structures must have originated with unknown Proterozoic forms and their early development must have taken place long before. Parker (2003) developed the fascinating idea that the Cambrian explosion was triggered by the sudden evolution of vision in small successive singular steps. It is important to understand both, the structure and possible function of early visual systems, because the quality of vision depends on them. On the other hand the structure of eyes may characterise the affiliation to a systematic group and may even provide evidence
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for phylogenetic relationships. Two observations support this idea. First of all there is melanin, a black protein that persists in fossilisation, as we know from the black ink sacs of Jurassic squids. Melanin accompanies the essential structures of nearly all-visual systems. The other observation is selection that diminishes in importance where a visual system is ecologically well, so, once evolved, may remain to the present day. This allows a comparison of recent systems and ancient structures to be made. This analysis is based on photographs alone (photographs in Hou et al., 2004; Hou and Bergstr¨om, 1997), which are not greatly reliable in detail, but may be possible to observe the main structures and consequently it is worth formulating some hypotheses in order to give a concrete direction for more detailed investigations. A precondition for detailed work, however, is a clear definition of what is an eye. There is an excellent definition by the physiologists Land and Nilsson (2002): “Eyes supply information about the nature of light distribution
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in the environment.” This definition carries several implications, such as: (1) Vision is not necessarily coupled with an image, as we are used to in human vision. (2) Eyes are not restricted to a fixed design. 2. Early eyes Eyes in early Cambrian animals are common, but there have been no detailed investigations except of holochroal (Clarkson, 1973, 1975, 1979) and abathochroal (Jell, 1975; Zhang and Clarkson, 1990) eyes of trilobites. There are to be expected, however, much simpler systems. Even nerve cells may be light sensitive and light sensory cells may aggregate into small systems of different complexity, where each cell has its own pigment cup. In recent animals we find such simple eyes widely spread (e.g., in turbellarian flatworms, leeches, polychaetes, some molluscs and even prochordates; Land, 1981). The simplest structures are so-called “spot-eyes,” small flat aggregates that are characterised by a dark homogenous colour and a perfectly round shape with a sharp margin. These spot eyes are usually smaller than 1 mm2 . They may just perceive “light or no light,” but usually we find them as paired structures or even sequenced. In relation to each other, they may indicate a direction of the incident light or even allow the perception of movement in the environment (Fig. 1a and b). The spot eye may be recessed into a “pit eye” and it thus becomes possible to detect directions and motion even with one eye (see Fig. 1c and d). Even a slight closure of the pit leads to the potential for image formation. Each object point, however, is projected over a wide field and many receptors. The image points are not sharp and result in a blurred image. In the left example in Fig. 1f, the front and back of the object may be estimated, but no acuity is possible. As illustrated in Fig. 1f (right), the quality of the image, especially its sharpness, depends on the width of the opening of the pit. It improves when the hole becomes smaller. The sharper the image, however, the darker it becomes. In this example the front and back of the object may both be seen independently. But if these points become truly sharp as in this optimal “pinhole camera eye”, it would become very dark inside the eye as well. Animals with eyes of this kind need a bright environment. This situation in evolution led to the invention of lens eyes, with a large aperture and finally sharp image formation, such as we know in human eyes. In simpler organisms we find lenses, where the pit is filled with a blob of jelly or mucus, surrounded by a mul-
ticellular retina. These simple lenses are able to collect light and to converge the incident rays slightly. Among recent animals we find such systems widely distributed, for example in onychophorans, several annelid worms, molluscs and even cnidarians (Land and Nilsson, 2002). The characteristic patterns of flat, simple spot eyes can be recognised, if unexpectedly, in an illustration of a priapulid worm, smaller than 1 cm, Palaeopriapulites parvus Hou, Bergstr¨om, Wang, Feng et Chen, 1999, NIGPAS115446 (Hou et al., 2004, p. 65). It is a picture of excellent quality and of a very well preserved specimen, as very fine structures, for example the hooks of the proboscis, are to be seen. From the physiological point of view this specimen shows two conspicuous spoteyes as discussed above, because of their perfect round form, their sharp margin, their homogenous black colour, their symmetrical arrangement and their equal size (see Fig. 1g). In this respect they differ from all other dark patterns in this specimen that show an inhomogenous area, a random position and a shadowy indistinct contour. Priapulids have a very simple nervous system, concentrated in an anterior throat-ganglion, and eyes, if present, should be expected as other sensory organs close to this ganglion. A posterior position, however, makes sense. These worms belong to a group of priapulids that are mud-burrowers and predators. While the animal is moving, the proboscis, being the anterior part of the body (Kaestner, 1969), is pulled forward, anchored with its hooks into the ground and the stretched-out posterior part of the body follows. If the animal catches something to devour, the prey is skewered with these hooks of the proboscis and pulled completely back into the posterior part of the body. Thus, every part of the animal is constantly changing and in motion except for the very posterior end, where the assumed eyes are positioned. Being paired structures they may inform the worm of approaching danger and from which direction it comes, if one of the assumed spot eyes is suddenly shadowed; the animal may then react appropriately. There are other posterior sensory inputs, e.g. bristles. Like these, the signals of simple eyes may be directly switched onto the motor system, as in recent organisms, where they cause phototactic reactions, and no further complex processing is necessary. Another point should be discussed. Spot eyes are very common in different recent worms, but do not occur in extent priapulids (Kaestner, 1969). This loss, however, may be associated with a changing environment or life-style. The more turbid and muddy the water becomes, the less eyes, especially complex ones, become necessary, and they may disappear after a short period of evolution. Such simple structures especially may dwindle or may be changed to simple organs with
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Fig. 1. (a, b) Spot eye. (a) Turbellarian flatworm. Inset: paired spot eyes, scale bar ∼100 m. (b) Light sensitive cells (yellow) embedded into the epidermis (blue cells) forming a spot eye. (c, d) Pit eye. (c) Gieysztoria cuspidata Schmidt, 1861 (Turbellaria). Inset: left eye formed as a cup-like pit eye, scale bar ∼100 m. (d) Pit eyes allow detection of light from different directions. (e, f) Pinhole camera eye. (e) Stylaria lacustris Linnaeus, 1767 (Annelida). Inset: Left pinhole camera eye, scale bar ∼50 m. (f) Quality of vision, especially of sharpness, depends on the width of the opening of the pit. (g) Palaeopriapulites parvus Hou, Bergstr¨om, Wang, Feng et Chen, 1999 (see Hou et al., 2004, p. 65). White arrows: presumed simple spot eyes, scale bar ∼1 mm. Part (a, c) courtesy: Wim van Egmond, Rotterdam; (e) courtesy: Yuuji Tsukii, Tokyo, http://protist.i.hosei.ac.jp/; (g) reproduced from The Cambrian Fossils, by Hou et al. (2004, p. 27), by permission of Blackwell Publishing. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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Fig. 2. Simple lens eyes. (a) Luolishania longicruris Hou et Chen, 1989 (see Hou et al., 2004, p. 83), scale bar ∼1 mm. (b) Path of rays through a simple lens eye. Lens with two refracting surfaces resulting in an image far outside the eye. (c) Index gradient lens with a continuously changing refractive index refracting the light continuously, resulting in an image in the range of the eye region. Part (a) Reproduced from The Cambrian Fossils, by Hou et al. (2004 p. 27), by permission of Blackwell Publishing.
other sensory functions, e.g. mechanical. Accordingly an investigation of more specimens of a comparable quality will show whether we are dealing here with a regular structure that may be interpreted as a spot eye. If not, this illustrative example may be taken as a demonstration for the structure one has to look for in other quite simply organised, small-fossilised animals. A more advanced design of simple eyes is to be found in the lobopodian Luolishania longicruris Hou et Chen, 1989 ZCBYU10242 (Hou et al., 2004, p. 83). The paired eyes are positioned dorso-laterally (Fig. 2a). In the spherical dark eye in Miraluolishania haikouensis Liu et Shu, 2004, I observed a bright oval structure inside that may be interpreted as a lens embedded in a pigment layer of the former retina, because lens structures are known to mineralise differently from the rest of the eye or the entire animal. Thus the structure of this eye resembles that of present day onychophorans, an interesting comparison with phylogenetic consequences, that are to be discussed elsewhere. Such a lens may be inhomogenously dense and with a changing refractive index, arranged like onion skins. This can easily arise due to an inhomogenous secretion when it was being formed out, the light is refracted on and on continuously (Fig. 2b).
It may be calculated that the light rays can be refracted even sufficiently in this gradient refractive index lens to form a rough image, good enough to recognise patterns of the surroundings. Another example of an even more complex system of Early Cambrian eyes is that of Leanchoilia illecebrosa Hou, 1987 from Maotianshan, Chengjiang, China. In the “Treatise” of 1959 (Moore, 1959) Leanchoilia is regarded as probably missing lateral eyes. This opinion was shared by Bruton and Whittington (1983), Hou and Bergstr¨om (1997) and Hou et al. (2004), who considered it to be probably blind. However, Hou (1987) had discovered suspicious dark dorsal structures, possibly eyes, and Chen and Zhou (1997) described stalked eyes in Alalcomenaeus illecebrosus Simonetta, 1970 (later on reassigned by Hou and Bergstr¨om (1997) to Leanchoilia illecebrosa Hou, 1987). Because the structures seemed to have the large pendulous character that Briggs and Collins (1999) found in Alalcomenaeus cambricus Simonetta, 1970, these authors assumed that the Chinese “Leanchoilia” were Alalcomenaeus. Now it is clear that both forms, Leanchoilia and Alalcomenaeus, are present in the Chengjiang Biota. Consequently Leanchoilia itself became a blind form again.
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The systematic assignment of Leanchoilia has proved enigmatic. If one has to look for an eye, the systematic position of the investigated organism may be helpful, because naturally the structure of the eyes, their function and their systematical context are coupled. The early authors thought Leanchoilia to be a shrimp, a crustacean or a closely associated form (Walcott, 1912; Fedotov, 1925; Henriksen, 1928; Raymond, 1935; Simonetta and Delle Cave, 1975, 1980; Delle Cave and Simonetta, 1991). In the “Treatise” of 1959 it is to be found as a trilobitomorph animal among the subclass Merostomata of the class Trilobitoidea, forming an order Leanchoilida. More recent morphological information and cladistic analysis resolve Leanchoilia as an arachnomorph. A strong affiliation for Leanchoilia or the closely related Alalcomenaeus and the “great appendage animals” in general to the Arachnomorpha is seen for example in the work of Wills et al. (1994, 1995, 1998), Briggs and Collins (1999), Chen et al. (2004) and Cotton and Braddy (2004). This ambiguous situation was formulated by Bergstr¨om (1992) and Bergstr¨om and Hou (1998), who failed to see any similarity between this genus and chelicerates. Even in 1998, Bergstr¨om and Hou (1998, p. 161), had assigned the “Great Appendage Animals” previously to an individual clade, the Megacheira, where the Leanchoiliida constitute an order (Hou and Bergstr¨om, 1997). Budd (2002) finally considered Leanchoilia to be a stem group arthropod close to Alalcomenaeus. Leanchoilia does have eyes. In specimen CN 115363 of Leanchoilia illecebrosa Hou, 1987 a fine stalked eye is clearly to be seen (Fig. 3a and c). It sits on a thin, fine stalk, distally on a disc-like plate. This eye looks atypical for the megacheiran visual system, which has a characteristic large pendulous structure as is seen in Alalcomenaeus. We may observe such a form also in Tanglangia caudata Luo et Hu in Luo et al., 1997, Jianfengia multisegmentalis Hou, 1987 and others. Here we are dealing with a fine stalked eye, as we are accustomed to find in certain shrimps such as Lysmata seticaudata Risso, 1816. Even smaller but also fine penduculated eyes are to be found in the middle Cambrian Leanchoilia superlata Walcott, 1912 from the Burgess Shale as well (Fig. 3d), as to be seen in specimen USNM 83943b (Briggs et al., 1994). The architecture of these eyes indicates several different ecological adaptations. Stalked eyes, which are usually mobile by means of a basal joint, may point actively to a target that is to be looked at, although the head of the animal is not movable. The main task, however, is to keep the visual world constant. With a centre of gravity far distant, they may keep a constant posi-
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tion despite small, sudden, passive movements due to turbulence of the water. On the other hand, these finely structured eyes with a small resistance to the flowing water may fix one point of vision and while the animal is swimming forward, it holds this aspect, fixing its sight. If the eye has reached its extreme outermost position, the eye is very rapidly moved forward, fixing a new point and so on. This so-called nystagmus, in humans taking place in microseconds, occurs in stalked-eyed crustaceans as well. In this respect, the conspicuous finestructured stalked eyes of Leanchoilia with their physical characteristics enables the presumption, that these were the eyes of an active, maybe predatorial (Butterfield, 2002) animal. Leanchoilia may have been more lively than that Alalcomenaeus with its big lethargic pendulate eyes. Some morphological characters reveal that Leanchoilia was a good swimmer (Hou et al., 2004). One may even deduce that the use of nystagmus to stabilise the visual world arrived with Leanchoilia, because other Megacheira likewise possessed this large lethargic system. “Weak” stalked eyes like those of snails, comparable to these of many other Early Cambrian animals, seem to show no nystagmus (Penzlin, 1970). In these newly recognised stalked eyes it would be highly important to analyse the structure of the surface of the eyes, whether there are facets, and if there are, whether the facets are round, hexagonal or even square, whether the lenses are separated from each other or whether they are positioned closely together. Important assumptions concerning their function, system, phylogenetic context and performance could be made. Such characters as the number of facets could also be highly interesting, because by this feature the acuity of vision could be estimated as well as other optical characteristics. Besides these stalked eyes it seems to be highly possible that a dorsal eye system likewise exists (Fig. 3b and e), first described by Hou (1987, p. 254) and indicated by other publications such as Briggs and Collins (1999) or Hou et al. (2004). Because in Leanchoilia, as discussed before, stalked eyes are to be found as well, these structures may not be interpreted as eyes that really contribute to vision such as do the dorsally positioned eyes, e.g. in recent jumping spiders. It is more likely that these structures represent eyes that are comparable to socalled median eyes of crustaceans or hexapods (Fig. 3g). Among other functions they may work as “light meters”, and while they control the activity of the animal during the course of day, they may control the sensitivity of the main eye system or they may stabilise the position of the body with respect to the horizon in free-moving, especially flying animals. The number of these dorsal eyes as well as the surface structure should be investigated more
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Fig. 3. Eyes of Leanchoilia. (a) Leanchoilia illecebrosa Hou, 1987 CN 115363 (see Hou and Bergstr¨om, 1997, p. 27). White circle: right eye, stalked, scale bar ∼100 m. (b) Leanchoilia superlata (Walcott, 1912) ROM 54211 (see Butterfield, 2002, p. 157). White arrows indicate possible eye structures, scale bar ∼5 mm. (c) Stalked eye (the right) of Leanchoilia illecebrosa Hou, 1987 CN 115363 (see Hou and Bergstr¨om, 1998, p. 27). (d) Stalked eye of Leanchoilia superlata Walcott, 1912, drawn after USNM 83943 (see Briggs et al., 1994, p. 180). (For enhanced comparison to part (c) the drawing is a mirror image of the original.) (e) Leanchoilia superlata Walcott, 1912, drawn after ROM 54211 (see Butterfield, 2002, p. 157), position of the possible median eyes. (f) Shrimp eye. The mirror-like appearance is due to the reflecting superpositional mechanism. Was it already realised in Cambrian animals? (g) Median eyes of a hornet. Note that the median structure is larger than the outer structure. (h) Positions of eyes in Leanchoilia. (1) Leanchoilia illecebrosa Hou, 1987, in dorsal view, (2) Leanchoilia superlata Walcott, 1912, in dorsal view. (i) Positions of eyes in Leanchoilia. (1) Leanchoilia illecebrosa Hou, 1987, in lateral view, (2) Leanchoilia superlata Walcott, 1912, in lateral view. Part (a) Reproduced from Fossils and Strata, by Hou and Bergstr¨om (1997, p. 27), by permission of Taylor and Francis AS; (b) courtesy: Nicholas Butterfield, Cambridge; (f) courtesy: Jim Kasson; (g) © 1999, Dr. Elmar Billig.
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closely. In the illustration of Leanchoilia superlata Walcott, 1912 (Fig. 3b) (Butterfield, 2002) it appears as if there were two dorso-lateral and two very close, slightly diverging eye structures in the middle (Fig. 3e). Alalcomenaeus cambricus Simonetta, 1970 may have three (Briggs and Collins, 1999, p. 955), respectively five (Orr et al., 1998, p. 1173). If it is confirmed that there are really three, with the median one divided into two parts (compare Fig. 3b), thus resulting in four structures in total, they share an euarthropodean autapomorphic feature that has been retained among the recent Crustacea (Ax, 1999). Equally remarkable is an observation made in certain specimens of Leanchoilia illecebrosa Hou, 1987, for there is possibly to be recognised another type of dorsal eye, e.g. in specimen CN 115371, see Hou and Bergstr¨om (1997), or ELR C25001(MQ1), see Chen and Zhou (1997). Such eyes of a conspicuous comparable structure exist in today living Atlantic hydrothermal vent shrimps, living far from daylight in a depth of 2000–3000 m. The dorsal eyes of these vent shrimps are equipped with hypertrophic light perceptive structures. They are considered to be highly sensitive to detect dim light of special wavelengths, here produced by sonoluminescence at the top of the volcanic chimneys (O’Neill et al., 1995). Thus, forms of even higher specialised vision may have been possible in the Cambrian as well, currently being investigated more closely. 3. Conclusions (1) Simple eye systems exist in the early Cambrian and even advanced systems, as we have found in the lobopodians such as Luolishania longicruris Hou et Chen, 1989 respectively Miraluolishania haikouensis Liu et al., 2004. More simple designs than this one-lens system remain to be discovered. (2) Leanchoilia illecebrosa Hou, 1987 from Chengjiang as well as Leanchoilia superlata Walcott, 1912 from Burgess Shale are not blind. Contrary to the large, lethargic system of Alalcomenaeus, they have two fine penduculated ventral eyes, while the system of Leanchoilia superlata Walcott, 1912 is smaller than that of the older Leanchoilia illebrosa Hou, 1987. (3) Leanchoilia is presumed to possess two separate eye systems: stalked (compound?) eyes and 2+(2?) dorsal median eyes. Even if this stalked eye is actually being seen as convergent in different groups (due to their kind of mobility and their agile life-style), this combination of ventral stalked eyes and the dorsal median eyes suggests a crustacean context.
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(4) That big pendulous eyes exist in the Chengjiang Fauna is confirmed by a specimen illustrated by Chen (2004, p. 462). Considering previous investigations and the high number of specimens studied there may exist blind forms as well. Thus it seems to be worthwhile to re-study the Leanchoilia forms, especially these from Chengjiang. If one tries to imagine, what these ancient animals may have seen, in specimen RCCBYU 10217 Maotianoascus octonarius Chen et Zhou, 1997 dark structures in the flap regions are obvious. It is very likely that these symmetrically arranged patterns are also the results of melanin. They may be interpreted as structural elements, essential to all photophores, except of cnidarians (Ladd Prosser, 1991). The assignment of Maotianoascus octonarius Chen et Zhou, 1997 to cnidarians is still disputed and this feature may give an additional argument. These dark structures, however, lie in the same position as the photophores in recent luminescent organisms like modern Deiopeas. One may conclude from this, that photoluminescence is an ancient phenomenon, to be observed in and by the Early Cambrian animals, if their eye systems had allowed it. If not, it may have been an evolutionary incentive to improve. Acknowledgements I am indebted to my reviewers Euan N.K. Clarkson (Edinburgh, Great Britain) and Joachim Reitner (G¨ottingen, Germany) for their excellent advice, to JiAn Han (Xi‘an, China) and Di-Ying Huang (Nanjing, China), who opened my eyes to other specimens of Palaeopriapulites parvus (Hou, Bergstr¨om, Wang, Feng et Chen, 1999) and its preferred life-style, to Nick Butterfield (Cambridge, Great Britain), who advised me to handle the eyes of Leanchoilia with care while being discussed and to Ulrike Falckenberg-Bongarts (Bonn, Germany) as to Bernhard R. Schoenemann (Bonn, Germany) for their great help in preparing the figures. References Ax, P., 1999. Das System der Metazoa II. Gustav Fischer Verlag, Stuttgart, Jena, L¨ubeck, Ulm, 384 p. Bergstr¨om, J., 1992. The oldest arthropods and the origin of the Crustacea. Acta Zool. (Stockholm) 73 (5), 287–291. Bergstr¨om, J., Hou, X.G., 1998. Chengjiang arthropods and their bearing on early arthropod evolution. In: Edgecombe, G.D. (Ed.), Arthropod Fossils and Phylogeny. Columbia University Press, New York, pp. 151–184.
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