Cambrian compound eye

Paleontological Research, vol. 17, no. 3, pp. 251–260, August 1, 2013© by the Palaeontological Society of Japandoi:10.2517/1342-8144-17.3.251

An unusual cornea from a well preserved (‘Orsten’) Cambrian compound eye

ANDREW R. PARKER1, BRIGITTE SCHOENEMANN2, JOACHIM T. HAUG3 AND DIETER WALOSZEK4

1Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK (e-mail: [email protected])2Steinmann Institute of Geology, Mineralogy and Palaeontology, University of Bonn, D-53115 Bonn, Germany3Zoological Institute and Museum, Cytology and Evolutionary Biology, Ernst Moritz Arndt University of Greifswald, Soldmannstrasse 23, D-17487 Greifswald, Germany4Biosystematic Documentation, University of Ulm, Helmholtzstrasse 20, D-89081 Ulm, Germany

Received August 9, 2012; Revised manuscript accepted December 15, 2012

Abstract. The tiny marine Cambrian ‘Orsten’ Cambropachycope clarksoni Walossek and Müller, 1990 (ca. 500Ma), a derivative of the stem lineage toward Eucrustacea (= crown group), bore an unusual anterior projectionof the head that has been designated a single compound eye. The cornea only of this eye has been preserved inthree dimensions and in fine detail – unprecedented for a non-trilobite, Cambrian arthropod eye. Here weinvestigate the ultrastructure of this cornea. The cornea was found to be relatively thin and composed of threelayers: an outermost and innermost layer of transparent material (a felt work of fibrils) and a hollow middlelayer containing a dark material. This middle layer appears not to be an artefact of phosphatization or theconsequence of moulting; probably it was present in the living, non-moulting-stage animal. The middle layermay have functioned as a filter – filled with pigmented oil that served to filter out the blue, scattered light fromsunlight, thus enhancing the appearance of tiny light signals (i.e., potential prey). This adaptation would sup-port 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.

Key words: Cambrian, compound eye, cornea, early vision, Orsten

Introduction

Compound eyesCompound eyes contain numerous units called omma-

tidia, where each ommatidium has its own lens and cor-nea. Compound eyes can be either stalked (housed onpurpose-formed extensions of the cuticle), as in crabs(ground-pattern feature of Malacostraca), or sessile (lying‘flush’ with the surrounding cuticle), as in isopods (auta-pomorphy of this eumalacostracan taxon) or pterygoteinsects (ground-pattern feature of Insecta) (Bowman,1984). Compound eyes can be further divided into func-tional groups depending on how light rays are focusedand how an image is formed on the retina (Nilsson,1989). This classification is based on information fromthe focusing system (the cornea and lens), the structureof the juxtaposed ommatidia, and the arrangement of thephotoreceptor cells, or rhabdoms. Apposition compoundeyes, for example, possess ommatidia, of which eachsees a specific and exclusive sector of the environment.A picture of the environment is constructed from the

combination of these sector images.The cornea in the eyes of most extant aquatic arthro-

pods cannot perform the role of focusing because it hasno refractive power. It may, however, contain filters(ommachromes, carotenoids or pteridines), or may haveanti-reflection properties, although these are more impor-tant in terrestrial species (Land and Nilsson, 2002).

Extinct eyesAmong Cambrian arthropods, trilobites are famous

for possessing a prominent, well preserved visual sys-tem. This has attracted attention in terms of their indica-tors of environment/lifestyle and the effect of the firsthighly mobile predators with eyes on Cambrian ecosys-tems (e.g. Parker, 1998, 2010). These visual predatorswere probably trilobites, about 521 Ma (Parker, 2003,2010). The plesiomorphic eye type in trilobites – theholochroal eye – certainly dates back to the upper lowerCambrian (Clarkson, 1973), and probably functionedlike apposition compound eyes (Fordyce and Cronin,1993; Schoenemann, 2007). Some trilobites were able to

Andrew R. Parker et al.252

achieve stereoscopic vision in a single eye (Stockton andCowen, 1976). There is a major difference between allliving euarthropod compound eyes and those of all trilo-bites: lenses today are organic whereas those of trilobiteswere calcitic (e.g. Towe, 1973; Clarkson and Levi-Setti,1975; Schoenemann, 2007), most likely an autapomor-phy of this taxon.

More compound eyes are evident in many Cambriannon-trilobite euarthropods, such as several taxa from theMaotianshan Shale faunas (lower Cambrian, China) orthe Burgess Shale-type faunas (middle Cambrian, forexample, British Columbia, Canada) (e.g. Whittington,1974; Ramsköld et al., 1997; Hou and Bergström, 1997;Liu et al., 2007; Schoenemann et al., 2009; Lee et al.,2011; Paterson et al., 2011; Schoenemann et al., 2011).However, the lack of scientific attention given to theseeyes may be attributed to their less easily resolved, two-dimensional preservation.

‘Orsten’ fossils and their preservation‘Orsten’ fossils, the majority described from upper

middle to upper Cambrian limestone nodules from south-ern Sweden, have preserved an abundance of phos-phatized cuticle-bearing euarthropods in three dimen-sions (e.g. Müller and Walossek, 1991; more recentoverview in Waloszek, 2003a, b; Maas et al., 2006).These fossils, now known from the lower Cambrian toLower Ordovician and from various continents reflectingthe early microcontinents north of the huge southernGondwana supercontinent (Canada, Balto-Scandianshield, Siberia, China and Australia, Maas et al., 2006),can be isolated from their rock matrices using 10% aceticacid, revealing cuticular surfaces in full detail. Hairs,bristles and sensillae thinner than 0.3 μm, pores of sen-sillae and gland openings, and even cellular surface pat-terns are evident in ‘Orsten’ fossils. No specimen of thearthropods recovered from this type of preservation lon-ger than 2 mm has been found so far, and consequentlymost species are considered as bottom-living meiofaunalanimals, so representing minute adults and many larvae(e.g. Müller and Walossek, 1991; Waloszek, 2003a, b).‘Orsten’-type fossilization is variable, but in all cases theouter layer of arthropod cuticle (epicuticle) seems tohave been replaced by phosphatic matter; this is the rea-son for the preservation of fine detail. Generally, the inte-rior of the fossils is empty or filled by amorphousphosphatic matter. “Steinkern”-like preservation is veryrare (e.g. internal fillings of the trunk skaracarid speci-mens, Müller and Walossek, 1985, their plate 17.1–4).

‘Orsten’ fossils represent a full suite of arthropodsranging from lobopodians (Maas et al., 2007) to tardi-grades (Müller et al., 1995), chelicerates (Waloszek andDunlop, 2002) and different crustaceans (e.g. summarized

by Waloszek, 2003a, b). Also, derivatives of the stem lin-eage toward the Eucrustacea (= crown group) have beenuncovered (e.g. Müller and Walossek, 1986; Walossekand Müller, 1990; Stein et al., 2008; Haug et al., 2009,2010a, b; Castellani et al., 2012). An example of the lat-ter taxon set is Cambropachycope clarksoni Walossekand Müller, 1990 (Figure 1).

The adult Cambropachycope clarksoni is only about1.5 mm long and bears relatively large paddle-shapeduniramous trunk limbs and a trunk constricting into along spinelike end. The distal parts of the tubular firstantennae and some other head-limb parts are littleknown, preventing an accurate determination of its feed-ing mode. Details of the limb parts of its sister species,Goticaris longispinosa Walossek and Müller, 1990, how-ever, indicate that this animal might have been an activepredator (Haug et al., 2009). Remarkably neither C.clarksoni nor G. longispinosa possess a well developedhypostome, but their mouths open freely on a smallhump on the ventral body side between their second headlimbs. The most significant character and synapomorphyof C. clarksoni and G. longispinosa is that the head con-stricts anterior to the mouth, forming a large bulbousextension projecting anteriorly. In both C. clarksoni andG. longispinosa this bulbous projection of the head hasan anteriorly turned ventral hook and elongates dorso-caudally in a cone (like a race-cyclists’ helmet). Minordifferences occur only in the larger height of the projec-tion of C. clarksoni, giving it a high oval cross section,while the projection of G. longispinosa is more or lesscircular in diameter (Haug et al., 2009).

A potential ‘Orsten’ eyeBoth C. clarksoni and G. longispinosa possess a mul-

tifaceted structure on their anterior projections that hasbeen presumed to be a compound eye in the first descrip-tion of these taxa (Walossek and Müller, 1990), a viewsubsequently supported by Haug et al. (2009). This struc-ture occurs on the anterior margin of the bulbous projec-tion occupying between one-tenth and one-third of itssurface area. Measurements on size and facet numbershave been made to distinguish stages (Haug et al., 2009),and further attention has been given to this faceted struc-ture with regard to its optic system, which is believed tofunction as an apposition compound eye (Schoenemann,J. T Haug, Parker, Waloszek, Maas, Castellani, C. Haugand Clarkson, pers. comm.). Specimens of C. clarksoniand G. longispinosa are comparatively rare with respectto numbers and numbers of samples in which theyoccurred relative to other Swedish ‘Orsten’ taxa, e.g.Rehbachiella kinnekullensis (Walossek, 1993), Agnostuspisiformis (Müller and Walossek, 1987), or the two spe-cies of Skara Müller, 1983 (Müller and Walossek, 1985;

A Cambrian (Orsten) arthropod cornea 253

about 100 specimens found of each species in the mean-time). Yet one relatively complete and uncoated putativeeye of C. clarksoni, with an apparently well preservedcornea, was made available for study. The aim of thisinvestigation is to examine the cornea of the putativecompound eye of C. clarksoni in detail, since such three-dimensionally preserved corneas from non-trilobite Cam-brian fossils are extremely rare. The external morphologyand any internal anatomy of the preserved cornea werestudied at high magnifications and using a variety ofmethods in order to abstract the maximum informationpossible from such a minimal amount of ancient structure.

Materials and methods

The material examined was an eye of Cambropachy-cope clarksoni from zone 1 of the Swedish alum shalesequence [new correlation after Peng et al. (2004)] inthe Kinnekulle area (sample no. 6780), Västergötland,Sweden (UB W138; held at the Institute of Palaeontology,Bonn, Germany). Its facet pattern would correlate best togrowth stage 5 of Cambropachycope clarksoni, but as itmeasures about 500 μm long it would appear too largeto be assigned to this stage. Such a size is only reachedby the largest specimens, thus stage 7. Also the compari-son of the facet pattern is complicated by the fact that thesepatterns appear differently in the SEM images of coated

specimens compared to the light microscopy images.The ‘eye’ was photographed from different angles

under a reflected-light microscope. Then groups of threeor four facets were removed and each subjected to oneof the following analyses. A group of facets was placedin a drop of distilled water and photographed at 1,000times magnification under a transmitted-light micro-scope. A second group of facets was embedded in waxand 1 μm sections were cut. The sections were stainedwith Toluidine Blue, examined under a transmitted-lightmicroscope and drawn using a camera lucida. The sec-tions were covered in a mounting medium (DPX) and bya cover slip, and re-examined.

A third group of facets was subjected to further inter-nal analysis using a transmission electron microscope(TEM). In preparation for the TEM, the facets were (i)treated with 2.5% glutaraldehyde in 0.1 mol/l phosphatebuffer for 1 hour at room temperature (23°C), (ii) rinsedwith 0.1 mol/l buffer, (iii) treated with 1% osmium tetrox-ide in 0.1 mol/l buffer for 1 hour at room temperature, (iv)dehydrated through an ethanol series, and (v) infiltratedwith Epon resin through a resin-ethanol series (each dilu-tion treatment took place overnight on a rotator). Sections60 nm thick were cut from the embedded facets.

A fourth group of facets was gold-coated and exam-ined in a scanning electron microscope (SEM) so as tobe able to study internal and external surfaces and

Figure 1. Computer reconstruction of C. clarksoni, whole animal, antero-lateral view, based on a stage 5 specimen.


exposed cross-sections. A fifth group of facets was sub-jected to X-ray analysis to determine their chemical com-position. For X-ray analysis the facets were carbon-coatedand examined using an Oxford Link Isis 200 energy dis-persive spectrometer (with a silicon/lithium detector andberyllium window) that detects elements with an atomicmass above that of oxygen (e.g. excludes carbon).Results were interpreted using Speedmap software (mapbased on counts alone, with no element corrections).

Results

External characteristicsThe putative eye of Cambropachycope clarksoni was

three-dimensional and solid but only its cornea has been

preserved; the internal parts including most of the lensand the rhabdoms are missing. The eye contains 95 rec-ognisable ommatidia, where the cornea of each omma-tidium is evident as a circular shape in external view, andwhere these circular shapes are hexagonally close-packed (Figure 2). No pentagonal or square-shaped fac-ets are apparent. The eye is approximately symmetricalabout a central vertical plane, being slightly higher thanwide (Figure 2D). The diameters of the cornea of eachommatidium vary from 19 to 48 μm. Generally they arelarger dorsally, although the largest ommatidia are thosejust dorsal to the horizontal central position, on the ver-tical symmetrical axis (Figure 2D). There are spacesbetween adjacent circular corneas (the “intra-lensarsclera”), which are only recognisable in light micros-

Figure 2. Anterior projection of Cambropachycope clarksoni, containing the putative single compound eye from different views. A–C, light micrographs; A, almost lateral view, in reflected light; anteroventral surface to the left; B, C, individual facets (corneas of ommatidia)in transmitted light, intra-lensar sclera is pale, relatively thin and has cracked irregularly; D, drawings from three views: dorsal, anterior andleft lateral. Scale bars: A = 0.1 mm, B and C = 15 μm.


copy; coated specimens do not allow the recognition ofthese areas. The intra-lensar sclera is in the order of 10μm wide. The corneas appear reddish brown in transmit-ted light, while the intra-lensar sclera appears pale yel-low (Figures 2A–C). When the cornea cracked, it brokecleanly along the intra-lensar sclera and never in theommatidial regions (Figures 2B, C). This suggests thatthe intra-lensar sclera is thinner than the cornea of theommatidia. The cornea of each ommatidium has aslightly convex outer surface, and very slightly convex(almost flat) inner surface.

Internal characteristicsThe cornea has a thickness of 4–5 μm and is divided

into three layers. The outer corneal layer is about 3 μmthick (slightly thicker towards the centre of the circularcornea) and has an extremely smooth outer surface (theoutermost surface of the eye) at the submicron level (Fig-ure 3C). This layer is transparent to light and electron

beams and is mechanically rigid. It has a fibrous con-struction, as observed where its outermost surface isremoved (Figure 3D). The individual fibres have a diam-eter of approximately 45 nm, and are spaced between 20and 200 nm. They are arranged randomly rather thanperiodically or subperiodically. The inner layer is similar,also with a smooth surface (the innermost surface of thecornea) at the submicron level (Figure 3B), but thinner,approximately 1.5 μm thick. Nodules have formed on theinner surface as artefacts (Figure 3A, B). However,attached to this surface, in the region representing thecentre of the circular cornea, are fibres an order of mag-nitude thicker belonging to another structure (Figure3A). Five ommatidia were examined, and all revealedthis character.

The middle layer of the cornea is the thinnest, about0.16 μm, and is physically hollow, although most of thespace is filled with an electron-dense material thatappears with smooth, meniscus-like edges in thin sec-

Figure 3. Scanning electron micrographs of the cornea of a single ommatidium of the putative eye of Cambropachycope clarksoni.A, an overall picture of the internal view, where the centre of the facet is to the left of the specimen (the large piece of material attached isaround the centre of the facet); B, a high magnification of the smooth region in (A); C, the external (outermost) corneal surface, from anangle of 35° to the surface; D, a higher magnification of the broken area in (C), revealing the felt work of fibrils that do not scatter incidentlight and provide transparency. Scale bars: A and C = 10 μm, B and D = 2 μm.


tions (Figure 4). This material appears reddish-brown toblack in transmitted light, and dark brown to black inreflected light, appearing similar to some melanins,ommachromes, carotenoids and pteridines as viewed inextant arthropod cuticle, for example. When stained withToluidine Blue the outer layers of the cornea appeared

blue and the middle layer red. However, when the slide-mounting medium (DPX) was added, the middle layeralso rapidly and evenly turned to blue. The colourationof the middle layer appeared to account for the regularcircular patterns of the cornea observed externally, pro-viding contrast against the intra-lensar sclera. The dorsalfacets are noticeably darker than the ventral facets; thereis a systematic decrease in darkness of the facets fromdorsal to ventral. Also, the central facets are slightlydarker than the lateral facets with the same horizontalplane. This general difference in shade can again beattributed to the thickness of the middle corneal layercontaining a dark material.

The middle layer is absent in the intra-lensar scleraand in the cuticle of the “eye” projection surrounding theommatidia. In these regions, the cuticle does not appearlayered in cross-section.

Element analysesX-ray mapping of the outer surface of the cornea

revealed widespread calcium and phosphorus with highcoincidence. The highest levels of both calcium andphosphorus occurred in the interommatidial spaces, orintra-lensar sclera, although both elements occurred inthe same proportion within the cornea of the circularommatidia as in the intra-lensar sclera. The elements alu-minium, potassium and sulphur were detected inextremely minor amounts, and iron, sodium and manga-nese were absent. More interestingly, relatively high lev-els of silicon were detected from the middle layer of thecornea when a cross-section of the cornea was examined.This middle layer also revealed a different proportion ofphosphorus and calcium due to a relative reduction inphosphorus; the ratio of phosphorus: calcium approxi-mately halved.

Discussion

The present investigation on the single isolated eye ofCambropachycope clarksoni gives slightly differentresults from the SEM investigations on other specimens;the number of ommatidia was greater in some smallerspecimens investigated in SEM (Haug et al., 2009). Onlythe very largest specimens known of C. clarksoni reachan eye size comparable to the investigated specimen, butthose have almost 150 facets (Haug et al., 2009). Addi-tionally these specimens proved to be incomplete con-cerning the anterior-posterior axis, i.e., the entire lengthof the posterior part of the projection appears not to havebeen preserved; this is probably also the case for theinvestigated specimen. Whether the difference in facetnumber can be explained by the nonrecognition of themarginal smaller facets or whether this special specimen

Figure 4. Cornea of an ommatidium of the putative eye ofCambropachycope clarksoni in cross-section. A, camera lucidadrawing of an oblique section, 1 μm thick, through a completecornea of an ommatidium; the stippled areas represent the middlelayer of the cornea, presumed to be a once continuous layer thatis now broken, which appears black in B and C. B, transmissionelectron micrograph of a section through an almost complete cor-nea of a single ommatidium; C, higher magnification of theregion at the very left of (B). The liquid in the middle layer of thecornea appears black (= electron-dense). Scale bars: A = 10 μm,B = 6 μm, C = 1 μm.


indeed bore fewer facets, perhaps due to a difference insex, cannot be answered.

Despite these difficulties, the results suggest that theanterior projection of C. clarksoni had a morphologysuited to collecting light and forming images, i.e., that itwas an apposition compound eye (Schoenemann, J. THaug, Parker, Waloszek, Maas, Castellani, C. Haug andClarkson, pers. comm., where the whole eye apart fromthe ultrastructure of the cornea was considered).

General anatomy of the corneaThe cornea of the eye of Cambropachycope clarksoni

is relatively thin by comparison with that of recentarthropod compound eyes, and shows only small varia-tions in thickness. The cornea of each ommatidium isonly very shallowly convex at its outer surface andalmost flat at its inner surface, and therefore probablycould not function as a lens on its own, also consideringthe low contrast in refractive indices between the chitinof the cornea and surrounding water. When also takinginto consideration the refractive index range possible inbiological material, this curvature would not be sufficientto focus light onto a retina within the anterior projection,but rather at a focal plane several times further away.Therefore we can assume that a lens, performing most ofthe focusing power of the eye, lay behind the cornea. Thefibres attached to the inner surface of the cornea areprobably the remnants of the original lens, which wouldhave been joined with the cornea. These fibres occur atthe centre of each circular-shaped ommatidium, addingfurther evidence to this hypothesis.

The smooth outer surface of the cornea, and lack ofmultiple internal thin layers (around half the wavelengthof light in thickness), suggests there are no antireflectivestructures present that would increase the capture ofavailable photons (Parker et al., 1998). However, mostmarine animals lack these characters since water has aconsiderably higher refractive index than air (1.33 com-pared to 1.0), reducing the optical contrast between thecornea (with a refractive index higher than 1.33) and thesurrounding medium. Hence aquatic animals suffer lessfrom light lost via surface reflections from the cornea.

Transparency of the corneaThe inner and outer layers of the cornea of C. clark-

soni have a very different construction to the corneas offossil trilobites, where precisely orientated crystals ofcalcite provide transparency (Towe, 1973; Clarkson andLevi-Setti, 1975; crystalline materials most closelyapproach the condition of a uniform refractive index nec-essary to minimise scattering; Miller, 1979). The mate-rial of the bulk of the cornea is comparable to“Bowman’s layer of cornea” (Miller, 1979) where the felt

work of fibrils, at a similar scale and organisation tothose in C. clarksoni, do not cause light to be scatteredand provide transparency in the cornea. The Bragg rela-tion for scattering by a three-dimensional lattice is

Sin θ = mλ/2d

where θ is the diffraction angle for light of wavelengthλ incident perpendicularly on the cornea, d is the spacingof the fibrils, and m is the order of diffraction (an inte-ger). For m ≥1 the grating equation cannot be satisfiedbecause d<λ for ultraviolet (UV-A) to red light (even tak-ing into account the effect of the refractive index of thefibrils, within the range of that known for biologicalmaterials). Therefore scattering in the cornea of C. clark-soni would have been minimal, and the cornea wouldhave been transparent to light. Transparency of the cor-nea is consequential for the absolute sensitivity functionof the receptors because maximal intensity at the receptorand lack of scatter (glare) are important for contrastdetection and visual acuity (Miller, 1979).

ChemistryThe high levels of calcium and phosphorus in the cor-

neal material suggests the presence of a calcium phos-phate mineral (apatite). As no chlorine was detected, theparticular apatite involved could be fluorapatite (withfluorine) or hydroxylapatite (with hydroxyl) but fluorap-atite is more probable. This is consistent with the knownpreservation of other ‘Orsten’ fossils, where fluorapatitereplaced the original organic material (Walossek andMüller, 1998). Fluorine and oxygen were not detectedsince they are beyond our detector window’s light ele-ment limit. In general, the outer layers of the cornea arevery uniform in composition, and different to that of themiddle layer. The middle layer revealed a relative reduc-tion in the proportion of phosphorus, and high levels ofsilicon. This is surprising because silicon has not beenfound in the ‘Orsten’ material previously (unpublisheddata).

Limitations in the range of elements detected by themethods employed (particularly the exclusion of carbon)are compounded by the unknown effects of fossilisationand diagenesis. The degree of replacement mineraliza-tion is uncertain as far as the middle layer of the corneais concerned. The eye examined may have been prefer-entially replaced or impregnated in a postmortem fashionby secondarily deposited minerals, or the mineralsrevealed here may have been those present in the livinganimal.

Middle layer of the corneaThe dark-coloured material, or rather the presence of

a thin middle layer, is the most unexpected and enigmatic


feature of the C. clarksoni cornea. Since the middle layer(and dark material) is absent in the intra-lensar sclera andin the cuticle of the “eye” projection surrounding theommatidia, this layer does appear to be a character of anon-moulting individual rather than an artefact (ofmoulting or preservation). The contents of this middlelayer, however, are probably not original.

The middle layer probably did not contain a dynamicscreening pigment, since no possible means of controlover pigment dispersal are evident. The dynamicallycoloured corneas of some fishes employ chromatophores(e.g. Orlov and Kondrashev, 1998), but no such charac-teristic cells or their lacunae are evident in the cornea ofC. clarksoni. The compound eyes of many extant marinecrustaceans also possess screening pigment to adapt todifferent levels of light in the environment (such as atdifferent times of the day or between clear and cloudydays) (e.g. Nilsson and Nilsson, 1981; Donner et al.,1994), however usually this pigment is housed betweenthe ommatidia and/or in the body of the retinal cells(Mazokhin-Porshnyakov, 1969; Hallberg and Elofsson,1989).

One possible function for this middle layer is that ithoused a light filter. Pigmented filters in extant arthro-pods usually consist of ommachromes, carotenoids orpteridines (Marshall et al., 1991; Land and Nilsson,2002). However, these are reactive compounds which aredegraded quickly after death – in freshly killed speci-mens the rapid degradation of these pigments can beobserved in a matter of days. Also, in the fossil C. clark-soni cornea, high levels of silica were detected in themiddle layer, indicating that the material has changedfrom the original. Nonetheless, this separate, thin layerwithin the cornea may have originally housed a filter.Further, the dark-coloured material that fills the middlelayer in the fossilized C. clarksoni specimen does appearto have an oil-like consistency, given its meniscus-likeedges where the layer is pulled apart and its rapid (nearinstantaneous) and thorough colour change when it wasstained with Toluidine Blue and then put in contact withDPX mounting medium. A solid material would beexpected to take longer to absorb the viscous mountingmedium, albeit the sections of the cornea were extremelythin. Interestingly, DPX breaks down pigments (but notchitin) in butterfly scales.

The majority of extant animals with pigmented visualfilters house their pigments (coloured oil droplets) inparts of the eye other than the cornea, particularly in theretina (e.g. Marshall et al., 1991; Vorobyev et al., 1998).In some extant Diptera (Arthropoda), multilayer reflec-tors rather than pigmented filters occur in the outerregion of the cornea, although they provide a similarvisual effect (Bernard and Miller, 1968). However, in

some non-arthropod marine animals (fish), a yellow pig-ment (a coloured oil) does occur in the cornea, and isknown to act as an eyeshade against the glare source ofdownwelling light (Moreland and Lythgoe, 1968). Thedorsal facets of C. clarksoni are noticeably darker thanthe ventral facets; there is a systematic decrease in dark-ness of the facets from dorsal to ventral. This could sug-gest a similar “eyeshade” function for the original middlelayer in C. clarksoni.

Alternatively, yellow pigments in the corneas of someother fishes are also known to function to significantlyreduce chromatic aberration by absorbing the shorterwavelengths (including ultraviolet A) (the Rayleigh scat-tered light), although probably this only improves visi-bility of very distant objects (Muntz, 1972) (and may notbe relevant to an apposition eye since all light is focusedon to the rhabdom anyway). The probable lifestyle of C.clarksoni was that of a pelagic predator, feeding onsmaller prey, which it detected by their smaller light sig-nals (at relatively long distances) (Schoenemann, J. THaug, Parker, Waloszek, Maas, Castellani, C. Haug andClarkson, pers. comm.). In this scenario, a yellow/orange/red filter would enhance the appearance of the smallestlight signals in the sea (those of its potential prey) by fil-tering out the “noise” or haze created by the scatteredblue light from sunlight. Here, one would expect to findthe filter enhanced in the upper (dorsal) ommatidia,which receive a greater incidence of blue rays from sun-light. This is indeed the case in C. clarksoni. Certainly,if the middle layer of the C. clarksoni cornea did containa yellow filter to absorb the shorter wavelengths of light,then it must have lived where the longer wavelengthsexisted, i.e., near to the surface of the water (Clarke,1933; Denton, 1990). However, some fishes are knownto employ yellow corneal filters to distinguish (via wave-length filtering) between bioluminescent light and sun-light at depths where sunlight becomes predominantlyblue (i.e., below about 200 m) (Clarke, 1933; Denton,1990).

Until further specimens of the corneas of C. clarksoniand its close relatives are examined, using additionaltests to those performed here, the function of this enig-matic middle layer of the cornea cannot be ascertained.However, the presence of this thin middle layer certainlysuggests that some form of filter did exist in the corneaoriginally.

Acknowledgements

We thank the late Klaus J. Müller, Bonn for access tothe eye of Cambropachycope clarksoni examined in thisproject and Andreas Maas, Ulm, for help with specimenpreparation. This project was funded by The Australian


Research Council and The Royal Society (London). JTHwas funded by the German Science Foundation (DFG)under Wa754/15-1 and is currently supported by theAlexander von Humboldt Foundation with a FeodorLynen return fellowship.

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