Retained colour pattern on the shells of Plectodonta sp. from the earliest Devonian of Podolia (Ukraine) is the first finding for strophomenide brachiopods and the oldest among articulate brachiopods. The colour pattern in Plectodonta sp. is composed of small, round, brownish spots scattered rather irregularly on the ventral valve only. This may suggest that the described pattern probably performed a protective function through disruptive camouflage against visual systems of potential predators. The occurrence of the colour pattern in Plectodonta sp. exclusively on the ventral valve strongly suggests that these brachiopods lived with the patterned (and convex) ventral valve upwards and the patternless concave dorsal valve facing to the underlying substrate. It thus contradicts a general assumption that concavo-convex brachiopods lived with their convex valves resting on the sediment.
Fossil invertebrates revealing some genuine colouration (when pigment is distributed more or less uniformly within shell matter) or colour patterns (when pigment is concentrated or arranged in bands, lines, spots, patches, etc.) are rather rare because a variety of factors destroys original colouring of the shells during the process of fossilisation. On the other hand, Blumer (1965) remarked that organic pigment compounds from plants and animals are preserved as molecular fossils in a wide range of geologic materials, often of great antiquity. Fossil brachiopods retaining colour pattern are of great interest especially when they come from rocks hundreds of millions years old. Although records of colour pattern in Devonian brachiopods are numerous (see list of citations in Blodgett et al. 1983; Kobluk and Mapes 1989) they invariably exemplify an exceptional state of preservation.
Devonian articulate brachiopods retaining colour markings are represented by eight taxa of Rhynchonellida, six taxa of Athyrididina, and 28 taxa of Terebratulida (see Boucot and Johnson 1968; Blodgett et al. 1983, 1988; Biernat 1984; Baliński 1985; Johnson 1986). The previously oldest articulate brachiopods with preserved colour patterns came from the middle Early Devonian. These are the athyridoid Merista Suess, 1851 (Křiž and Lukeš 1974) and two terebratulid genera ?Prionothyris Cloud, 1942 (Murphy 1972) and Beachia Hall and Clarke, 1893 (Blodgett et al. 1988). No Devonian representatives of the order Strophomenida have been reported to retain the colour pattern. The aim of this report is to illustrate specimens of Plectodonta sp. from the earliest Early Devonian of Podolia, which are the first strophomenides and the oldest articulate brachiopods known to the author retaining shell colour pattern.
Colour-patterned fossils have a great potential value for palaeoecologic, palaeogeographic, evolutionary, and taxonomic purposes (Nicol 1967; Blodgett et al. 1983, 1988; see also Newton 1907; Foerste 1930; Kobluk and Mapes 1989; Hagdorn and Sandy 1998; Manda and Turek 2009; Turek 2009). For example, remarkable pattern consistency of a single pair of radial bands on the brachial valve in Beachia and ?Prionothyris prompted Blodgett et al. (1983, 1988) to regard this morphologic feature as a supplementary diagnostic for at least part of the subfamily Eurythyridinae Cloud, 1942.
Institutional abbreviation.—ZPAL, Institute of Paleobiology, Polish Academy of Sciences, Warszawa, Poland.
Material and methods
All material presented here was collected from beds 47–48 representing the lowest part of the Khudykivtsi (former Tajna) Member, about 5.5 m above the Silurian—Devonian boundary, exposed in a trench near the village of Dnistrove (former Volkovtsy) in Podolia (Ukraine; see Małkowski et al. 2009 for details on the locality). The specimens of Plectodonta sp. with retained colour pattern occur in a single fossiliferous interval measuring about 18 cm in thickness and belonging to an otherwise poorly fossiliferous, monotonous, 180 m thick complex of platy limestones and variably interbedded dark grey argillaceous shales, marls and marly to micritic limestones extending from the base of the Lower Devonian through the Khudykivtsi to the top of the Mytkiv members. Beds 47–48 are remarkable in their relatively rich, well-preserved, and taxonomically diversified brachiopod fauna. The fauna yields 15 species, of which the most characteristic are Resserella elegantuoides (Kozłowski, 1929), Dalejina frequensis (Kozłowski, 1929), Plectodonta sp., Glossoleptaena sp., Clorinda pseudolinguifera Kozłowski, 1929, Sphaerirhyncha gibbosa (Nikiforova, 1954), Lanceomyonia borealiformis (Siemiradzki, 1906), and Septatrypa (Septatrypa) secreta Kozłowski, 1929 (systematic description of the brachiopod fauna from the locality will be published elsewhere). Nearly 170 specimens of Plectodonta sp. were recovered from beds 47–48, of which 92 retain variably preserved colour pattern. This species is externally very close to Plectodonta mariae Kozłowski, 1929 which occurs in a slightly younger horizon representing the Mytkiv Member (upper part of the Borshchiv Horizon). Plectodonta sp. illustrated here is persistently smaller, has less numerous primary costellae, and deeper, more restricted ventral sulcus. According to Nikiforova et al. (1985) the species from the Khudykivtsi Member is not conspecific with P. mariae from Mytkiv Member. This species will be studied and described taxonomically in detail elsewhere.
The colour pattern of Plectodonta sp. consists exclusively of spots (Figs. 1A–C, E–G, 2). They are scattered more or less evenly, although irregularly, over the whole surface of the valve except for the most posterior 0.4–0.6 mm (umbonal region). On some specimens the spots reveal a weak subradial arrangement but this condition is rather rare and obscure. Usually the size of the spots does not change much during ontogeny although on some shells the spots around the anterior margin are slightly larger from those situated more posteriorly (Fig. 1E). Rarely, some spots show a tendency to coalesce to form larger, irregularly outlined patches (Figs. 1A, F, 2G, R, AG). Spot density varies in a rather wide range from 7 to 17 per mm2 and averages at 11 spots per mm2. It seems that spot density is more or less uniform over the whole surface of the valve excluding the spotless umbonal region.
The spots are more or less circular in outline, light to dark brown in colour, darkest in their centre and gradually fading away peripherally. The diameter of the spots varies over a wide range from 0.06 to 0.25 mm but most often averages about 0.15 mm. The variability of the pattern and character of the distribution of spots as observed on the 40 best preserved ventral valves are shown diagrammatically on Fig. 2.
One of the most appealing features of the material presented here is the fact that all of the examined colour pattern-bearing shells have this feature retained exclusively on the ventral valve. Although several specimens have the dorsal valve well exposed none of them has the colour pattern clearly visible (Fig. 1D). In the studied material there is a remarkable specimen of a small rock slab showing on one surface two specimens of Plectodonta sp. with exposed ventral valves and one shell with a dorsal valve visible (Fig. 1G): all of the former show distinct colour pattern, whereas the latter does not show any perceptible pattern. This rock slab clearly supports the observation that the colour pattern in Plectodonta sp. was probably restricted to the ventral valve only.
Reimann (1945) noted that some dark coloured radial pattern observed in a few Meristella species from the Middle Devonian of New York was caused by differential absorption and reflection of light by the corrugated prismatic shell layer. In consequence, the angle of view affects the appearance or disappearance of the pattern on such specimens. On the other hand, the appearance of the colour pattern which is caused by a presence of a real pigment or its remnants within shell substance is not affected by the angle of view. Parker (2000: R15) discussed the array of structural colours (selective reflectance of light by the physical nature of a structure) found in animals as early as the Cambrian. Towe and Harper (1966) described iridescent pearly or nacreous lustre in Devonian pholidostrophiid brachiopods that resulted from the crossed lamellar shell structure. Yet some types of colouration or colour patterns of fossil exoskeletons may have been the result of diagenetic alteration (e.g., Klug et al. 2009; Turek 2009). These kinds of colour patterns or colourations should not be confused with the undoubtedly genuine colour retained in fossils. The colour-spotted pattern in Plectodonta sp. described here is an example of the last case, i.e., it is caused by retention of a pigment derived from original colour and embedded in the shell matter. Noteworthy is that the colour spots are equally visible from the exterior of the valve as on its interior. This suggests that the colouring substance, as presently preserved, occurs not superficially but is embedded within the shell substance.
There are several kinds of colour patterns which can be found in fossil and Recent articulate brachiopods. One of the most common is radial banding which has been found in the rhynchonellides, athyridides, and terebratulides (Fig. 3E–G, I). Concentric bands are described in orthotetides, productides, athyridides, and terebratulides (Fig. 3B, C, J). Among the Devonian brachiopods with preserved pattern 25 have radial and 5 concentric banding (Blodget et al. 1983). Spotted patterns have been recognised in productides, rhynchonellides, terebratulides, and, in this paper, strophomenides (Fig. 3A, B, D, H). Frequently, the spots are arranged radially, or, as in the Middle Devonian Solidipontirostris radwanskii Biernat, 1984, the spots and bands can form a spectacular pattern (Biernat 1984; Fig. 3D). Rarely, spots are combined with banding (Fig. 3B, D). In some brachiopods, the colour pattern consists of large irregular patches, as is observed in the Recent terebratulid Shimodaia MacKinnon, Saito, and Endo, 1997 (Fig. 3K).
Plectodonta is a member of the superfamily Plectambonitoidea, which is characterised by the presence of a pseudodeltidium, chilidium, and supra-apical pedicle foramen. According to an exhaustive description of a type species of the genus, i.e., P. marine Kozłowski, 1929 given by its founder, this pedicle foramen, although comparatively small, was fully functional at earlier growth stages, but then became sealed off and nonfunctional in adults (Kozłowski 1929). The diameter of the foramen in P. mariae, as given by Kozłowski (1929), ranges from 0.08 to 0.1 mm. In a few specimens presently studied, in which the pedicle foramen is preserved satisfactorily enough, it attains up to 0.06 mm in diameter. Thus, at an earlier ontogenetic stages Plectodonta had a functional pedicle and was anchored to the substrate. At the adult stage, however, individuals lost the pedicle and became free-living. Generally, it is assumed that free-living concavo-convex brachiopods rested on the soft sediment on the convex valve (e.g., Rudwick 1970). However, Lescinsky (1995) presented epibiontic and taphonomic evidences that concavo-convex orthides and strophomenides lived on probably firm mud bottoms with the convex valve on top.
As described above, the colour pattern of the studied shells of Plectodonta sp. is confined to the ventral valve. This may suggest that the life position of the brachiopod was with the patterned (and convex) ventral valve uppermost and the patternless concave dorsal valve lying next to the underlying substrate. This is in agreement with the general life position of many living (as well as fossil) brachiopods with a functional pedicle whose shell is inclined above the substrate with ventral valve uppermost. At the adult stage, however, when individuals of the species lost their pedicle, the thickened posterior region of the shell might have helped them maintain a preferred orientation, presumably still with the colour-patterned and convex ventral valve uppermost. The presence of the colour pattern exclusively on the ventral valve seems so meaningful that it justifies supposition of yet another and unknown (not preserved on the shell exterior) mode of anchoring in some adult plectambonitoids which enabled them to stabilise the orientation of the shell above the substrate (for example, by cementing with a short, thin organic pad secreted by a gradually atrophying pedicle).
The colour-patterned ventral valve of Plectodonta sp. suggests also, that the pattern may perform a protective function through mimicry or a kind of disruptive camouflage. This brachiopod lived in shallow waters (photic zone) where a patterned body cover might perform an important protective function against the visual systems of potential predators. Irregularly scattered spots probably blurred the shell outline and distracted potential predators. In other words, the predator's “searching image” (a few visual characters which enable the predator to recognise pray; see Wicksten 1983) may be seriously disturbed by patterned shells of Plectodonta sp. as potential prey. Protective function of a camouflage seems to be strongly linked with the development of vision in predators. Kobluk and Mapes (1989) suggest that vision capable of discerning form and colour pattern developed as early as the Late Ordovician. Since then camouflage served as a valuable protective function (Kobluk and Mapes 1989: 75). It needs to be mentioned, however, that the suggested function of the pattern was possible only when the outermost organic shell layer in Plectodonta sp., i.e., periostracum, was thin enough and did not obscure the visibility of the spots. Indeed, a fully developed periostracum in living brachiopods is extremely thin measuring usually up to 5–6 µm in thickness (Williams et al. 1997) and, to a large extent, is translucent.
The occurrence of the colour pattern in Plectodonta sp. may be helpful in obtaining useful data about the probable bathymetrical zone of the sea in which the species lived. It has been noted long ago by Forbes (1854; see also Newton 1907, Foerste 1930, and Blodgett et al. 1988) that marine organisms with colour-patterned shells essentially inhabit shallow-water depths related to the photic zone. He noted that marine shelly fauna living below 100 fathoms (about 200 m; 1fathom = ca. 1.85 m) depth are quite white or colourless whereas those living from 50 fathoms shorewards have colours and patterns well marked (Forbes 1854: 21).
Distribution of colour-patterned marine invertebrates may also indicate a difference in temperature of water areas. As noted by Nicol (1967), Recent colour-patterned marine pelecypod shells are very common in warm tropical waters and quite common in temperate-water areas, whereas in cold polar regions colour-patterned shells usually do not occur and are rare on shells found in water that never exceeds 12°C. Blodgett et al. (1988) confirm this phenomenon within the distribution of the Devonian marine invertebrates. They noted that all colour-patterned forms occurred in either the Old World Realm or Eastern America Realm, i.e., roughly tropical—subtropical and warm—temperate belts, respectively. High latitude Malvinokaffric Realm of the Southern Hemisphere totally lacks marine colour-patterned invertebrates (Blodgett et al. 1988). Occurrence of colour-patterned brachiopods in the earliest Devonian strata of Podolia, which at that time was situated quite near the equator (Małkowski et al. 2009: fig. 8), supports this distributional model.
Numerous specimens of Plectodonta sp. described here from the earliest Early Devonian of Podolia are the first strophomenide and the oldest known articulate brachiopod retaining shell colour pattern.
The colour pattern of Plectodonta sp. consists of brownish spots scattered more or less evenly, although irregularly, excluding the spotless umbonal region. The pattern is caused by the retention of a pigment derived from original colour and embedded in the shell substance.
The colour pattern is developed exclusively on the ventral valves.
The colour pattern on the ventral valve of Plectodonta sp. might have performed a protective function through mimicry or a kind of disruptive camouflage against visual systems of potential predators. This suggests that the life position of the brachiopod was with the patterned (and convex) ventral valve uppermost and the patternless concave dorsal valve lying next to the underlying substrate.
Distributional characteristic of marine invertebrates with colour-patterned shells and carapaces supports the observation that Plectodonta sp. inhabited shallow and warm water areas.
I express my gratitude to Arthur J. Boucot (Oregon State University. Corvallis, USA) and Jisuo Jin (University of Western Ontario, London, Canada) for their thorough reviews, which improved the manuscript. The research was supported by a grant (No. N N307 057834) from the Ministry of Science and Higher Education to Hubert Szaniawski (Institute of Paleobiology, Warsaw, Poland).