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Comment on "Small Bilaterian Fossils from 40 to 55 Million Years Before the Cambrian"
Chen et al. (1) reported coelomate bilaterians from the 600-million-year-oldDoushantuo phosphorites in southern China. Such a find mightmeet some common expectations of small, simple bilaterians emergingafter the worldwide glaciations of the Neoproterozoic. The interpretationis not well founded, however, because it fails to take intofull account taphonomy (changes in the organism after death)and diagenesis (changes in the sediment after deposition).
The specimens presented by Chen et al. (1) represent a commonmode of preservation of microfossils in phosphatic sediments,including those of the Doushantuo (2) and the overlying Dengying(3) formations: a more or less undeformed outer membrane; ashrunken, irregular internal mass, often connected to the outermembrane by occasional threads or sheets; and thin layers ofdiagenetic mineral, commonly apatite (calcium phosphate), liningthe surfaces of the resulting cavities (Fig. 1). Such diageneticminerals usually have a characteristic crystallographic structuredue to the growth direction normal to the encrusted surface.Chen et al. have provided no information on the structure ofthe layers they interpret as cellular, but even the publishedfigures show clear evidence of diagenetic origin:
Fig. 1. Lingulate brachiopod Linnarssonia from Middle Cambrian phosphatized limestone in south Sweden (locality Kvasa, Scania). (A and B) Scanning electron microscopy pictures of broken specimen. Swedish Museum of Natural History (SMNH) Br138245. Posterior parts of dorsal (bottom) and ventral (top) valves preserved, together with shrunken soft tissues still connected by stretched threads or sheets to shell, mainly to areas of strong epithelial adherence (sites of muscle attachment). All internal cavities are lined by diagenetic apatite consisting of surface-normal acicular crystallites (ac), in places forming spherulitic fans (sph). (C to E) Thin section of similarly preserved specimen in limestone matrix. SMNH X1520 [also shown in figure 3, D and E, in (7)]. Plane-polarized light (C and D) and crossed nicols (E); frame in (C) indicates position of (D). Note layered structure of diagenetic lining, ordered crystallography [see polarizing cross in spherulite in (E)], inwardly convex spherulitic fans growing over irregularities on encrusted surface, absence of later-formed layer in narrow spaces [arrow in (C)], and surface-normal lineations (corresponding to direction of acicular apatite crystallites) crossing boundary between generations of diagenetic lining. This kind of diagenetic lining, also exemplified in (2), (3), and (6), is analogous to the purported cellular layers of the Doushantuo bilaterians as interpreted by Chen et al. (1).
[View Larger Version of this Image (132K GIF file)]
The layers have a regular banding of color and thickness thatis different between the specimens but consistent within theindividual specimens, whether counted from the outer wall inwardor from the central body outward. In the direction toward whatthey describe as the coelomic lumen, Chen et al. showed a thicknesssequence of approximately 2 + 2 + 5 µm [figure 1A in (1)];one of 3 + 5 + 5 µm, with the first layer considerablydarker than the subsequent two [figure 1B in (1)]; and one of2 + 5 µm [figure 1C in (1)]. This pattern defies + biologicalexplanation but is easily explained as representing two to threegenerations of diagenetic overgrowth (Fig. 1, C to E).
Ratherthan being sinuously folded, as would be expected fromdeformedtissue layers, the layers consistently have their convexfeaturesdirected toward the putative coelomic lumen. This isa typicalfeature of diagenetic crusts, in which irregularitieson theovergrown surface serve as nuclei for spherulitic fans(Fig. 1, B to E).
The layers show typical cavityfilling geometry.The outermostlayer is missing in narrow spaces where earliergrowth leftno room for it [compare, for example, figure 1B-1,lower part,in (1) and Fig. 1C, arrow, in this comment].
Thelayers show conspicuous dark lines perpendicular to thesurfaces.Chen et al. (1) refer to these as "cellular structurepreserved."Cellwalls may indeed be preserved in these sequences(35),typically by internal encrustation by diageneticminerals (6).Surfaceperpendicular lines within diagenetic crusts,however,more likely represent fine cracks propagated alongthe directionsof surface-normal acicular crystallites. Thefact that the linesin the specimens depicted by Chen et al.[for example, figure2, C and D, in (1)] commonly continue acrossthe boundariesbetween the layers is strong evidence that theyare propagatingcracks rather than cell boundaries.
Chen et al. concede that one thin partial coating of the layersis of diagenetic origin. They do not address, however, any ofthe clear indications of diagenesis in the main layers, butsimply assert that they represent cellular layers because theyhave been consistently observed in independent specimens ofthe same morphological organization and similar dimensions.In view of the fact that the supposedly bilaterian specimenshave been selected from among 50,000 to 100,000 microfossils,the perceived consistencies are far from impressive. The supposedmouth and anus are reported from two specimens each. The putativepharynx, gut, and coeloms are reported from all 10 selectedspecimens, but these features will be present by construct ifspecimens are selected that happen to have the internal lumpof shrunken matter touching or connected with the outer wallin two places in the plane of section. No information is given,other than conjecture, on the three-dimensional structure ofthe figured specimens, and there is no account of the variabilityof any of the 50,000 to 100,000 microfossils not selected asbilaterians. As a result, even a reader unacquainted with diagenesiswould be hard put to identify any morphological regularitiesin the specimens.
Similarly, the "regularly spaced pits"on the outer surface,interpreted as sensory organs, appear to represent irregularitiesformed by mineral growths penetrating the surface of the originalmicrofossil and accentuated by typical spherulite fans in thecavity-lining layers (see, for example Fig. 1D, upper left, and E,in this comment). Numerous such structures exist in thespecimens depicted by Chen et al.for example one specimen[figure 1B in (1)] shows at least a dozen of them along theperiphery and half that number around the area that Chen etal. interpret as the gutand the ones selected as pitsdiffer in no important way from the others. Even the designatedpits are not regularly spaced as claimed, as can be easily seenfrom the figured specimens.
When taphonomy and diagenesis are taken into account, the evidencethat these fossils preserve minute coelomate bilaterians disappears.The objects illustrated and described by Chen et al. (1) maywell be eukaryotic microfossils, but their reconstructed morphologyas bilaterians is an artifact generated by cavities being linedby diagenetic crusts. The appearance of the fossils now haslittle resemblance to that of the living organisms that generatedthem.
To paraphrase Theodosius Dobzhansky: Nothing in paleontologymakes sense except in the light of taphonomy and diagenesis.
Stefan Bengtson*
Department of Palaeozoology Swedish Museum of Natural History Box 50007 SE-104 05 Stockholm, Sweden
Graham Budd
Department of Earth Sciences, Palaeobiology Norbyvägen 22 SE-752 36 Uppsala, Sweden
* To whom correspondence should be addressed: E-mail: stefan.bengtson{at}nrm.se
References
1. J.-Y. Chen et al., Science305, 218 (2004); published online 3 June 2004 (10.1126/science.1099213).[Abstract/Free Full Text]
2. S. Xiao, X. Yuan, A. H. Knoll, Proc. Natl. Acad. Sci. U.S.A.97, 13684 (2000).[Abstract/Free Full Text]
3. Z. Yue, S. Bengtson, Lethaia32, 181 (1999). [ISI]
4. S. Xiao, Y. Zhang, A. Knoll, Nature391, 553 (1998). [CrossRef]
6. S. Bengtson, in The New Panorama of Animal Evolution, Proceedings of the 18th International Congress of Zoology, A. Legakis, S. Sfenthourakis, R. Polymeni, M. Thessalou-Legaki, Eds. (Pensoft, Sofia, Bulgaria, 2003), pp. 289300.
7. S. Bengtson, Lethaia9, 185 (1976).
Received for publication 10 June 2004. Accepted for publication 16 October 2004.
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