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Interpreting Late Precambrian Microfossils

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Science  04 Dec 1998:
Vol. 282, Issue 5395, pp. 1783
DOI: 10.1126/science.282.5395.1783a

Chia-Wei Li et al. describe microfossils found in Doushantuo phosphate rocks from Guizhou Province, South China that are about 580 million years old (1). Well-preserved macroscopic multicellular fossils associated with prokaryotic and eukaryotic microfossils from the same source rocks have been documented in several studies (2–6). The Doushantuo fossils are outstanding in both preservation quality and diversity, showing some details of cellular and tissue structures, and thus providing an exceptional opportunity to understand the evolution and diversification of early plants and animals just before the Ediacaran metazoan radiation. Interpretation of these fossils, however, should not be based only on a superficial morphological comparison between the fossils and some living forms. Taphonomic changes of the macro- and microfossils embedded in the Neoproterozoic phosphorites have to be taken into consideration. Postmortem degradation and diagenetic changes of the biological structures, which led to the present morphology of the fossils, are important for judging the biological nature of the ancient organisms (7).

We have studied the Doushantuo phosphorite fossils for more than a decade, and we disagree with the interpretation of Li et al. that some of the submillimeter microfossils were parenchymella larvae and amphiblastula embryos of sponges (1).

The putative parenchymella larvae of sponges, with a shoe-shaped morphology and dense peripheral flagella, as described by Li et al., are actually acanthomorphic acritarchs. Acritarchs are organic-walled microfossils that cannot be placed confidently into any existing classification categories, but most are comparable to remains of cysts of planktic eukaryotic algae (8). The acanthomorphic acritarchs (an acritarch group with distinct peripheral processes) are common and abundant in Neoproterozoic and Paleozoic deposits. Each individual acanthomorphic acritarch consists of an ovoid body (vesicle) surrounded by processes (Fig. 1, A and B). The processes of different taxa are varied in shape and size: mammillate, spine-form, hair-like, or flagellum-like. The specimen illustrated by Li et al., figure 2E of their report (1), is a deformed individual, with a shrunk vesicle and hair-like (or spine-like) processes. This specimen is morphologically comparable to those of the acritarch genus Ericiasphaera, which was set by Vidal in 1990 (9) and was redescribed to apply the large sphaeroidal acritarchs bearing numerous regularly arranged, solid, flexible, or rigid processes (6). Three species from the Doushantuo Formation have been described and assigned to this genus (6). We have observed many acanthomorphic acritarch specimens in the Doushantuo phosphorites (4,6, 10), which display a wide range of morphological variation resulting from taphonomic changes: from a relatively intact specimen (Fig. 1, A and B), to the shrunk forms at different degradation states (Fig. 1, C and D). Some of these specimens are similar to those illustrated by Li et al. (figure 1C in the report).

Figure 1

Acritarchs and diagenetic structures in the Doushantuo phosphorites (microscopic photographs on the thin sections) for comparison with the “parenchymella larvae” described by Li et al. from the same source-rock. (A andB) Sectional view of the acritarchs (assigned toEriciasphaera sp. and Meghystrichosphaeridiumsp., respectively). In well-preserved condition, they maintain a spheroid shape of vesicle and peripheral spine-like or flagellum-like processes. Diagenetic structures composed of amorphous kerogenous materials often occur within the vesicles; some are similar to the “amoebocytes” described by Li et al. (1) [arrows in (B)]. (B through D) Collapsed acritarchs (Ericiasphaera sp.) showing taphonomic variation caused by degradation and deformation. They are comparable to “parenchymella larvae” described by Li et al. (E and F) Granular and spine-like diagenetic structures in the Doushantuo phosphorites. They are similar to the structures described as “sclerocytes” and “spicules” of fossil sponges by Li et al.

Figure 2

Doushantuo fossil algal thalli (A and C) and a modern red algal thallus (B), for comparison with the “amphiblastula embryo” described by Li et al. (A) Sectional view of an algal thallus of W. globosa (the taxon was first found and described from the Doushantuo phosphorites in Wengan, Guizhou Province, by Y. Zhang in 1989). Cells maintained their rectangular or polygonal shape by their rigid cell wall (the surrounding rime), and the cytoplast had shrunk into a dark condensed inclusion. Specimen described as “amphiblastula embryo” by Li et al. bears the same features of algal tissue. (B) Sectional view of a modern red algaCorallina sp., showing same cellular features as those of fossils. (C) Well-preserved tissue of the Doushantuo algal fossil, showing cell-wall (arrows) and the condensed shrunk cytoplast (the dark bodies).

The granular and variable structures within the phosphorites have been interpreted as sclerocytes (sponge skeleton-setting cells) and amoebocytes, respectively, by Li et al. (1). However, as the figures in their report show, these structures have no distinct boundary membranes. Instead, they consist of amorphous kerogen. We have seen such structures in the vesicles of acritarchs (Fig. 1B) or in fossil remains (Fig. 1, E and F). These structures may not be original biological structures, but amorphous kerogenous forms resulting from organic degradation and diagenetic processes.

The structure interpreted as the sponge's amphiblastula embryo by Liet al. is actually a part of the alga thallus. Similar structures have often been observed from the Doushantuo phosphorites; they have been assigned to Wengania globosa, Zhang, with global thallus consisting of rectangular, polygonal, and irregular cells, and possible affinity of rhodophytes (Fig. 2A). This form of algae was first found and described in 1989 from Wengan Phosphate Mine by one of us (2) and was redescribed subsequently in several papers (3, 6). The so-called amphiblastula shown by Li et al. [figure 2F in (1)] are the same as the thallus of W. globosa. The tissues of the fossil algae are composed of regularly arranged cells, which display clear cell wall and condensed cytoplast (Fig. 2A and C). The tissue of modern rhodophytes, in a sectional view, shows morphological features similar to those of the fossils (Fig. 2B). The figure provided by Li et al. for the amphiblastula embryo [figure 2F in (1)] shows regularly arranged rectangular cells, cell-walls, and condensed cytoplast. Thus, the specimen of “amphiblastula” is an algal thallus (a broken thallus) rather than a sponge embryo.

The tiny spine- or needle-formed structures interpreted as monaxonal spicules of sponges by Li et al. are questionable. These structures in the phosphorite rocks could be multiple in origin. They could be detached broken spines of collapsed acritarchs (Fig. 3, A and B).

Figure 3

Acritarch specimen of Ericiasphaera magna(Zhang) preserved in the Doushantuo phosphorite from Wengan, South China. (A) Acritarch has a collapsed vesicle and surrounding spines. (B) Enlarged view of the specimen, showing the detached spines that look similar to the “sponge spicules” described by Li et al.

Our criticism does not mean that the Doushantuo Formation has only preserved remains of algae. On the contrary, we have pointed out that, among the discovered Doushantuo fossils, “a few forms exhibit certain features of metazoan tissue” (3). In addition, triact spicules have been found in the cherts of the Doushantuo Formation in Yangtze Gorge area (11), and we have found that the Doushantuo phosphorites preserved early-staged embryos of possible bilaterally symmetrical animals (5).

We expect more convincing evidences for early animals and plants to be found from the Doushantuoan and other contemporaneous or even older deposits in the near future.


Response: In our report (1), we described microscopic sponges and metazoan embryos from the 580-million-year-old Doushantuo phosphorites at Wengan, South China. Recently, Xiao et al. described multicellular algae and animal embryos from the same phosphorites (2). These discoveries not only offered a glimpse of familiar-looking animals before the Cambrian explosion, but also have implications for the study of early animal evolution (3). Recently, after examining more than 3000 embryo fossils, we are now able to reconstruct the sequential embryogenesis of the Wengan sponge. Zhang and his colleagues have done the pioneering work on describing well-preserved acritarchs and multicellular algae from the Wengan phosphorites (4–7). However, they have misidentified some of the abundant globular metazoan embryos as phytoplanktonic organisms (7, 8), and still identify an array of organisms as multicellular algae or as ambiguously defined acritarchs.

In their comment, Zhang et al. propose that spicules of the sponge that we described could be aggregates of detached broken spines of collapsed acritarchs. We disagree and would like to present further evidence (Fig. 1) in support of the identifications we made in our report. We have examined three specimens of this type of mushroom-shaped sponges. One specimen (Fig. 1) is a juvenile, and consists of a main crown, a slender stalk, and a flattened holdfast. It has been cracked into two halves during the late diagenesis, and the cracking space has been filled with diagenetic silica. That the spicules occur only in the body of the sponge, not anywhere along the crack or in surrounding matrix, indicates that they are biogenic in nature, not diagenetic products. The most important features of this sponge specimen are the preservation of the surface ornaments and the abundant interior spicules. The surface of this organism is ornamented with tiny knobby structures, which are regularly spaced and triangular in shape (Fig. 1A). The spicules occur randomly within the distinct body, and all spicules are monaxial, with two tapering ends (Fig. 1B). The axial canals could be observed in well-preserved spicules (Fig. 1, C and D). These characteristics fit well with the criteria of the sponge's spicules. Furthermore, we have illustrated two sclerocytes that attach to one end of each forming spicules. Both the sclerocytes are bounded by a distinct plasma membrane, which was marked as “pm” in figure 1F in our report, and which indicates a distinct boundary membrane.

Figure 1

Microscopic images of fossils from Wengan phosphorites. (A) Longitudinal section of a mushroom-shaped sponge with a holdfast (h), a stalk (st), and a crown (c). Specimen has been cracked during the Late Diagenesis; si, diagenetic silica. Surface ornamentation in the square is magnified (insert). Scale bar, 100 μm. (B) High magnification of the sponge in (A), showing the randomly dispersed monaxial spicules (s) in the mesohyl. Scale bar, 25 μm. (C and D) Two partially fractured spicules, showing their internal axial canal (ac). Scale bar, 2.5 μm.

In their comment, Zhang et al. refer to some organic remains with peripheral processes as the products of “collapsed acritarchs resulting from taphonomic changes,” and stated that these organic remains are comparable to the parenchymella larva described by us. We have quite different views on this issue. First, the specimens shown by Zhang et al. are evidently different from our specimen. The peripheral flagella of our specimen not only taper to their distal ends, but also have a flexible outline, while the peripheral processes of their specimens are uniform in diameter, with broadly rounded distal ends. We aim to be cautious in describing the larva. Our tentative identification is mainly based on the shoe-shaped morphology and dense peripheral flagella. However, there are many kinds of organisms that could share these characteristics, including protists and planula larvae of coelenterates, so we called it “possible parenchymella larva” or “parenchymella-type larva” consistently.

Second, the purported “collapsed acritachs” with peripheral processes are not only different from our “possible parenchymella larva” specimen, but also appear to be filamentous bacteria growing on organic remains. We have examined tens of this type of specimen, which are comparable to the specimens described as collapsed acritarchs, and we conclude that these filamentous bacteria (Fig. 2, A–D) are quite different from both the peripheral processes of the acritarchs and the flagella of the parenchymella larvae. These filaments are uniform, with a diameter of ∼0.75 μm through their long axes, length varying from 20 μm to 93 μm, and distal ends that are broadly rounded. This kind of association is a common phenomenon in extant aquatic environments. A reasonable explanation is that they were fossilized in situ, keeping their original shape through the taphonomic process. That is the beauty of the Wengan phosphorites in which almost all the organisms, including these bacteria, are kept intact and preserved in three dimensions. The acritarch (Gr. “of uncertain origin”), a loosely defined group, has become a grab bag containing a variety of unicellular microfossils. Although some are the right size and shape to be the coats of cysts similar to those made by certain extant protists, acritarchs should be much more polyphyletic than what palaeontologists generally conjectured.

Figure 2

Possible association of filamentous bacteria (fb) and their organic substrates (os). Scale bar, 20 μm. (A) Dense colony of long filamentous bacteria growing on a thin layer of organic substrate. (B) High magnification of the framed portion in (A). (C and D) Two colonies of filamentous bacteria with medium length, which are similar to the “collapsed acritarchs” recognized by Zhang et al.

We have assigned a specimen as a possible amphiblastula larva based on the similarity between our specimen and the amphiblastula larva of an extant sponge (Grantia compressa) (9, p. 77) in morphology and arrangement of component cells. Zhang et al.tend to interpret our specimen as an algal thallus (Wengania globosa), but there are fundamental differences between our “possible amphiblastula larva” and the specimen of W. globosa shown by Zhang et al. By comparing the schematic drawings (Fig. 3) that reveal the anatomy of our “possible amphiblastula larva” and W. globosa, one can observe the distinct differences in size, morphology, and arrangement of the component cells between them. Furthermore, the description of W. globosa in their comment seems inconsistent with other publications of theirs. Although the very same figure of this taxon shown in the comment by Zhang et al. was apparently used earlier by them (5), there seem to be discrepancies between the associated legends concerning the species names and the size of the thallus. In that paper (5), this organism was referred to asW. rotatoria and the size of the thallus was stated as 393 × 330 μm not 86 × 73 μm as stated in the comment. The genusWengania was also loosely defined. Zhang and Yuan erected a new genus Cerionopora in 1992 (5) and briefly described the diagnostic difference between it and Wengania, but in 1993, they illustrated the same figure [plate I, figure 3 in (6)] under the name W. globosa without apparent explanation.

Figure 3

Schematic drawings of W. globosa (A) and our “possible amphiblastula larva” (B), showing differences in size, morphology, and arrangement of component cells. Scale bar, 20 μm.

The discoveries of microscopic animals and embryo fossils from Wengan phosphorites (1, 2) have created some challenges for scientists to tackle. Further research and evaluation is needed to clarify the ultrastructure of the phosphatized fossils in order to reveal the scope and significance of the Wengan biota.


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