Three-Dimensional Microct Analysis of the Ediacara Fossil Pteridinium

Home , Dickinsonia, Eoandromeda, Proarticulata, Pteridinium

Precambrian Research 249 (2014) 79–87

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Precambrian Research

jo urnal homepage: www.elsevier.com/locate/precamres

Three-dimensional microCT analysis of the Ediacara fossil Pteridinium

simplex sheds new light on its ecology and phylogenetic afﬁnity

a,∗ b c c d

Mike Meyer , David Elliott , Andrew D. Wood , Nicholas F. Polys , Matthew Colbert ,

d b b e

Jessica A. Maisano , Patricia Vickers-Rich , Michael Hall , Karl H. Hoffman ,

e a

Gabi Schneider , Shuhai Xiao

Department of Geosciences, Virginia Tech, Blacksburg, VA 24061, USA

School of Geosciences, Monash University, Clayton, Victoria 3800, Australia

Advanced Research Computing, Virginia Tech, Blacksburg, VA 24061, USA

Jackson School of Geosciences, The University of Texas, Austin, TX 78712, USA

Geological Survey of Namibia, Windhoek, Namibia

a r t i c l e i n f o a b s t r a c t

Article history: Ediacara fossils often exhibit enigmatic taphonomy that complicates morphological characterization and

Received 12 September 2013

ecological and phylogenetic interpretation; such is the case with Pteridinium simplex from the late Edi-

Received in revised form 15 April 2014

acaran Aar Member in southern Namibia. P. simplex is often preserved as three-dimensional (3D) casts

Accepted 21 April 2014

and molds in coarse-grained quartzites, making detailed morphological characterization difﬁcult. In addi-

Available online 2 May 2014

tion, P. simplex is often transported, distorted, and embedded in gutter ﬁlls or channel deposits, further

obscuring its morphologies. By utilizing microfocus X-ray computed tomography (microCT) techniques,

Keywords:

we are able to trace individual specimens and their vanes in order to digitally restore the 3D morphol-

Pteridinium

MicroCT ogy of this enigmatic fossil. Our analysis shows that P. simplex has a very ﬂexible integument that can

Taphonomy be bent, folded, twisted, stretched, and torn, indicating a certain degree of elasticity. In the analyzed

Namibia specimens, we ﬁnd no evidence for vane identity change or penetrative growth that were previously

Ediacaran used as evidence to support a fully endobenthic lifestyle of P. simplex; instead, evidence is consistent

Aar Member with the traditional interpretation of a semi-endobenthic or epibenthic lifestyle. This interpretation

needs to be further tested through microCT analysis of P. simplex specimens preserved in situ rather

than transported ones. The elastic integument of P. simplex is inconsistent with a phylogenetic afﬁnity

with xenophyophore protists; instead, its physical property is consistent with the presence of colla-

gen, chitin, and cellulose, an inference that would provide constraints on the phylogenetic afﬁnity of

P. simplex.

1. Introduction 2009), but understanding their phylogenetic placement has been

impeded by their unusual taphonomy (Cai et al., 2012; Gehling,

Ediacara-type fossils (580–541 Ma) represent the earliest- 1999; Laﬂamme et al., 2011; Schiffbauer and Laﬂamme, 2012) and

known complex multicellular organisms in the fossil record the lack of morphological analogs among extant taxa (Laﬂamme

(Laﬂamme et al., 2013; Narbonne, 2005; Xiao and Laﬂamme, et al., 2013; Seilacher et al., 2003). Among all Ediacara fossils, the

genus Pteridinium (Gürich, 1930), ﬁrst described from the Nama

Group in southern Namibia (Fig. 1A), best encapsulates these

∗ two confounding factors (Fedonkin et al., 2007). Pteridinium has

Corresponding author at: Department of Geology, Bucknell University, Lewis-

a unique body plan (Fig. 1B), consisting of three vanes which are

burg, PA 17837, USA. Tel.: +1 8479515610.

E-mail addresses: [email protected], [email protected], connected along an axis known as the ‘seam’. Each vane is made

[email protected] (M. Meyer), [email protected] (D. Elliott),

of a single row (or possibly two overlapping rows) of segments

[email protected] (A.D. Wood), [email protected] (N.F. Polys), [email protected]

that are attached to the seam (Jenkins, 1992). Pteridinium can

(M. Colbert), [email protected] (J.A. Maisano), [email protected]

be preserved two-dimensionally on bedding surfaces or three-

(P. Vickers-Rich), [email protected] (M. Hall), [email protected]

(K.H. Hoffman), [email protected] (G. Schneider), [email protected] (S. Xiao). dimensionally within massive quartzite, resulting in multiple

http://dx.doi.org/10.1016/j.precamres.2014.04.013

80 M. Meyer et al. / Precambrian Research 249 (2014) 79–87

Fig. 1. Geological map, stratigraphic column, and construction of Pteridinium simplex. (A) Geological map and stratigraphic column showing the location and horizon from

which the hand sample in this study was collected (in the Aar Member, Dabis Formation, Kuibis subgroup). Radiometric dates from Schmitz (2012). (B) Morphological and

ecological reconstruction and descriptive terms of P. simplex.

taphomorphs. When preserved in 3D, Pteridinium specimens are 2. Geological and stratigraphic background

often jumbled within mass ﬂow deposits, with their morphology

strongly modiﬁed and difﬁcult to interpret (Elliott et al., 2011; The analyzed hand sample was collected from the Aar Mem-

Grazhdankin and Seilacher, 2002). ber of the Dabis Formation, Kuibis Subgroup, located at Aar Farm

The unusual morphology and non-actualistic (without modern in the Aus region of southern Namibia (Fig. 1A) (Hall et al., 2013;

analog) taphonomy of Pteridinium have led to various ecologi- Vickers-Rich et al., 2013). Available radiometric and chemostrati-

cal and phylogenetic interpretations. It has been interpreted as a graphic data constrain the Kuibis Subgroup to be older than

frondose epibenthic organism similar to Charniodiscus (Glaessner 547.32 ± 0.65 Ma but likely younger than 551.09 ± 1.02 Ma (Condon

and Daily, 1959), a semi-endobenthic organism similar to Erni- et al., 2005; Grotzinger et al., 1995; Narbonne et al., 2012; Schmitz,

etta (Fedonkin et al., 2007), or a fully endobenthic organism that 2012). The Aar Member consists mainly of interbedded sandstones

lived entirely within sediments (Grazhdankin and Seilacher, 2002). (1–2 m thick) and shales with a few limestone beds. It was likely

The phylogenetic afﬁnity of Pteridinium has also been a matter deposited in an extensive, sandy, braided ﬂuvial to shallow marine

of intense debate; it has been interpreted as a colonial organism system, partly reworked into vast inter-tidal sand ﬂats along a low

(Pﬂug, 1994), a giant single-celled protist similar to modern xeno- gradient coastal plain (Elliott et al., 2011; Hall et al., 2013; Saylor

phyophores (Seilacher et al., 2003), a lichen (Retallack, 1994), or an et al., 1995). Individual sandstone beds were likely deposited during

animal (Glaessner, 1984). sheet ﬂood events, which brought sandy sediments over mud-

Central to the current debate on the ecology and phylogenetic dominated inter-tidal to sub-tidal sediments. P. simplex fossils are

afﬁnity of Pteridinium is a better understanding of its taphonomy found in these sandstone beds, particularly in the lower part of the

and morphology. For example, the fully endobenthic interpreta- Aar Member (Hall et al., 2013). The Aar Member is directly over-

tion rests on convoluted Pteridinium simplex specimens with their lain by bedded limestones of the Mooifontein Member, suggesting

vanes growing in sediments, penetrating each other, and switch- a major marine transgression in the area (Gresse and Germs, 1993).

ing identities (e.g., lateral vane changing to medial vane when

organism is twisted) (Grazhdankin and Seilacher, 2002). However, 3. Materials and methods

these features are difﬁcult to resolve without a three-dimensional

understanding of the fossils, and it is thus difﬁcult to rule out the The analyzed hand sample (V-8-2009; Fig. 2) contains multiple

possibility that some of these features may result from taphonomic P. simplex specimens. The fossils are preserved as casts or molds in

alteration. Thus, to better characterize the three-dimensional mor- massive quartzite, with their vanes probably replicated by pyrite

phology of P. simplex and to shed light on its taphonomy, ecology, but represented by stylolitic surfaces, void spaces, or secondary cal-

and phylogenetic afﬁnity, we examined a single hand sample with cite formed during diagenesis or weathering (Meyer et al., 2014).

multiple P. simplex specimens using microfocus X-ray computed The segments in each vane are seen as parallel lines or ridges ema-

tomography (microCT). nating perpendicularly from the seam. These ridges fade away and

M. Meyer et al. / Precambrian Research 249 (2014) 79–87 81

Fig. 2. Light photographs of hand sample V-8-2009, shown in different views. Colored arrows point to correspondingly colored P. simplex specimens in Figs. 3–4. Asterisks,

triangles, and stars mark landmark locations in all views. (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web version of this

article.)

grade into a smooth surface farther away from the seam (Crimes tools available in Seg3D (CIBC, 2013), an image processing and seg-

and Fedonkin, 1996; Elliott et al., 2011; Grazhdankin and Seilacher, mentation application built on ITK (Yoo et al., 2002). The segment

2002; Jenkins, 1992). The hand sample was cut into three slabs per- masks of interest (individual specimens, vanes) were then exported

pendicular to the main axis/seam of the largest and most prominent as image stacks, resized using ImageJ to a useable 258 × 258 × 258

P. simplex specimen. The slabs are labeled 1–3 and cut lines are voxels for real-time rendering, and converted to NRRD using UNU.

marked by i–ii in Fig. 3A. Slab 1 was used for petrographic analyses Finally, the NRRD segments were composited and rendered using

(Meyer et al., 2014) while slabs 2 and 3 were used in this study. H3D (Sensegraphics, 2013); an X3D browser with strong support

Slabs 2 and 3 were cut so that they can ﬁt in the microCT scanner. for NRRD and the volume rendering styles provided by the X3D 3.3

The two slabs were scanned separately using the ultra-high- standard (Brutzman and Daly, 2007; Consortium, 2012). Each seg-

resolution subsystem of the ACTIS scanner at the University of ment was represented as an isosurface and uniquely false-colored

Texas High-Resolution X-ray CT Facility. A FeinFocus microfocal X- for easy visualization. Using H3D, the two slabs were then scaled

ray source operating at 200 kV and 0.24 mA with no X-ray preﬁlter and “stitched” to restore their original pre-cut conﬁguration. The

was employed. An empty container wedge was used. Slice thick- original microCT data, reslicings, and derivative animations are

ness corresponds to one line in a CCD image intensiﬁer imaging available at www.digimorph.org/specimens/Pteridinium simplex.

system, with a source-to-object distance of 275 mm for slab 2 and

330 mm for slab 3, resulting in 0.096 mm and 0.115 mm interslice 4. Results

spacing, respectively. For each 1024 × 1024 pixel slice, 1400 views

◦

were acquired with three samples per view over 360 of rotation. A comparison of light photographs and corresponding microCT

The ﬁeld of reconstruction was 91 mm for slab 2 and 107 mm for renderings, shown at two different perspectives, is presented in

slab 3, resulting in 0.089 mm and 0.104 mm in-plane resolution, Fig. 3. MicroCT reveals ﬁve P. simplex specimens embedded in the

respectively. scanned blocks (labeled 1–5 in Fig. 4). These specimens do not have

The scan data were processed to reduce ring and beam- a consistent orientation; for example, specimens 1 and 3 are ori-

◦

hardening artifacts, and 16 bit TIFF image stacks were reconstructed ented at 90 from each other. Four of the ﬁve specimens are partially

(1312 and 1083 slices for slabs 2 and 3, respectively). While useful exposed, with the exposed vanes marked by colored arrows match-

on their own, these image stacks did not allow for easy 3D visual- ing the color of segmented specimens in Fig. 3. Three specimens (1,

ization of the fossils within the slabs. Thus, the data were further 2 and 4) have some part of all three vanes present while the other

processed using open-source image processing, segmentation, and two specimens have at least one preserved vane (Figs. 3–5).

volume rendering tools to create 3D reconstructions of the features Specimen 1 is bent tightly and twisted slightly, but its three

of interest. Because of the large size of the original data volumes vanes are easily identiﬁable (colored individually in Fig. 5). It can

(2.6 and 2.2 Gb for slabs 2 and 3, respectively), the images were be seen in Fig. 5D that the blue medial vane is incompletely pre-

reduced to 512 512 pixels and 8 bit depth using ImageJ (Schneider served where the specimen is bent. As the fossil is bent over itself,

et al., 2012) to facilitate rendering. The resulting stack was saved the outer lateral vane is stretched (yellow vane in Fig. 5) and the

as a RAW ﬁle and then converted to NRRD format using the com- inner lateral vane is compressed (green vane in Fig. 5). Interest-

mand line utility UNU (2013) for initial rendering and import into ingly, the green lateral vane is also ruptured or torn along segment

segmentation software. boundaries (Fig. 5C and D), although the proximal part of the vane

The volumes were then segmented into individuals and vanes (the part closer to the central seam) is still intact (Fig. 5A). The

◦

using a combination of manual mask painting and semi-automated two torn pieces are oriented at ∼90 to each other; because of

82 M. Meyer et al. / Precambrian Research 249 (2014) 79–87

Fig. 3. Light photography and 3D reconstruction of Pteridinium simplex specimens within hand sample V-8-2009. (A and C) Light photographs from two different perspectives,

with (C) showing a view from the yellow arrow in (A). (B and D) MicroCT segmentations of P. simplex specimens, oriented at the same perspectives as (A) and (C), respectively,

with dashed lines representing the outline of the hand sample. Colored arrows point to specimens segmented in corresponding colors. Yellow arrows point to main specimen

(specimen 1) in this study. Numbers 1–3 denote the three slabs resulting from cuts represented by lines i and ii. Slabs 2 and 3 were microCT scanned. Asterisks mark the

same location on slab 1 near cutline i and can be used for orientation. Scale bar = 1 cm. (For interpretation of the references to color in this ﬁgure legend, the reader is referred

to the web version of this article.)

Fig. 4. Two different views of the ﬁve specimens of Pteridinium simplex. Specimens are colored and numbered. Asterisks mark the same location locations on slab 1 near

cutline i. Scale bar = 1 cm. (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web version of this article.)

M. Meyer et al. / Precambrian Research 249 (2014) 79–87 83

Fig. 5. Four different views of Pteridinium simplex specimen 1. Lateral vanes are yellow and green, and medial vane is blue. (A–C) Views including slabs 2 and 3. (D) View of

only slab 3. Asterisks and triangles mark the same two locations on slab 3 in all views. Scale bar = 1 cm. (For interpretation of the references to color in this ﬁgure legend and

the text, the reader is referred to the web version of this article.)

this, they could be easily mistaken for two different vanes, with but this specimen has the least preservational ﬁdelity and is difﬁcult

the dangling piece in Fig. 5C and D misidentiﬁed as a medial vane, to reconstruct. Despite the interactions among the ﬁve speci-

particularly when the real medial vane (blue color in Fig. 5B and mens in the analyzed sample, there is no evidence for penetrative

5D) is not well preserved. Thus, taphonomic alteration could lead growth.

to false interpretation of vane identity change.

Specimen 3 abuts against specimen 1, with their exposed vanes 5. Taphonomic and ecological interpretations

oriented at a right angle (Figs. 3A and C, 4A and 6A), giving an

impression of possible penetrative growth. However, rock mate- Our microCT analysis conﬁrms the basic morphological archi-

rial at the exposed contact between the two specimens has been tecture of P. simplex, with three vanes attached to a single central

removed by weathering, making it impossible to determine the seam. The nature of vane preservation as void space or secondary

exact nature of the contact based on visual examination of the hand calcite, however, does not allow us to resolve whether each vane

sample. MicroCT allows a closer look at the nature of the contact is composed of a single row or two overlapping rows of segments

inside the hand sample, and the slice images show that (1) the vanes (Jenkins, 1992). Nonetheless, the microCT data do reveal several

of these two specimens do not crosscut each other, and (2) a vane of important aspects of P. simplex morphology, taphonomy, and pale-

specimen 3 is bent slightly at the distal edge when it comes in close oecology.

contact with one of the lateral vanes of specimen 1 (Fig. 6). The lat- First, the folding, bending, and twisting of P. simplex speci-

ter relationship is best seen in unexposed vanes where the effect mens, as well as the stretching, warping, and breakage of P. simplex

of weathering is minimal (e.g., compare the exposed and unex- vanes, are interpreted as taphonomic in origin. Such taphonomic

posed parts of the same vane marked by green arrows in Fig. 6B alteration is expected given the sedimentological inference that

and 6C, respectively). Thus, we have found no evidence for pene- these specimens were entrained and transported in mass ﬂow

trative growth, even though the jumbled specimens seem to give deposits (Elliott et al., 2011). Entrainment in high-density mass

the impression of a penetrative relationship. ﬂow deposits also better explains the lack of preferred orientation

The other three specimens also interact with specimen 1. One among tightly packed specimens. Indeed, different parts of a single

lateral vane of specimen 2 is also in contact with the distal ends of specimen can assume different orientations; for example, the bend-

the two lateral vanes of specimen 1 (Figs. 3D and 4B). Again, there is ing and twisting of specimen 1 resulted in different orientations of

no evidence for penetrative growth. Specimen 4 can be clearly seen the two ends of this fossil (Figs. 5C, D and 7).

as a curved space on the surface of the hand sample (Fig. 2B). How- Second, although P. simplex vanes are stretchable, they can

ever, only a small part of this specimen is preserved and one of its be torn, apparently along segment boundaries which may

vanes is in contact with the seam of specimen 1 (Fig. 4B). Specimen represent mechanical weakness. That the distal part of the vane

5 sits against one of the lateral vanes of specimen 1 (Figs. 3D and 4B), is torn whereas the proximal part is intact suggests that the former

84 M. Meyer et al. / Precambrian Research 249 (2014) 79–87

Fig. 6. Three-dimensional reconstruction and microCT slice images of Pteridinium simplex specimens 1 (yellow) and 3 (green). (A) View showing that the vanes of the two

specimens abruptly abut against each other. (B–C) MicroCT slice images, showing the relationship between the two specimens. Colored arrows point to vanes of specimens

segmented in corresponding colors. Note that the apparent vane termination of specimen 3 at specimen 1 is due to weathering on exposed surface (green arrows and green

dashed line in B) and that, when unexposed, the same vane is distally bent where it is compressed against specimen 1 (yellow arrows and yellow dashed line in C). Scale

bar = 1 cm. (For interpretation of the references to color in this ﬁgure legend and the text, the reader is referred to the web version of this article.)

may have been mechanically weaker than the latter. This inference of P. simplex (Fig. 1B) with its central seam buried in the sedi-

is consistent with previous interpretations that the seam of P. sim- ments but the distal part of the vanes remaining free in the water

plex seems to be the most rigid part of the organism, with the vanes column (Elliott et al., 2011; Meyer et al., 2014). The epibenthic

and segments quickly losing deﬁnition farther away from the seam or semi-endobenthic ecological interpretations can also account

and grading into a smooth surface (Elliott et al., 2011; Grazhdankin for Pteridinium specimens that are preserved more or less two-

and Seilacher, 2002; Jenkins, 1992). The taphonomic reorientation dimensionally on the bedding surface (Narbonne et al., 1997).

of broken vanes would also make it difﬁcult to determine vane

identity, particularly when the medial vane is poorly preserved (as

commonly is the case), and when three-dimensional morphologi- 6. Discussion on biomaterial composition and phylogenetic

cal reconstructions are not available and thus the determination of afﬁnity

vane identity has to be based on vane orientation.

Third, detailed microCT imaging of the interrelationship A major taphonomic problem for many Ediacara fossils (includ-

between tightly packed P. simplex specimens with sharply abutting ing P. simplex) is that, although they are ‘soft-bodied’, their

vanes shows no evidence for penetrative growth; instead, the distal integument seems to be rigid enough to survive transport, but also

edges of vanes are bent when compressed against other vanes. Pre- pliable enough to account for bent and twisted specimens (Dzik,

vious interpretation of penetrative growth in P. simplex was based 1999, 2003; Fedonkin et al., 2007; Gehling, 1999). The absence of

on hand sample observation of specimens with vanes abruptly preserved organic material in many Ediacara fossils, particularly

abutting against each other (Grazhdankin and Seilacher, 2002). those hosted in sandstones, has led some investigators to pur-

Such a relationship can be alternatively interpreted as taphonom- sue biomechanical studies using ﬂume or ﬂow tank experiments,

ically broken vanes jammed against other specimens. A positive in order to infer the biomechanical properties of their original

identiﬁcation of penetrative growth requires microCT data to con- integument (Schopf and Baumiller, 1998; Singer et al., 2012). While

ﬁrm that vanes crosscut each other rather than just abut against this study was not set up to examine the biomechanics of P. sim-

each other. plex, biomechanical information can be indirectly inferred from the

Thus, some of the evidence previously used to infer a fully three-dimensional scan data. The degree of stiffness and elastic-

endobenthic lifestyle of P. simplex—convoluted specimens with ity exhibited by the vanes of P. simplex may help to constrain the

penetrative growth and vane identity change (Grazhdankin and biomechanical properties and possible biomaterial makeup of its

Seilacher, 2002)—needs to be reconsidered in light of the new integument. This information can then be used to indirectly infer

data presented here. Because the analyzed specimens have been the possible phylogenetic afﬁnity of P. simplex. However, in order

transported, it is important to carry out microCT analysis of spec- to constrain the biomaterial makeup of P. simplex integument, we

imens preserved in life position to further test the endobenthic must ﬁrst understand what stiff yet elastic biomaterials are present

hypothesis. Nonetheless, our data are consistent with an epiben- in extant (and extinct) organisms and how they may have affected

thic model, and they do not falsify a semi-endobenthic life mode the taphonomic behavior of P. simplex vanes.

M. Meyer et al. / Precambrian Research 249 (2014) 79–87 85

muscles, and unbound, as in mesoglea) are structurally elastic,

meaning that it can be stretched or compressed and still return to

its original form. Other potentially elastic biomaterials in extant

organisms are mostly structural polysaccharides, including chitin

and cellulose. Chitin is a nitrogen bearing polysaccharide that has

variable biomechanical properties depending on the inclusion

of additional materials such as sclerotin or calcium carbonate

(Bengtson and Conway Morris, 1992; Varki, 2009). Various forms

of chitin are present in the cell walls of fungal hyphae, the pro-

teinaceous matrix of arthropods (with high levels of sclerotin), and

the exoskeletons of crustaceans and calciﬁed shells of molluscs

(Marin and Luquet, 2005; Schönitzer et al., 2011). Cellulose is the

main structural component in the cell walls of algae and plants

(Vogel, 2003), but it is also present in the tunic of tunicate animals

(Endean, 1961; Vogel, 2003). Cellulose ﬁbers are highly ﬂexible, as

can be observed in some algal fronds (Koehl, 1999; Martone, 2007;

Martone and Denny, 2008), but highly packed cellulose ﬁbers can

be brittle due to the crystalline nature of cellulose (Vogel, 2003).

Pectin and pellicle are present in the cell walls of some eukary-

otes (Kirby, 1941). Pectins are complex polysaccharides in the

primary cell walls of non-woody terrestrial plants and bind the cells

together (Braconnot, 1825; Buchanan et al., 2000). Pellicle is a thin

layer of proteinaceous strips supporting the cell membrane in vari-

ous protozoa (Kirby, 1941). Both pectin and pellicle can be ﬂexible,

elastic, or rigid, but these variable biomechanical characteristics are

only expressed on small scales (Kirby, 1941). Additionally, bacte-

rial cell walls have a mesh-like layer of peptidoglycan (murein) that

serves a structural role (increasing the strength of the cell wall) and

controls osmotic pressures (Demchick and Koch, 1996; van den Ent

et al., 2001). However, because we do not have any biomechanical

information of P. simplex at the cellular scale, the presence/absence

of pectin, pellicle, or peptidoglycan in P. simplex integument cannot

be tested using the currently available data.

Finally, some living organisms form an agglutinated test as their

“integument”. For example, some single-celled foraminifers are

well known for their agglutinated tests (Murray, 2006). Aggluti-

Fig. 7. Simpliﬁed diagram showing bending, twisting, and tearing in specimen 1

nated walls consist of sediment particles, sometimes bound with

(vane colors correspond to those in Fig. 5). (A) Pre-deformation morphology. (B–C)

organic material (Murray, 2006). Xenophyophoran foraminifers

Bending. (D) Twisting and tearing along segment boundaries. (For interpretation of

the references to color in this ﬁgure legend, the reader is referred to the web version can form agglutinated tests of macroscopic size, consisting of ﬁne

of this article.)

sediment bound with fecal pellets (Murray, 2006; Seilacher et al.,

2003; Tendal, 1972, 1979). Structurally, however, their tests are

6.1. Extinct biomaterials very brittle and do not deform easily (Seilacher et al., 2003; Tendal,

1972).

Ediacara fossils were once placed in the extinct clade Vendo-

bionta and were noted for their distinct morphology, preservation, 6.3. Taphonomic constraint on phylogenetic afﬁnity

and biocoenosis (Grazhdankin and Seilacher, 2002; Seilacher, 1989,

1992, 2007). The placement of P. simplex within the Vendobionta Any phylogenetic interpretations for P. simplex must also con-

opens up the possibility that its integument may have been com- sider its taphonomy. Since Pteridinium fossils are preserved as casts

posed of a distinct biomaterial that has since been lost along with or molds in massive quartzite, there is no original organic material

the extinction of Ediacara organisms. While we cannot exclude this or any carbonaceous material associated with the fossils. Preser-

possibility, it is very difﬁcult to constrain, without the aid of mod- vation in coarse-grained siliciclastic rocks is common for Ediacara

ern analogs, the range of materials that accord with the inferred fossils (Gehling, 1999; Schiffbauer and Laﬂamme, 2012), with few

biomechanical properties of P. simplex integument. Even though of them being preserved through carbonaceous compression, the

the vendobionts may represent an extinct clade, they must be evo- main taphonomic mode of Burgess Shale-type fossils. One of the

lutionarily related to extant organisms. Thus, our search for the exceptions is the Ediacara fossil Eoandromeda, which is preserved

possible biomaterial makeup of P. simplex integument is necessarily both as casts/molds in sandstone and as carbonaceous compres-

based on extant analogs. sions in black shale (Zhu et al., 2008; Xiao et al., 2013). It is thus

inferred that P. simplex must have had an organic integument and

6.2. Extant biomaterials the lack of carbonaceous preservation is due to secondary loss.

Indeed, many Phanerozoic plant fossils, when preserved in coarse-

Collagen is exclusively found in animals and is most commonly grained sandstones, lack carbonaceous material as well (Driese

present in their integuments, muscles, and connective tissues et al., 1997; Sharon, 2010).

(Müller, 2003; Vogel, 2003). It is also present (in a more loosely The minor clay minerals found in association with P. simplex

packed form) in the mesoglea of diploblastic animals such as vanes (Meyer et al., 2014) may be important, because detrital and

cnidarians and ctenophores (Hernandez-Nicaise and Amsellem, authigenic clay minerals are thought to play a constructive role in

1982; Tucker et al., 2011). Collagen ﬁbers (both bound, as in the preservation of soft tissues (Anderson et al., 2011; Butterﬁeld,

86 M. Meyer et al. / Precambrian Research 249 (2014) 79–87

1990; Cai et al., 2012; Laﬂamme et al., 2011; Meyer et al., 2012; Orr 7. Conclusions

et al., 1998). Clay minerals have been known from Burgess Shale-

type biotas where carbonaceous material is preserved (Butterﬁeld, MicroCT offers an effective approach to study P. simplex spec-

1990; Gaines et al., 2008; Orr et al., 1998; Xiao et al., 2002). Although imens preserved three-dimensionally within mass ﬂow deposits.

detrital or authigenic clays may have played a constructive role in Our investigation conﬁrms the basic morphology of P. simplex:

the preservation of Ediacaran fossils such as Aspidella (Laﬂamme three vanes attached at the seam. The vanes can be bent, folded,

et al., 2011), Conotubus (Cai et al., 2012), and Shaanxilithes (Meyer twisted, stretched, and torn, through taphonomic processes. Such

et al., 2012), the origin of clays in association with P. simplex vanes taphonomic alterations complicate morphological reconstruction

cannot yet be resolved with available data and they have been ten- of P. simplex, and can potentially lead to false interpretation of vane

tatively interpreted as weathering products (Meyer et al., 2014). identity change and penetrative growth, particularly when obser-

With the lack of carbonaceous material and the problematic origin vation is limited to the external surface of fossiliferous blocks. Our

of minor clay minerals in association with P. simplex (Meyer et al., microCT analysis reveals no evidence for vane identity change or

2014), our phylogenetic interpretation has to be indirectly based penetrative growth. Thus, this important basis for postulating an

on the integument biomaterials, which are in turn inferred from entirely endobenthic P. simplex should be treated with caution and

the taphonomic behavior and the elastic biomechanical property should be further tested with microCT analysis of specimens pre-

of the integument. served in life position. Nonetheless, the data presented here are

consistent with the traditional ecological interpretation of P. sim-

6.4. Phylogenetic discussion

plex as a semi-endobenthic or epibenthic organism because this life

style also accounts for specimens preserved two dimensionally on

Collagen, cellulose, and chitin have been the most commonly

bedding surfaces. The taphonomic deformation of P. simplex indi-

hypothesized biomaterials for P. simplex integument (Buss and

cates that it had an elastic integument, which is inconsistent with

Seilacher, 1994; Dzik, 1999; Elliott et al., 2011; Retallack, 1994,

a phylogenetic afﬁnity with xenophyophores. Its integument may

2007; Seilacher, 1992), although agglutinated tests similar to extant

have been made of a collagenous, chitinous, and cellulose bioma-

xenophyophores have also been suggested as possible construc-

terial. Because collagen synthesis is a synapomorphy of the animal

tional biomaterials (Seilacher et al., 2003). The elastic behavior of

kingdom, P. simplex may be phylogenetically related to animals,

P. simplex vanes is consistent with the presence of collagen or chitin

likely representing a stem-group animal considering its unique

in its integument. Both of these materials can add to the elasticity

body plan.

and ﬂexibility of the integument. However, the sharply torn edge

of P. simplex vanes also suggests a stiffness or rigidity that could be

Acknowledgments

attributed to the presence of cellulose ﬁbers within the integument.

Agglutinated tests, however, can be excluded as they do not have

Financial support for this study was provided by the

the degree of ﬂexibility as observed in the taphonomic analysis of

U.S. National Science Foundation (EAR-0844235, EAR-0948842,

P. simplex. Thus, a phylogenetic afﬁnity with xenophyophores can

EAR-1124062, EAR-1250800), International Geosciences Program

also be excluded. As stated above, the presence/absence of pectin,

Projects 493 and 587, and National Geographic Society, and both

pellicle, or peptidoglycan in P. simplex integument cannot be tested

the international and national committees of the International Geo-

because of the lack of cellular scale behavior of P. simplex integu-

science Programme (IGCP). We would like to thank the anonymous

ment.

reviewers for constructive comments and the owners of Farm Aar,

The possible presence of collagen, cellulose, and chitin in the

B. Boehm-Erni and the late B. Boehm, for granting access to the

integument of P. simplex can be used to constrain the phylogenetic

fossils site and their hospitality.

afﬁnity of this enigmatic Ediacara fossil. Collagen is found exclu-

sively in animals. Extant animals use collagen in a diverse array of

functions (e.g., collagen in muscles and connective tissues can assist Appendix A. Supplementary data

locomotion), but these functions may have been derived character-

istics that evolved after the origin of collagen. With a few exceptions Supplementary data associated with this article can be found,

(Ivanstov, 2009, 2011; Ivanstov and Malakhovskaya, 2002), most in the online version, at http://dx.doi.org/10.1016/j.precamres.

Ediacara fossils including P. simplex were probably immobile orga- 2014.04.013.

nisms. Thus, the presence of collagen P. simplex integument may

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