Skeletogenesis and asexual reproduction in the earliest biomineralizing animal Cloudina

Abstract

The tubular fossil Cloudina is emerging as an important Ediacaran index fossil. However, its morphology, skeletogenesis, reproduction, and phylogenetic affinity have not been fully resolved. New material from the Dengying Formation of south China confirms that Cloudina tubes consist of eccentrically and sometimes deeply nested funnels and that the tubes lack transverse cross-walls, inconsistent with the traditional cone-in-cone morphological reconstruction. Tube walls are composed of micrometer-sized, more or less equant crystals. A number of Cloudina tubes branch dichotomously, in which daughter funnels split within parent ones. The Cloudina animal is interpreted to have been able to initiate biomineralization of new funnels within old ones. Its skeleton was probably secreted as calcite crystals suspended in organic matrix; the crystals do not appear to have nucleated and grown on a sheeted substrate. It was clearly capable of asexual reproduction, through budding within parent funnels rather than at the apertural end. The morphology, skeletogenesis, and asexual reproduction of Cloudina are broadly similar to modern serpulid annelids, indicating possible phylogenetic relationships or morphological convergence.

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Geology; April 2005; v. 33; no. 4; p. 277–280; doi: 10.1130/G21198.1; 2 figures. 277
Skeletogenesis and asexual reproduction in the earliest
biomineralizing animal
Cloudina
Hong Hua Department of Geology and Laboratory of Continental Dynamics, Northwest University, Xi’an 710069, China
Zhe Chen
Xunlai Yuan 

Nanjing Institute of Geology and Paleontology, Nanjing 210008, China
Luyi Zhang Xi’an Institute of Geology and Mineral Resources, Xi’an 710054, China
Shuhai Xiao Department of Geosciences, Virginia Polytechnic Institute, Blacksburg, Virginia 24061, USA
ABSTRACT
The tubular fossil Cloudina is emerging as an important Ediacaran index fossil. How-
ever, its morphology, skeletogenesis, reproduction, and phylogenetic affinity have notbeen
fully resolved. New material from the Dengying Formation of south China confirms that
Cloudina tubes consist of eccentrically and sometimes deeply nested funnels and that the
tubes lack transverse cross-walls, inconsistent with the traditional cone-in-cone morpho-
logical reconstruction. Tube walls are composed of micrometer-sized, more or less equant
crystals. A number of Cloudina tubes branch dichotomously, in which daughter funnels
split within parent ones. The Cloudina animal is interpreted to have been able to initiate
biomineralization of new funnels within old ones. Its skeleton was probably secreted as
calcite crystals suspended in organic matrix; the crystals do not appear to have nucleated
and grown on a sheeted substrate. It was clearly capable of asexual reproduction,through
budding within parent funnels rather than at the apertural end. The morphology, skele-
togenesis, and asexual reproduction of Cloudina are broadly similar to modern serpulid
annelids, indicating possible phylogenetic relationships or morphological convergence.
Keywords: Cloudina, skeletogenesis, asexual reproduction, Ediacaran System, Dengying For-
mation, south China.
INTRODUCTION
The millimeter-sized tubular fossil Cloudi-
na is one of the earliest biomineralizing ani-
mals that occurs widely in deposits of the ter-
minal Neoproterozoic Ediacaran Period
(Grant, 1990; Hofmann and Mountjoy, 2001).
Radiometric dates from Namibia and Oman
constrain its stratigraphic occurrences to the
late Ediacaran, between 549 61 Ma and 542
61 Ma (Grotzinger et al., 1995; Amthor et
al., 2003). Its wide geographic distribution
and geochronologically calibrated stratigraph-
ic occurrences make Cloudina an excellent in-
dex fossil for the biostratigraphic subdivision
of the Ediacaran System.
However, the morphological detail of Clou-
dina has not been fully resolved, and little is
known about its skeletogenesis, mode of re-
production, and phylogenetic affinity. The
poor understanding of this important fossil is
largely because most Cloudina populations
are preserved as calcareous tubes in carbon-
ates (Germs, 1972) or as bedding-plane im-
pressions in siliciclastic rocks (Hagadorn and
Waggoner, 2000). As a result, it is difficult to
accurately reconstruct the three-dimensional
morphology of Cloudina based on the inter-
pretation of thin sections or external molds. In
this regard, phosphatized Cloudina from do-
lostone of the Dengying Formation in south-
ern Shaanxi Province, south China (Conway
Morris et al., 1990; Bengtson and Yue, 1992;
Hua et al., 2003), offers an opportunity to
learn more about its morphology, because the
Dengying material can be isolated from the
rock matrix. In this paper we report new ob-
servations and interpretations of the skeleto-
genesis and reproduction of Cloudina.
GEOLOGIC SETTING
The Dengying Formation in southern
Shaanxi Province is underlain by the Dou-
shantuo Formation (siltstone) and overlain by
the Kuanchuanpu Formation. The latter con-
sists of black chert and phosphatic dolostone
with basal Cambrian acritarchs (Yin, 1987)
and small shelly fossils (Xing et al., 1984).
The Dengying Formation comprises two
members—in stratigraphic order, the Algal
Dolostone Member (.10 m thick; light gray,
thick-bedded dolostone) and the Gaojiashan
Member (72 m thick; gray, thin-bedded cal-
careous mudstone and siltstone in the lower
part and thick-bedded dolostone in the upper
part). The Gaojiashan Member yields the
wormlike fossil Shaanxilithes ningqiangensis,
the tubular fossils Sinotubulites and Cloudina,
and many other metazoan fossils (Hua et al.,
2000). The Dengying Formation in the Yang-
tze Gorges area, ;400 km southeast of south-
ern Shaanxi Province, yields the tubular fossil
Sinotubulites baimatuoensis (Chen et al.,
1981) and frondose Ediacaran fossils that have
affinity with the Nama assemblage (Waggoner,
2003). Biostratigraphic and chemostratigraph-
ic correlations with Neoproterozoic succes-
sions in Namibia and Oman suggest that the
Dengying Formation in south China is prob-
ably ca. 550–542 Ma (Amthor et al., 2003;
Waggoner, 2003).
The Cloudina fossils described in this paper
were collected from dolostone of the upper
Gaojiashan Member at Lijiagou, southern
Shaanxi Province. They came from the same
horizon where previously reported Cloudina
was collected in this region. A stratigraphic
column can be found in Bengtson and Yue
(1992) and Hua et al. (2003). Samples were
digested in 5%–10% acetic acid for three
days, and Cloudina fossils were handpicked
from digestion residues. Isolated specimens
were studied by using a JSM 6300 scanning
electron microscope.
MORPHOLOGY
Most Cloudina tubes from the Dengying
Formation are incomplete and show evidence
of brittle breakage. They are preserved in
three dimensions, with none as a compressed
tube. Their basic morphology is broadly con-
sistent with previous descriptions (Germs,
1972; Glaessner, 1976; Conway Morris et al.,
1990; Grant, 1990; Bengtson and Yue, 1992;
Hagadorn and Fedo, 2000; Hua et al., 2003).
Tubes are typically 250–450 mm, but can
reach 2–3 mm, in diameter. They are as long
as 15 mm still-incomplete specimens. The
Dengying population can be referred to as
Cloudina riemkeae—the smaller of the two
recognized Cloudina species (Germs, 1972;
Grant, 1990). However, as the two species
may be synonymous (Grant, 1990), we follow
previous workers (Bengtson and Yue, 1992;
Hua et al., 2003) to refer the Dengying pop-
ulation to the type species, Cloudina
hartmannae.
The tube of Cloudina hartmannae is often
curved, with a closed base and an aperture
(Figs. 1A, 1B, 1F). There are no attachment
scars or anchoring structures on the hemi-
spherical basal end. The tube is made of a
series of funnel-shaped units, each 100–1000
mm in length. Except for the basal unit, the
funnels do not have a base; thus the tube has
no transverse cross-walls. Funnels are eccen-
trically stacked on each other so that neigh-
boring funnels may be closely juxtaposed on

278 GEOLOGY, April 2005
Figure 1.
Cloudina hartmannae
from Dengying Formation (A–P) and modern serpulid
Sal-
macina dysteri
from Qingdao, North China (Q–S). A–B: Hemispherical or bulbous basalend.
C: Deeply nested funnels. D–E: Eccentrically nested funnels with external annulations or
corrugations (E). F: Tube with funnel walls peeled off.No transverse cross-walls arepresent
within tube. G: Magnified view (arrow in F) showing stacked funnels. H: Magnified view
(arrow in G) showing granular crystals in funnel walls. Exterior to left. I: Dichotomous
branching (at upper end) within parent funnel. J–K: Magnified views of lower (J) and upper
(K) ends of specimen illustrated in I. L: Transverse cross section of two daughter funnels
within parent funnel. M–P: Daughter funnels diverge after reaching parent aperture. N is
basal view of specimen illustrated in M, showing medial split of daughter funnels. Parent
funnel in O is incompletely preserved, exposing daughter funnels. Q:
Salmacinadysteri
tube
showing asexual reproduction through dichotomous branching. Note annulations and cor-
rugations on external surface of tube wall. R: Dichotomous branching with daughter funnel
nested within parent funnel. S: Cross-section view of tube wall showing calcite crystals.
Internal surface (upper side) of tube wall is smooth. All are scanning electron microscope
images. Illustrated fossils are reposited in Nanjing Institute of Geology and Paleontology
(NIGPAS) and Early Life Institute (ELI) of Northwest University.Scale bar represents 400 mm
for A (NIGPAS 132516), F (ELI 20040014), I (ELI 20040015), M (ELI 20040016), O (ELI
20040018); 100 mm for B (ELI 20040011), G; 1000 mm for C (ELI 4370); 200 mm for D (ELI
20040012), E (ELI 20040013), J–L (NIGPAS 132529), N (ELI 20040017), P (NIGPAS 132528),
Q–R; 4 mm for H, S.
one side but widely separated on the other side
of the tube (Figs. 1D, 1E). The space between
neighboring funnels is variable (Figs. 1C–1E).
The funnels are sometimes deeply nested (Fig.
1C) and typically flare to form flanges (Figs.
1E–1G). Flanges may bend adaperturally to
join neighboring flanges, forming an outer
wall (Fig. 1C). The outer surface of the fun-
nels often has closely spaced annulations or
corrugations (Fig. 1E), but the inner surface is
typically smooth. In cross section, the funnels
are more or less circular with a 3–10-mm-thick
wall composed of more or less equant apatite
crystals ;0.5–2 mm in size (Fig. 1H).
Approximately 20 specimens in our collec-
tion of several hundred branch dichotomously
(Figs. 1I–1P). Branching begins with an al-
most equal split of a cylindrical funnel into
two half-cylinders (Figs. 1L–1N). The split
occurs within the parent funnel, typically
100–1000 mm below the aperture (Figs. 1I–
1K, 1O). The two daughter funnels gradually
become cylindrical but remain confluent with-
in the parent funnel. As soon as they reach the
parent aperture, the two daughters diverge at
an angle of ;458and their diameter increases
significantly (Figs. 1M–1P).
Germs (1972) reconstructed Cloudina as a
tubular fossil made of truncated cones stack-
ing on each other. On the basis of thin-section
interpretation, Grant (1990) suggested that
each stacking unit had a closed base, seen as
a transverse cross-wall in thin section. Grant
(1990) thus reconstructed Cloudina as a cone-
in-cone structure with multiple cross-walls, al-
though the majority of his material shows no
evidence of cross-walls. Hagadorn and Fedo
(2000) showed, through microscopic comput-
ed tomographic analysis, that Cloudina tubes
have no cross-walls.
No specimen isolated from the Dengying
Formation shows any evidence of transverse
cross-walls. It is unlikely that the cross-walls
were present but not preserved in our material
because their preservability would be similar
to the sidewalls. Instead, Cloudina tubes like-
ly did not have cross-walls (Hagadorn and
Fedo, 2000; J. Hagadorn, 2004, personal com-
mun.). The apparent cross-walls in the few
thin sections (Germs, 1972, Plate 1, Fig. 1
therein; Glaessner, 1976, Plate 2, Fig. 2 there-
in; Grant, 1990, Figs. 4B, 7A therein) are
probably artifacts resulting from oblique sec-
tions. As the stacking funnels are eccentric
and the tubes are curved, an oblique section
slanted toward the side where the funnels are
widely separated would produce apparent
cross-walls (Fig. 2). Such cross-walls are ac-
tually sections of sidewalls of nested funnels.
As most Cloudina tubes are curved, the like-
lihood of oblique sections is high. Apparent
cross-walls are expected to concentrate where
the tube curves out of the thin-section plane,

GEOLOGY, April 2005 279
Figure 2. A: Schematic diagram showing
oblique section (gray) of
Cloudina
tube. Ap-
parent transverse cross-walls are actually
sections of funnel sidewalls. B–E: Trans-
verse cross sections at different levels (ar-
rows) of
Cloudina
tube. Dashed lines repre-
sent approximate location of oblique
section. Numbers 1–4 indicate reference
points on tube and transverse cross
sections.
and the number of cross-walls in an oblique
section is expected to be fewer than that of
flanges. These appear to be true in sections
with apparent cross-walls (Germs, 1972;
Glaessner, 1976; Grant, 1990).
Cloudina hartmannae is thus reconstructed
as a tubular fossil with a closed base, an ap-
erture, but no transverse cross-walls (see also
Hagadorn and Fedo, 2000). The tube grows
through addition of funnel-shaped units that
are eccentrically stacked on each other. The
funnels have flared flanges that may join to-
gether to form an outer wall. The tube branch-
es dichotomously.
SKELETOGENESIS
The stacking pattern of the funnels suggests
that the Cloudina organism secreted new cal-
careous funnels within old ones. No algae are
known to grow by constructing new skeletons
within old ones. Protistan skeletons (e.g., for-
aminifers) tend to have restricted, rather than
flaring, apertures. The style of Cloudina skel-
etal growth is most consistent with animal
biomineralization (see following for modern
analogs).
The stacking pattern indicates that Cloudina
skeletal growth was episodic. The deeply nest-
ed funnels require that each episode of ske-
letogenesis was initiated within older funnels.
It is possible that the Cloudina animal had a
cylindrical mantle that was capable of build-
ing a new funnel instantaneously. Alternative-
ly, the Cloudina animal was able to retract it-
self to allow its specialized skeleton-secreting
organs to incrementally construct a new fun-
nel within an old one.
The funnel walls are made of micrometer-
sized apatite crystals (Hua et al., 2003). The
calcareous tubes from Namibia and Oman also
appear to be micritic (Conway Morris et al.,
1990; Grant, 1990). Diagenetic recrystalliza-
tion and replacement must have occurred, but
the fine grain size in the phosphatic and cal-
careous walls suggests that the original walls
were also made of micrometer-sized, probably
high-magnesium, calcite crystals (Grant,
1990). Because Cloudina tubes do not show
radial fibrous microstructure or palisade ori-
entation of crystals, crystal nucleation and
growth on a sheeted organic or inorganic sub-
strate did not play a significant role in Clou-
dina skeletogenesis. Rather, crystals were
probably precipitated by skeleton-secreting or-
gans and mixed with an organic matrix. The
mixture was then molded by the epidermis of
the Cloudina animal and cured to make cal-
careous walls. Such a process can explain why
the Cloudina skeletons show evidence of flex-
ibility (e.g., corrugation and folding on outer
surface) at skeletogenesis but brittleness at
burial.
ASEXUAL REPRODUCTION
Possible budding in Cloudina hartmannae
was reported by Germs (1972), and the Deng-
ying population includes well-preserved di-
chotomously branched Cloudina tubes, which
can be interpreted as evidence for asexual re-
production. The dichotomous split occurs
deep within the parent funnel, suggesting that
new buds were produced within the tube rath-
er than at the aperture. Thus, asexual budding
or splitting must have occurred at a subaper-
tural position of the Cloudina animal, or after
the parent animal retracted itself within the
parent funnel. Either way, the daughter ani-
mals, more or less simultaneously and shortly
after budding, began secretion of new funnels,
perhaps partially using the parent funnel wall
for economy of material (Figs. 1D, 1L). As no
polytomous branching has been known, the
Cloudina animal seems to be able to asexually
produce only two individuals at a time.
MODERN ANALOGS
Cloudina has been compared with serpulid
annelids and fossil cribricyathans, the latter
interpreted by some paleontologists as serpu-
lid annelids (Germs, 1972; Glaessner, 1976).
The Dengying fossils shed new light on the
comparison between Cloudina, serpulids, and
other living animals.
Serpulids are filter-feeding polychaete an-
nelids that make submillimeter- to millimeter-
sized calcareous tubes with small amount of
phosphorus (Vovelle et al., 1991). Like Clou-
dina, their tubes have a closed base, an aper-
ture, but no transverse cross-walls. Serpulid
tubes grow as new material—a mixture of cal-
cium carbonate and mucopolysaccharide—is
secreted by a pair of glands and molded onto
the apertural end by the collar (Hanson, 1948;
Hedley, 1958; Nott and Parker, 1975). Also
like Cloudina, the outer surface of serpulid
tubes has annulations or corrugations, whereas
the inner surface is smooth (Figs. 1Q, 1S).
Some serpulid tubes (e.g., Serpula) have reg-
ularly spaced, flaring flanges. Microstructure
of serpulid tubes is diverse. Many have a char-
acteristic chevron-like structure (Weedon,
1994). Neovermilia falcigera tube consists of
two layers—an inner layer of micrometer-
sized granular crystals and an outer layer of
micrometer-sized, radially oriented, acicular
crystals (Zibrowius and ten Hove, 1987). The
serpulid tube of Ficopomatus enigmaticus also
contains acicular calcite crystals, although not
radially arranged (Aliani et al., 1995). Our
own observation of Salmacina dysteri shows
that its tube is made of micrometer-sized gran-
ular calcite crystals (Fig. 1S), similar to that
of Cloudina (Fig. 1H).
Serpulids (e.g., Salmacina and Filograna)
can reproduce asexually, and they do so by
posterior budding in which a daughter bud is
formed at the basal (posterior) end of the an-
imal (Hanson, 1948; Pernet, 2001). When
asexual reproduction occurs, a biologically
programmed opening, temporarily covered by
a loosely secured calcareous disc known as an
escape hatch (Pernet, 2001), is created near
the aperture. After the daughter bud reaches
the opening, it either breaks away from the old
tube or secretes a new tube on the old one
(Hanson, 1948). Thus, serpulids can form di-
chotomous branches broadly similar to those
of Cloudina (cf. Figs. 1P, 1Q).
There are some significant differences be-
tween Cloudina and modern serpulid tubes,
however. Serpulid tube walls are thicker and
solid, and they do not consist of nested fun-
nels. In addition, the dichotomous branches of
serpulids are not as deeply nested within the
parent tube (Figs. 1Q, 1R). The solid and
thicker tubes of modern serpulids are likely an
adaptive response to stronger predation pres-
sure in the Phanerozoic. As the tubes become
thicker, the degree of funnel-in-funnel nesting
may be reduced because of economy of ma-
terial. Even Cloudina funnels partially utilize
parent walls when they are abutted against
each other (Figs. 1D, 1L).
Other animal tubes depart from Cloudina
tubes, in morphology and mineralogy, much
farther than serpulid tubes. Hydrozoans and
anthozoans, for example, make tubular calcar-

280 GEOLOGY, April 2005
eous skeletons. But hydrozoan skeletons have
distinct canals and pores, and anthozoan tubes
typically have vertical septa and transverse ta-
bulae. Anthozoan skeletons are secreted by a
calicoblastic layer that forms cup-like skeletal
units with transverse cross-walls. Further-
more, anthozoan skeletons are made of calcite
or aragonite needles that are organized into
fascicular sclerodermites, which nucleate and
grow on centers of calcification (Hill, 1981;
Cohen and McConnaughey, 2003). This struc-
tural organization is different from the gran-
ular microstructures seen in Cloudina tubes.
In addition, anthozoan asexual reproduction is
through longitudinal, lateral, or transverse fis-
sion (Ezaki and Yasuhara, 2004); it is impos-
sible for this style of asexual reproduction to
generate dichotomous branches that are deeply
nested in parent funnels. Other animals—such
as scyphozoans (e.g., Stephanoscyphus)
(Chapman and Werner, 1972), pogonophorans
(Ivanov, 1963), and pterobranchs—also pro-
duce dichotomous tubes. However, these are
all organic tubes, and pogonophorans are not
known to be able to reproduce asexually (Iva-
nov, 1963).
Several Neoproterozoic and Cambrian tu-
bular fossils, including Anabarites (Kouchin-
sky and Bengtson, 2002), Sphenothallus (van
Iten et al., 1992), and Sinocyclocyclicus (Xiao
et al., 2000), may also be compared with
Cloudina. However, these are distinguished
from Cloudina by their biomineralogy (Sphen-
othallus), transverse cross walls (Sinocyclo-
cyclicus), and triradial symmetry (Anabari-
tes). More significantly, the phylogenetic
affinities of most Neoproterozoic–Cambrian
tubular fossils are uncertain. Thus, compari-
son with these phylogenetically unresolved
fossils does not provide phylogenetic insight
for Cloudina.
CONCLUSIONS
The best modern analogs to Cloudina are
probably serpulid annelids. The morphology,
skeletogenesis, and asexual reproduction of
Cloudina are similar to serpulid annelids but
inconsistent with other tube-building animals.
Although such similarities can be convergent,
the traditional interpretation that Cloudina
was a close phylogenetic relative of annelids
(Germs, 1972; Glaessner, 1976) remains a
plausible hypothesis. Definitive tests of the
nature of this and other phylogenetic hypoth-
eses depend on knowledge about the soft-
tissue anatomy of the Cloudina animal. Con-
fident resolution of the phylogenetic position
of Cloudina is an important step toward a bet-
ter understanding of the early evolution of
biomineralizing animals.
ACKNOWLEDGMENTS
This work was supported by the National Natural
Science Foundation of China, the Chinese Ministry
of Sciences and Technology, the Chinese Ministry
of Education, and the National Science Foundation.
We thank Y. Xue and Y. Mao for field and technical
assistance, A.H. Knoll for lending Namibia speci-
mens, and J.W. Hagadorn and B. Pratt for thoughtful
reviews.
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Manuscript received 13 September 2004
Revised manuscript received 16 December 2004
Manuscript accepted 17 December 2004
Printed in USA