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The earliest Foraminifera from southern Shaanxi, China

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Biodiversity and taphonomy of the Early Cambrian Guanshan biota, eastern Yunnan

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Phylogeny and evolutionary significance of vermiform animals from the Early Cambrian Chengjiang Lagerstätte

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SCIENCE CHINA
Earth Sciences
• RESEARCH PAPER •

December 2010 Vol.53 No.12: 1756–1764
doi: 10.1007/s11430-010-4085-x

The earliest Foraminifera from southern Shaanxi, China
HUA Hong1*, CHEN Zhe2, YUAN XunLai2, XIAO ShuHai3 & CAI YaoPing1
1

Early Life Institute, State Key Laboratory of Continental Dynamics, Department of Geology, Northwest University,
Xi’an, 710069, China;
2
Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China;
3
Department of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia, 24061, USA
Received May 25, 2010; accepted September 13, 2010

Vase-shaped microfossils (VSMs) described herein mainly occur as isolated individuals in thin bedded siltstone and silty carbonate of the Gaojiashan Member of the upper Ediacaran Dengying Formation (ca. 551–541 Ma). Although these fossils are
abundant, chained tests or other types of colonial aggregates have not been observed. Specimens in the siltstones can easily be
isolated from the host rocks by ultrasonic vibrators. Compared with the co-occurring fossils Gaojiashania and Conotubus,
VSMs are rarely pyritized, yet they are always three-dimensionally persevered with little deformation, suggesting that their
tests were sturdy and possibly mineralized. Petrological observation and elemental mapping reveal two types of tests that are
respectively calcareous and siliceous in composition. Calcareous tests typically consist of two to three crypto-crystal laminae,
somewhat resembling bilamellar walls of foraminifers. Siliceous tests consist of fine-grained particles agglutinated with siliceous cement, similar to agglutinated walls of foraminifers. The Gaojiashan VSMs are broadly similar, at least in gross morphology, to the testate amoebae-like VSMs, but their relative large sizes (600–2400 µm) and possibly mineralized (rather than
organic) tests argue against this comparison. They also show some similarities to other protozoans, especially tintinnids. However, tintinnids ha; ve robust pesudochitinous loricae consisting of both secreted and agglutinated materials. Moreover, tintinnid
loricae differ in shape from the Gaojiashan VSM tests in having a constricted aboral end (sometimes with a caudal appendix)
and a flaring oral opening. If the Gaojiashan VSMs are indeed related to foraminifers, they indicate that foraminifers were important players in late Ediacaran communities.
Gaojiashan biota, vase-shaped microfossils, Foraminifera

Citation:

Hua H, Chen Z, Yuan X L, et al. The earliest Foraminifera from southern Shaanxi, China. Sci China Earth Sci, 2010, 53: 1756–1764,
doi: 10.1007/s11430-010-4085-x

The Foraminifera is one of the most important groups of
heterogeneous protists in modern marine ecosystems, and
has been extensively utilized for biostratigraphic, paleoceanographic, and paleoclimatic studies. However, many
questions about the earliest history of foraminifers are still
unresolved. When did the first foraminifers appear in the
geological record? What is the evolutionary and ecological
history of early foraminifers? Gaucher and Sprechermann [1]

*Corresponding author (email: huahong@nwu.edu.cn)

© Science China Press and Springer-Verlag Berlin Heidelberg 2010

reported small spheroidal to vase-shaped agglutinated fossils (Titanotheca coimbrae) from Vendian strata of Uruguay
and interpreted them as sacamminid foraminifers. Titanotheca’s simple morphology and poor preservation, however, do not allow an unambiguous interpretation as a foraminifer and alternative interpretations (e.g., agglutinated
testate amoebae such as Difflugia) are possible. The oldest
unambiguous foraminifers are from Early Cambrian Atdabanian Stage strata of the Taoudeni Basin in West Africa [2],
and the pre-Tommotian agglutinated tube-like fossils
Platysolenites, Spirosolenites and ?Psammosphera [3, 4].
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HUA Hong, et al.

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Fossil evidence thus indicates that the origin of foraminifer
biomineralization/agglutinization occurred during the
Ediacaran-Cambrian transition.
The term VSM is not a taxonomic name, but an informal
term originally proposed to describe microfossils with vaseto tear-shaped tests recovered from phosphatic nodules from
the Visingsö Group, Sweden [5]. VSMs are widely distributed in at least 18 horizons/localities in Neoproterozoic
rocks ranging from pre-Sturtian to Cryogenian in age (ca.
800–635 Ma) [6]. Various VSMs have been interpreted as
chitinozoans [7], Algal cysts [8], algal sporangia [9, 10],
heterotrophic planktonic protists similar to tintinnids [5, 11],
and testate amoebae [6, 11]. Although VSMs may include
different phylogenetic groups, test morphology of VSMs
from carbonate nodules of the upper Chuar Group suggests
their affinity with extant testate amoebae [12].
The study of VSMs in China can be traced back to the
late 1980s. Chinese VSMs have been reported from early
Neoproterozoic rocks [13, 14], the Ediacaran Doushantuo
Formation [15–18], the Ediacaran Dengying Formation
[19–21] and lower Cambrian rocks [22–24]. Among them,
the early Neoproterozoic VSMs came from the Diaoyutai
Formation in eastern Liaoning [13] and the Liulaobei Formation of the Huainan Group in Shouxian county of northern Anhui [14]; these fossils were processes through maceration, and their organic walls and small size (52–63 μm)
are comparable to the VSMs from the Chuar and Visingsö
groups. VSMs from chert nodules of the Doushantuo Formation are problematic, as their morphology is irregular and
they could represent phosphatic grains, poorly preserved
fossils of uncertain origin, or sedimentary structures [25].
Questionable VSMs have also been documented from Doushantuo phosphorites at Weng’an; however, their lack of a
distinct aperture weakens their comparison with aperturate
VSMs, and the Weng’an VSMs could represent poorly preserved acritarchs or algae. The early Cambrian VSMs from
the Xihaoping Member in southern Shaanxi and northwestern Hubei [26–29] are considered as disarticulated sclerites
of chancelloriids and synonyms of Cambrothyra [30].
VSMs of the late Ediacaran Dengying Formation are
mainly from the Gaojiashan biota. Previously reported as
Oolivoids-like fossils [31], these Gaojiashan fossils were
later redescribed as vase-shaped microfossils under two
genera and six species whose distinction was based on aperture morphology [19, 20]. The original compositions of
VSM tests are thought to be calcareous. A vase-shaped fossil has been reported from a thin section of the Taozichong
Formation at Qingzhen, Guizhou Province [21], and resembles closely the tests of Gaojiashan VSMs in size, shape,
and wall composition. This discovery greatly expands the
geographic distribution of VSMs in China.
This paper is to present new data about the test structure,
wall composition, and size variation of the Gaojiashan
VSMs. Two types of VSMs tests are recognized and they
show some similarities to the tests of agglutinated and cal-

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careous foraminifers.

1

Materials and methods

The fossiliferous samples described here were collected
from the middle Gaojiashan Member at the Haihaoliang and
Gaojiashan-Niuluokeng sections of the Gaojiashan outcrop
belt and Shiziya and Tudimiao sections of the Hujiaba outcrop belt [32]. VSMs occur mainly as isolated individuals in
thin-bedded siltstone and silty carbonate [31], but they can
be concentrated on certain bedding surfaces at a density of
over 30 individuals in an area of about 20 cm×15 cm. Despite such dense occurrences, the fossils do not form chains
or other types of colonial aggregates. Specimens can be
easily distinguished by their light grey to brownish or dark
grey colors.
Forty five samples (each 2–5 kg) were systematically
collected from the fossiliferous middle Gaojiashan Member.
The samples were crushed to fragments approximately 8
cm×5 cm×2 cm in size. The fragments were then soaked in
water for a period of about two or three days. An ultrasonic
vibrator was used to dislodge the fossils from the soaked
fragments. The residues from ultrasonic disintegration were
washed using a 63 µm screen and were dried. Nearly one
thousand fossils were handpicked from the dried residue
under a binocular microscope. The extracted fossils were
mounted on aluminum stubs and examined in a Philips
Quantum 400 scanning electron microscope (SEM) at 5 or
10 kV. A few selected fossils were embedded in epoxy, thin
sectioned, and studied under a compound light microscope.

2 Paleobiology
2.1

Test morphology

The test consists of a spherical to ellipsoidal body, a constricted neck, and flaring aperture (Figure 1); sometimes, a
lip-like structure partially covers the aperture (Figure 1(b)).
The aperture is circular. The maximal diameter of the test is
typically located at 22%–31% of the test from the aboral
end. The maximum diameter is about 1.23–6.52 times the
diameter at the flaring aperture end. The aboral end is always rounded, never with a protuberance, spine, or appendix (Figure 1).
Gaojiashan VSMs have a large range of size. The aboraloral length of the test varies from 560 to 2400 μm (Figure 2,
mean 1280 μm, standard deviation 388 μm, n=100), and test
maximum diameter from 560 to 2179 μm (Figure 3, mean
1071 μm, standard deviation 261 μm, n=96). Despite the
wide ranges, the size distributions are unimodal, with 61%
of aboral-oral length measurements within the limit of
900–1500 μm, and 77% of the maximum diameter measurements within 700–1300 μm. The diameter at the apertural end has a wide variation from 160 to 1079 μm (mean

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December (2010) Vol.53 No.12

Figure 1 Morphology of VSMs in the Gaojiashan biota. All specimens illustrated here are from the middle Gaojiashan Member at the GaojiashanNiuluokeng section in Hujiaba, Ningqiang county, Shaanxi Province, and deposited at the Department of Geology, Northwest University. All Scale bars
measure 200 µm. Sicylagena formosa Zhang 1994, ELI-H-10021; (b) Sicylagena latistoma Zhang 1994, ELI-H-10022; (c) Protolagena cylindrata Zhang
1994, ELI-H-10023; (d), (f), (h), (i) Protolagena gaojiashanensis Zhang et Li 1991; ELI-H-10024 (d), ELI-H-10026 (f), ELI-H-10028 (h), ELI-H-10029 (i);
(e) Vase-shaped microfossil gen. et sp. undetermined, showing brittle fractures, ELI-H-10025; (g) Vase-shaped microfossil gen. et sp. undetermined, showing deformed test, ELI-H-10027; (j) Protolagena papillatus Zhang 1994, ELI-H-10030.

466 μm, standard deviation 168 μm, n=88). The ratio of test
maximum diameter over aboral-oral length varies between
0.344 and 2.214 (Figure 4), with 87% of the measurements
within the limit of 0.7–1.0. The ratio of test maximum diameter over apertural end diameter ranges from 1.23 to 6.52,
with 67% of the measurements within the limit of 1.5–2.7
(Figure 5). Among the six species named by Zhang et al.
[19, 20], there seems no significant difference in size variation. This indicates that the six named species may be synonymous. Analyses of other morphological characters (apertural end diameter, neck diameter, neck length, and body

length) also show similarities among the six species.
Only a few protist groups have a vase-shaped tests or loricae; of these, testate amoebae, especially the agglutinated
Difflugia resemble the Gaojiashan VSMs in their tear- or
cup-shaped test and conical or cylindrical neck. Although
some may reach as large as 600 μm, testate amoebae typically are only 50–200 μm in length and 15–105 μm in width,
with a ratio of length: width between 1:1 and 3:1. Thus, the
Gaojiashan VSMs are significantly larger than living tested
amoebae. They are also much larger than Neoproterozoic
Testate amoebae-like VSMs [6], which are typically 25–286

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Figure 2

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Histogram showing the distribution of aboral-oral lengths.

December (2010) Vol.53 No.12

1759

Figure 5 Histogram showing the distribution of maximum diameter/neck
diameter ratios.

differ from Gaojiashan VSMs in their aboral appendix and
much wider oral opening.
2.2

Figure 3

Histogram showing the distribution of maximum diameters.

Figure 4 Histogram showing the distribution of maximum diameter/aboral-oral length ratios.

μm in length and 17–202 µm in test width.
The Gaojiashan VSMs also show some similarities to
other protists such as chitinozoans and tintinnids. Chitinozoans have organic tests, which often bear complex ornamentations. Tintinnids have robust pesudochitinous loricae
(some with an appendix) consisting of a combination of
secreted and agglutinated materials. Ttintinnid loricae also

Wall composition and texture of Gaojiashan VSMs

Gaojiashan VSMs, generally three-dimensionally preserved,
offer an opportunity for observation using both light microscopy and SEM. Two types of tests can be recognized
using light microscopy: one type is characterized with light
grey tests consisting of calcareous material, and the other
type is characterized with darker colored tests presumably
siliceous in composition. SEM elemental analyses of the
tests confirm the calcareous and siliceous composition of
the two types of tests.
The original chemical composition of the tests is still not
so clear, although Zhang and Li [19] proposed that the tests
were originally calcareous but can be secondarily silicified
or pyritized. CuO and ZnO were also detected by Zhang
[20]; of the 13 analyzed specimens, 9 contained CuO and
ZnO up to 10.79% and 12.65% respectively. Given the low
content of CuO in matrix (only 10×10−6–30×10−6), it is possible that the concentration of CuO and ZnO was related to
biomineralization. However, we analyzed 56 specimens but
none showed detectable amount of CuO and ZnO. We thus
suspect that the relatively high CuO and ZnO contents reported by Zhang were due to contamination from copper
sieves during sample processing.
The two types of VSMs are described below.
(1) VSMs with calcareous tests. They account for about
1/3 of the studied population. They are mostly threedimensionally preserved, with little deformation. The thickness of the wall is relatively uniform within a specimen, but
may vary from 14 to 40 μm between specimens. Apart from
the apertural region, the wall is generally laminated and
composed of 2–3 crypto-crystal layers. Often, a transverse
fibrous layer is discernible (Figure 6). Chemical compositions of the walls are quite distinct, with CaO ranging from
85.3% to 100%, Fe2O3 from 0% to 4.07%, and only minor
amount of MgO and SiO2. The result is compatible with

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Laser Raman microprobe analysis that detected calcite and
aragonite in the tests [19].
Laser Raman analysis of foraminiferal tests has thus far
been limited to hyaline tests. The hyaline taxa Ammonia
beccarii (Linné) and Rosalina posidonicola (Colom) are
calcitic and Hoeglundina elegans (d'Orbigny) is aragonitic
[33].
(2) VSMs with siliceous tests. They are generally deformed and compressed (thus showing evidence of flexibility), although brittle cracks also occur at outer margin of
some samples (Figure 1(e)). Wall thickness is generally not
so uniform and varies greatly in a test (Figure 7(a)). The
wall is mainly of SiO2 in composition as revealed by elemental spectrum analysis; however, the presence of particles of distinct compositions in the test wall suggests a possible agglutinated nature of the siliceous tests.
Although there is significant variation in wall texture
among different siliceous tests, three different types of
laminae can be recognized (Figure 7).
Type I laminae. Elemental mapping shows that this type
of laminae consists of siliceous material of variable thickness from 14 to 17 μm. It is typically smooth in the outer
margin or has a transitional boundary with an outer type II
lamina. Dissolution of the agglutinated particles leaves a
ragged boundary between types I and II laminae. The inner

December (2010) Vol.53 No.12

surface of type I laminae is generally coated with acicular
carbonate minerals of type III laminae.
Type I laminae are the most common texture of siliceous
VSMs, and they are characterized with zonal distribution of
irregular microvoids, which are interpreted as molds of agglutinated particles. Close-ups of the wall under SEM show
the presence of two distinct micro-layers, and the microvoids in the outer micro-layer are relatively bigger than
those in the inner micro-layer. The selective dissolution of
agglutinated particles is a feature similar to dissolution of
clasts in silicified breccias, although at a much smaller scale.
Such microvoids are widely distributed along the boundary
between type I laminae and the outer type II laminae.
Some agglutinated foraminifers with siliceous wall
(microcrystalline quartz) from the Barnett Shale (Lower
Mississippian) of central Texas [34] and from Late Devonian (Frasnian and Famennian) black shales of the Appalachian and Illinois basins of the eastern US [35] also have
wall texture similar to type I laminae of the Gaojiashan
VSMs. In these foraminifers, the agglutinated grains are
recrystallized and are hard to identify; silt- and mud-sized
detrital grains can only be recognized under cathodoluminescence imaging. Test walls of the giant agglutinated foraminifera Bathysiphon from Cretaceous turbidites of
northern California also consist of quartz grains, sponge

Figure 6 Thin section photomicrographs of calcareous VSMs, showing the laminated wall texture and transverse fibrous structure. (a) Protolagena limbata
Zhang et Li 1991, longitudinal thin-section, showing the laminated texture of the wall, with a dark inner layer surrounded by lighter outer layers consisting of
cryptocrystalline calcite; (b), (c) Sicylagena latistoma Zhang 1994, longitudinal thin-section, showing laminated wall structure, (c) is an enlargement of (b)
showing the transverse fibrous structure. Scale bars are 200 μm (a); 150 μm (b), and 50 μm (c), respectively.

Table 1

Elemental analysis of a siliceous test

3.48

Al2O3 (%)
0.92
22.08

0.97

19.91

MgO (%)
Spot 1
Spot 2
Spot 3
Spot 4

SiO2 (%)
90.20
59.49
100.00
62.48

CaO (%)
8.88

K2O (%)

TiO2 (%)

Fe2O3 (%)

10.43

0.84

3.69

15.17

1.48

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Figure 7 Electron microphotographs showing texture of siliceous VSMs from the Gaojiashan Member. Lamina types I, II, and III are indicated as I, II and
III on the figures (see text for explanation).

spicules, and less commonly other mineral grains and bioclasts [36]. After recrystallization, these agglutinated grains
appear only as ghosts.
Type II laminae. Type II laminae occur only in some
specimens, and have a thickness varying from 14 to 17 μm.
They typically overlie (or lie outside of) type I laminae. They
have a smooth outer margin but an irregular inner margin due
to the dissolution of agglutinated grains. The boundary between types I and II laminae is often transitional.
Type II laminae are constructed from agglutinated material of various morphologies, grain sizes, and composition.
The agglutinated grains have fair to poor roundness, and
they are relatively large (with grain sizes ranging from 0.5
to 5 μm) than those in type I laminae. Composition of the
grains is very complex, including both calcareous and siliceous grains.
Type III laminae. Type III laminae are rare and they oc-

cur only in some samples. They usually occur on the inner
side of the test wall, with a thickness of about 40 μm, and
consist of calcareous lime mud and are rimmed with radially orientated acicular calcite crystals of diagenetic origin.
Gaojiashan VSM test wall texture can have the following
combinations of laminae, namely: type I lamina alone; types
I and II laminae; and types I and III laminae.
There is a tendency for agglutinated particles to increase
in grain size from the inner to outer wall in many agglutinated foraminifers, a phenomenon that has also been well
documented in the Early Cambrian fossil Platysolenites [37].
Agglutinated grains in Platysolenites tests are typically
about 20 µm and may be up to 36 μm on the outer wall, but
only about 10 µm on the inner wall. The size gradient of
agglutinated particles in the Gaojiashan VSM tests is thus
similar to some agglutinated foraminifers.

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Discussion

Foraminifers are single-celled protists belonging to the
clade Rhizaria. They are amoeboid protists with reticulating
pseudopods and fine strands of cytoplasm that branch and
merge to form a dynamic net. They typically produce a test,
which can have either one or multiple chambers, some
becoming quite elaborate in structure. The shell can be
made of organic material, calcium carbonate (CaCO3), or
agglutinated sediments including sand grains, sponge
spicules, mica flakes, etc.
Traditionally, the origin and early evolution of the Foraminifera are depicted as a gradual change in test composition and structure, from simple organic-walled thecate
unilocular forms, to forms with agglutinated walls, and
eventually to multilocular forms [38]. Paleontological evidence places the first appearance of agglutinated foraminifers in the Early Cambrian [3, 37]. Recent molecular
phylogenies, however, indicate that the divergence of naked
foraminifers and unilocular agglutinated foraminifers occurred about 690–590 Ma [39], and the origin of foraminifera may have a deeper history that dates back a billion or
more years [40]. The fossil record of the earliest foraminifers may be systematically biased by their poor preservation
potential.
Testate amoebae and tintinnids are two groups of protozoa with simple vase-shaped morphology, and although
they are somewhat similar to the VSMs reported herein,
they differ in many respects such as relatively small sizes
and mostly organic walls with distinct ornamentations. The
Gaojiashan VSMs, with their unilocular and aperturate tests,
agglutinated or calcareous walls and relatively large sizes
resemble foraminifers more closely than testate amoebae
and tintinnids. The earliest foraminifers might have been
naked or organic-walled unilocular forms and left no recognizable fossils. The agglutinated Platysolenites is thus far
the first known foraminifer fossils. The size gradient of agglutinated grains across Platysolenites walls, as well as the
brittle breakage and plastic deformation of Platysolenites
tests, are features shared by the Gaojiashan VSMs. Bulbous
proloculi were first discovered in Platysolenites by McIlroy
et al. [3], and a non-septate tubular chamber preceded by the
proloculi was interpreted as the adult test of this foraminifer.
Based on their study of Platysolenites and related fossils,
McIlroy and his colleagues proposed three evolutionary
trends of early foraminifers, namely the evolution of spiral
growth, the loss of prolucus, and the loss of the adult tubular test. The bulbous proloculus of Platysolenites in the
Lower Cambrian of Nevada [37] also shows some close
similarities to the Gaojiashan VSMs: it has an agglutinated
wall, a distinct neck with an aperture, and a relatively large
size (about 680 µm long and about 200 µm in maximum
diameter).
“Calcispheres” are spherical calcareous microfossils of

December (2010) Vol.53 No.12

unknown biological affinity commonly found in Paleozoic
limestones, especially in the Carboniferous and Permian.
They are about 75 to 200 μm in diameter, and consist of a
micritic wall enclosing an interior space that is hollow or
filled with sparry-calcite (sparite). Calcispheres somewhat
resemble the Gaojiashan VSMs in their spherical morphologies, but they lack an aperture, they are much smaller
in sizes, and their tests consist of well orientated calcite
crystals. They have long been considered as “microproblematica” [41], although some paleontologists interpret
them as dasycladacean algae (e.g., reproductive cysts of
Acetabularia [42]) or perhaps as possible foraminifera [43].
Some Paleozoic calcispheres have also been interpreted as
secondarily (post mortem) calcified acritarchs and volvocacean algae [44, 45].
The origin of biomineralization represents one of the
prime episodes of evolutionary innovation that transformed
the paleontological record from one of non-skeletal fossils
to one that is familiarly dominated by skeletal remains. The
origination of animal skeletons also significantly expanded
the possibilities of ecological interactions in marine ecosystems. These new ecological tenets included enhanced utilization of, and thus competition for, ecospace above the sea
floor, i.e., epibenthic tiering [46–49] and sophisticated
predatory and defense mechanisms and strategies [50–52].
Finally, at the global scale, the origin and diversification of
biomineralizing organisms had an immense impact on
global biogeochemical cycles, modulating marine C, Ca, Si,
and P cycles [53] and ultimately affecting global climate
change [54]. Thus, the origin(s) of biomineralization may be
viewed as one of the most critical events in the evolutionary,
ecological, and biogeochemical history of this planet, and
understanding the earliest biomineralizing organisms is of
utmost importance to gaining insight into the evolution of
advanced life and a biological planet.
Much paleontological research on biomineralization has
been directed to the study of the Cambrian radiation of
biomineralizing animals [55, 56]. However, increasing evidence suggests that the evolutionary radiation of biomineralization in the Cambrian Period was preceded by weakly
biomineralized animals in the late Ediacaran period around
550–541 Ma [57–61] and biomineralizing protists in the
middle Neoproterozoic [62].
As indicated by Culver [2], little attention has been paid
to the protists when we studied the origin of biomineralization in animals. Indeed, some hypotheses concerning the
origin of hard parts in animals (e.g., biomineralization as a
way to increase body size or a detoxification strategy) could
be potentially weakened if one considers the origin of
biomineralization in protists. What may have triggered the
advent of skeletonization in the Neoproterozoic? The independent evolution of biomineralization in calcareous and
agglutinated foraminifers, Cloudina and related organisms,
and other weakly biomineralizing metazoans in the Gaojiashan biota strongly supports the “arm race” hypothesis,

HUA Hong, et al.

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and indicates that the primary function of skeletons might
be for protection against predation.

4

Conclusions

(1) VSMs in Gaojiashan biota may be the earliest foraminifers, and if so they may have played an important
ecological role in Ediacaran shallow marine environments.
(2) Two types VSMs (respectively with calcareous and
agglutinated tests) are found in the Gaojiashan biota. Their
wall structures and textures are broadly similar to those of
calcareous and agglutinated foraminifers.
We sincerely thank Wang Xin and Ma Ji for help with SEM analysis, Shen
Shuzhong, Zhu Maoyan and Li Guoxiang provided constructive comments.
This study was supported by National Basic Research Program of China
(Grant No. 2006CB806400), National Natural Science Foundation of
China (Grant No. 40872021), Program for New Century Excellent Talents
in University, State Key Laboratory of Continental Dynamics and
Northwest University Doctoral Dissertation Funds (Grant No. 09YYB01).
1
2
3

4
5

6

7

8

9

10

11

12

13

14

Gaucher C, Sprechermann P. Upper Vendian skeletal fauna of the
Arroyo del Sodado Group, Uruguay. Beringeria, 1999, 23: 55–91
Culver S J. Early Cambrian foraminifera from West Africa. Science,
1991, 254: 689–691
McIlroy D, Green O R, Brasier M D. Palaeobiology and evolution of
the earliest agglutinated Foraminifera: Platysolenites, Spirosolenites
and related forms. Lethaia, 2001, 34: 13–29
Lipps J H, Rozanov A Y. The Late Precambrian-Cambrian agglutinated fossil Platysolenites. Palaeontol J, 1996, 10: 687–697
Knoll A H, Vidal G. Late Proterozoic vase-shaped microfossils from
the Visingsö Beds, Sweden. Geol Föreningen Stockholm Förhandl,
1980, 102: 207–211
Porter S M, Knoll A H. Testate amoebae in the Neoproterozoic Era:
Evidence from vase-shaped microfossils in the Chuar Group, Grand
Canyon. Paleobiology, 2000, 26: 360–385
Bloeser B, Schopf J W, Horodyski R J, et al. Chitinozoans from the
Late Precambrian Chuar Group of the Grand Canyon, Arizona. Science, 1977, 195: 676–679
Bloeser B. Melanocyrillium, a new genus of structurally complex
Late Proterozoic microfossils from the Kwagunt Formation (Chuar
Group), Grand Canyon, Arizona. J Paleontol, 1985, 59: 741–765
Horodyski R J. A new occurrence of the vase-shaped fossil Melanocyrillium and new data on this relatively complex Late Precambrian
fossil. Geol Soc Amer Abstr Programs, 1987, 19: 707
Horodyski R J. Paleontology of Proterozoic shales and mudstones:
Examples from the Belt Supergroup, Chuar Group and Pahrump
Group, western USA. In: Nagy B, Leventhal J S, Grant R F, eds.
Metalliferous Black Shales and Related Ore Deposits. Precambrian
Res, 1993, 61: 241–278
Knoll A H, Calder S. Microbiotas of the late Precambrian Ryssö
Formation, Nordaustlandet, Svalbard. Palaeontology, 1983, 26:
467–496
Porter S M, Meisterfeld R, Knoll A H. Vase-shaped microfossils
from the Neoproterozoic Chuar Group, Grand Canyon: A classification guided by modern testate amoebae. J Paleontol, 2003, 77:
409–429
Yin L M. Late Precambrian microfossils from Diaoyutai Formation,
Eastern Liaoning, China. Paper for the 5th International Conference.
Nanjing: Nanjing Institute of Geology and Palaeontology, Chinese
Academy of Sciences, 1980. 18
Zang W L, Walter M R. Late Proterozoic and Early Cambrian mi-

December (2010) Vol.53 No.12

15

16

17

18
19

20

21

22

23

24
25

26

27
28

29
30

31

32

33

34

35

36
37
38

1763

crofossils and biostratigraphy, northern Anhui and Jiangsu, centraleastern China. Precambrian Res, 1992, 57: 243–323
Duan C H, Cao F. New discovery of vase-like fossils from Eastern
Yangtze Gorges, Hubei. Period Tianjin Institute Geol Mineral Resources, 1989, (21) : 130–147
Wu X H, Wang S Y. Possible phosphatized protozoan fossils from
the late Neoproterozoic Doushantuo phosphorites in Guizhou Province. Acta Micropalaentol Sin, 2004, 21: 194–198
Li Y, Guo J F, Zhang X L, et al. Vase-shaped microfossils from the
Ediacaran Weng’an biota, Guizhou, South China. Gondwana Res,
2008, 14: 263–268
Ren C Y, Liu L Q, Zhou Y H, et al. Vase-shaped Microfossils from
Weng’an Biota. J Earth Sci Environment, 2008, 30: 249–252
Zhang L Y, Li Y. The Late Sinian vasiform microfossils of Ningqiang, Shaanxi Province. Period Xi’an Institute Geol Min Resources,
1991, (31): 77–86
Zhang L Y. A new progress in research on vase-shaped microfossils
from the Dengying Formation of Sinian in southern Shaanxi Province.
Acta Geol Gansu, 1994, 3: 1–8
Xue Y S, Zhou C M, Tang T F. New material of animal fossils from
the Upper Sinian of the Yangtze Region, southern China. Acta Palaeontol Sin, 2002, 41: 137–141
Duan C H, Cao F, Zhang L Y. Vase-shaped microfossils from top of
the Dengying Formation in Xixiang, Shaanxi. Acta Micropalaeontol
Sin, 1993, 10: 397–408
Cao F, Duan C H, Zhang L Y. The discovery and significance of the
vase-shaped microfossils in Meishucunian stage in Ningqiang,
Shaanxi. Geol Rev, 1995, 41: 355–362
Cao F. Study on the vase-shaped microfossils in China. Acta Micropalaeontol Sin, 1998, 15: 404–416
Zhang Z Y. Comments on the “Vase-shaped microfossils” from the
Doushantuo Formation of the eastern Yangtze Gorges. Acta Micropalaeontol Sin, 1994, 11: 369–371
Qian Y, Zhang S B. Small shelly fossils from the Xihaoping Member
of the Dongying Formation in Fangxian county of Hubei Province
and their stratigraphic significance. Acta Palaeontol Sin, 1983, 22:
82–94
Duan C H. Vase-like fossils of Precambrian in Hubei, Fangxian. Period Tianjin Institute Geol Mineral Resources, 1986, (13): 87–120
Geng L Y, Zhang S B. Early Cambrian problematic fossils from
Fangxian, Hubei, China. In: Stratigraphy and Paleontology of Systemic Boundaries in China. Precambrian-Cambrian Boundary (1).
Nanjing: Nanjing University Publishing House, 1977. 523–536
Zhao Z Q, Xing Y S, Ding Q X, et al. The Sinian System of Hubei.
Wuhan: China University of Geosciences Press, 1988. 1–205
Qian Y, Sun W G, He D G, et al. Restudy on “vase-shaped microfossils” from the Lower Cambrian Xihaoping Member in south Shaanxi
and west Hubei. Acta Micropalaeontol Sin, 2000, 17: 317–326
Zhang L Y. A discovery and preliminary study of the Late Sinian
stage Gaojiashan Biota from Ningqiang county, Shaanxi. Bull Xi’an
Institute Geol Mineral Res Chin Acad Geol Sci, 1986, 13: 67–88
Cai Y, Hua H, Xiao S, et al. Biostratinomy of the late Ediacaran pyritized Gaojiashan Lagerstätte from southern Shaanxi, South China:
Importance of event deposits. Palaios, 2010, 25: 487–506
Vénéc-Peyré M T, Jaeschke-boyer H. Application de la microsonde
moléculaire à laser à Pétude du test de quelques Foraninifères
cslcaires. Copt Rend Acad Sci Paris-Sér D, 1978, 287: 607–609
Milliken K L, Choh S J, Papazis P, et al. “Cherty” stringers in the
Barnett Shale are agglutinated foraminifera. Sediment Geol, 2007,
198: 221–232
Schieber J. Discovery of agglutinated benthic foraminifera in Devonian black shales and their relevance for the redox state of ancient
seas. Palaeogeogr Palaeocl Palaeoecol, 2009, 271: 292–300
Miller W III. Giant bathysiphon (Foraminiferida) from Cretaceous
turbidites, Northern California. Lethaia, 1988, 21: 363–374
Streng M, Babcock L E, Hollingsworth J S. Agglutinated protists
from the Lower Cambrian Nevada. J Paleontol, 2005, 79: 1214–1218
Hansen H J. Test structure and evolution in the Foraminifera. Lethaia,
1977, 122: 173–182

1764
39
40
41
42
43

44

45

46

47
48

49

50
51

HUA Hong, et al.

Sci China Earth Sci

Pawlowski J, Holzmann M, Berney C. The evolution of early Foraminifera. Proc Natl Acad Sci, 2003, 100: 11494–11498
Langer M R. Origin of foraminifera: Conflicting molecular and paleontological data? Mar Micropaleontol, 1999, 38: 1–5
Flügel E. Microfacies of Carbonate Rocks—Analysis, Interpretation
and Application. Berlin: Springer, 2004. 976
Marszalek D S. Calcisphere ultrastructure and skeletal aragonite from
the alga Acetabularia antillana. J Sediment Petrol, 1975, 45: 266–271
Samtleben C, Munnecke A, Bickert T, et al. Shell construction, assemblage and species dependent effects on the C/O-isotopic composition of brachiopods—Examples from the Silurian of Gotland. Chem
Geol, 2001, 175: 61–107
Kazmierczak J. Volvocacean nature of some Paleozoic nonradiosphaerid calcispheres and parathuramminid “foraminifera”. Acta
Paleontol Pol, 1976, 10: 73–85
Kazmierczak J, Ittekkot V, Degens E T. Biocalcification through time:
Environmental challenge and cellular response. Paläontol Zeitschrift,
1985, 59: 15–33
Ausich W I, Bottjer D J. Sessile invertebrates. In: Briggs D E G,
Crowther P R, eds. Palaeobiology II. Oxford: Blackwell, 2001.
384–386
Clapham M E, Narbonne G M. Ediacaran epifaunal tiering. Geology,
2002, 30: 627–630
Yuan X, Xiao S X, Parsley R L, et al. Towering sponges in an Early
Cambrian Lagerstätte: Disparity between non-bilaterian and bilaterian epifaunal tiers during the Neoproterozoic-Cambrian transition.
Geology, 2002, 30: 363–366
Clapham M E, Narbonne G M, Gehling J G. Paleoecology of the
oldest known animal communities: Ediacaran assemblages at Mistaken Point, Newfoundland. Paleobiology, 2003, 29: 527–544
Vermeij G J. Evolution and Escalation. Princeton: Princeton University Press, 1987
Bengtson S, Yue Z. Predatorial borings in late Precambrian mineralized exoskeletons. Science, 1992, 257: 367–369

December (2010) Vol.53 No.12

52

53
54

55

56

57

58

59

60

61

62

Hua H, Pratt B R, Zhang L Y. Borings in Cloudina shells: Complex
predator-prey dynamics in the terminal Neoproterozoic. Palaios, 2003,
18: 454–459
Van Cappellen P. Biomineralization and global biogeochemical cycles. Rev Mineral Geochem, 2003, 54: 357–381
Westbroek P, Brown C W, Bleijswijk J V, et al. A model system approach to biological climate forcing: The example of Emiliania huxleyi. Global Planet Change, 1993, 8: 27–46
Bengtson S, Conway M S. Early radiation of biomineralizing phyla.
In: Lipps J H, Signor P W, eds. Origin and Early Evolution of Metazoa. New York: Plenum Press, 1992. 447–481
Bengtson S. Mineralized skeletons and early animal evolution. In:
Briggs D E G, ed. Evolving Form and Function: Fossils and Development. New Haven, CT: Yale Peabody Museum Publications, 2005.
101–124
Grant S W F. Shell structure and distribution of Cloudina, a potential
index fossil for the terminal Proterozoic. Am J Sci, 1990, 290-A:
261–294
Amthor J E, Grotzinger J P, Schröder S, et al. Extinction of Cloudina
and Namacalathus at the Precambrian-Cambrian boundary in Oman.
Geology, 2003, 31: 431–434
Hua H, Chen Z, Yuan X, et al. Skeletogenesis and asexual reproduction in the earliest biomineralizing animal Cloudina. Geology, 2005,
33: 277–280
Hua H, Chen Z, Yuan X. The advent of mineralized skeletons in
Neoproterozoic Metazoa: New fossil evidence from the Gaojiashan
Fauna. Geol J, 2007, 42: 263–279
Bowring S A, Grotzinger J P, Condon D J, et al. Geochronologic
constraints on the chronostratigraphic framework of the Neoproterozoic Huqf Supergroup, Sultanate of Oman. Am J Sci, 2007, 307:
1097–1145
Francis A M, Cohen P A, Dudás F Ö, et al. Early Neoproterozoic
scale microfossils in the Lower Tindir Group of Alaska and the
Yukon Territory. Geology, 2010, 38: 143–146