[Palaeontology, Vol. 50, Part 6, 2007, pp.

13911402]

RHYNCHONELLIFORMEAN BRACHIOPODS WITH

SOFT-TISSUE PRESERVATION FROM THE EARLY
TTE OF SOUTH
CAMBRIAN CHENGJIANG LAGERSTA
CHINA
by ZHIFEI ZHANG*, DEGAN SHU*, CHRISTIAN EMIG, XINGLIANG ZHANG*,
JIAN HAN*, JIANNI LIU*, YONG LI and JUNFENG GUO*
*Early Life Institute, State Key Laboratory of Continental Dynamics, Northwest University, Xian 710069, China; e-mail: elizf@nwu.edu.cn or, zhangelle@126.com
Centre dOceanologie de Marseille, Rue de la Batterie-des-Lions, 13007 Marseille, France
College of Earth Science and Land Resources, Changan University, Xian 710054, China
Typescript received 13 July 2006; accepted in revised form 30 November 2006

ophore attains an early spirolophe stage, clearly homologous

to that in the coeval lingulids. The digestive tract consists
of a mouth, oesophagus, swollen stomach, intestine and a
terminal anus. The pedicle protruding between the valves is
stout and elongate, with annulated lamellae on the surface,
and contains a putative clomic cavity. K. chengjiangensis
displays the characteristics of the stem group of calcareous
brachiopods, and illustrates anatomical similarities between
Cambrian phosphatic- and calcareous-shelled brachiopods,
thus corroborating that the Brachiopoda are a monophyletic
group.

Abstract: Cosmopolitan kutorginates, the most abundant

Early Cambrian rhynchonelliformean brachiopods, became
extinct at the end of the Middle Cambrian. Consequently,
any information concerning the anatomy of this peculiar
lineage of brachiopods has great phylogenetic significance
with regard to their extant relatives for analogies with the
stem-group clade. Such data have been supplied from fossils of which the soft parts have been preserved in exceptional detail. A new brachiopod, Kutorgina chengjiangensis
sp. nov., from the Early Cambrian Chengjiang Lagerstatte
of southern China, is described here. It is the first articulated brachiopod species collected from this deposit. The
specimens preserve a set of soft-body parts, i.e. lophophore,
digestive tract and pedicle, all previously poorly known in
almost all Palaeozoic calcareous brachiopod taxa. The loph-

Key words: Early Cambrian, Chengjiang Lagerstatte, brachiopoda, lophophore, digestive tract, pedicle, soft-tissue
preservation.

Although only minor members in present-day marine communities, brachiopods have an extensive fossil
record, exhibiting morphological diversity and geological
continuity that reflect their dominance in the marine benthos throughout the Palaeozoic era. Recent molecular
studies suggest that the Phoronida should be assigned to
the phylum Brachiopoda as a shell-less subphylum or
class (Cohen 2000; Cohen and Weydmann 2005), but it is
now generally argued that the Brachiopoda comprise
three subphyla: Linguliformea, Craniiformea and Rhynchonelliformea. The Rhynchonelliformea comprise five
classes, of which only the Rhynchonellata unquestionably
have living relatives. Calcareous-shelled brachiopods,
known since the Early Cambrian, soon became the largest
group, dominant since Late Cambrian times. Nevertheless,
fossils of this particular lineage are known almost exclusively from their shells. Consequently, anatomical knowl-

edge of extinct taxa relies heavily on analogies with their

extant relatives; yet these analogies have been untested
conjectures as regards stem-group clades (Sutton et al.
2005). Information regarding these clades has been
obtained recently from the fossil record, notably from
those deposits with exceptional preservation of soft parts
(Zhang, Z. F. et al. 2003, 2004a, b, 2005, 2006, 2007a, b;
Zhang X. G. et al. 2003; Sutton et al. 2005; Holmer and
Caron 2006).
Now perhaps surpassing in fame the classic Middle
Cambrian Burgess Shale (Briggs et al. 1994), the Chengjiang Lagerstatte is an exceptional mudstone deposit
acclaimed for yielding one of the earliest, most abundant
and diverse faunas of soft-bodied organisms in the Phanerozoic (Shu et al. 2001, 2003, 2004, 2006; Hou et al.
2004). It preserves details of soft tissues in brachiopods
with fine fidelity. The deposit yields an abundant variety

The Palaeontological Association

doi: 10.1111/j.1475-4983.2007.00725.x

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PALAEONTOLOGY, VOLUME 50

of inarticulated brachiopods, often with fine preservation

of soft parts, notably lophophores, digestive tracts and
mantle canal system, which are very rarely fossilized elsewhere. However in this Lagerstatte, rhynchonelliformean
brachiopods are sparse, numerically overshadowed by
their linguliformean cousins. Consequently, to date the
rhynchonelliformeans in these Early Cambrian mud
deposits have not been described.
Continuing excavations near Kunming, Yunnan (Textfig. 1AB), in south-western China have led to the
discovery of many specimens of rhynchonelliformean
brachiopods. The specimens are referred to Kutorgina and
described as Kutorgina chengjiangensis sp. nov., based on
the outline and morphology of the valves. As compared
with the other kutorginate brachiopods of similar age
without preserved soft parts from Greenland, Russia,
Kazakhstan and Australia (Rowell 1977; Popov and
Tikhonov 1990; Popov 1992; Popov et al. 1997; Popov
and Williams 2000; Skovsted and Holmer 2005), our
specimens show soft tissues, including pedicle, mantle
canals, lophophore and digestive tract, as well as a marginal setal fringe. Although soft parts in Silurian articulated brachiopods from the Herefordshire (UK)
Konservat-Lagerstatte have been reported recently (Sutton
et al. 2005), no records of soft parts in Cambrian
rhynchonelliformean brachiopods have been described

previously. Thus, the c. 520525 Ma fossils provide evidence about the state of anatomical characters of the
rhynchonelliformean stock of brachiopods, a first step in
elucidating the radiation of brachiopods during the Cambrian explosion and the evolution of their functional
morphology.

MATERIAL AND PRESERVATION

The majority of the specimens were recovered from Jianshan Hill at Haikou (Text-fig. 1AB), where the hitherto
earliest-known agnathan Haikouichthys (Shu et al. 2003)
and a variety of remarkable body plans of deuterostomes,
including vetulicolians (Shu et al. 2001) and vetulocystids
(Shu et al. 2004), as well as the most recently reported
Early Cambrian vendobionts (Shu et al. 2006) have also
been discovered. Ten specimens of the brachiopod were
collected in the Shankoucun Section at Anning, about
30 km south-west of Kunming, Yunnan, and eight specimens in the Erjie section near Meishucun (Text-fig. 1A),
where a candidate section for the global stratotype of the
Precambrian Cambrian boundary was proposed (Luo
et al. 1984).
The strata containing these fossils belong to the Yuanshan Member (Eoredlichia-Wudingaspis Zone), i.e. the

A, map of the Kunming area, showing the localities where the Early Cambrian brachiopod Kutorgina chengjiangensis
sp. nov. was collected. B, stratigraphy of the Early Cambrian of the Jianshan section at Haikou, showing the stratigraphic level of the
brachiopods described here.

TEXT-FIG. 1.

ZHANG ET AL.: RHYNCHONELLIFORMEAN BRACHIOPODS WITH SOFT-TISSUE PRESERVATION

upper part of the Early Cambrian Heilinpu (formerly

Qiongzhusi) Formation (Text-fig. 1B), exposed in a wide
area around Kunming (Luo et al. 1999). The deposits,
commonly regarded as late Atdabanian in age (Qian and
Bengtson 1989; Bengtson et al. 1990; Zhu et al. 2001a),
are considered to have accumulated in proximal offshore
to lower shoreface environments disturbed by episodic
storm events (Zhu et al. 2001b; Hu 2005). So far, more
than 60 specimens of Kutorgina chengjiangensis have been
collected from those localities by the work-team of the
Early Life Institute (ELI) and are deposited in the ELI,
Northwest University, Xian, China (designated ELI
BK-001 to BK-062; part and counterparts indicated by
suffixes A and B). Among them are 25 with more or less
well-preserved pedicle remains (Text-figs 2AC, G, 3AF,
4DH, 5AC); six with partial or paired lophophoral
imprints (Text-figs 2AH, 5AD), which in a few cases
have a little relief and marginal setae (Text-fig. 4AC);
and five specimens have an exceptionally preserved digestive tract, dorsally curved, with a putative dorso-terminal
anus located near the proximal end of a pedicle (Textfigs 2C, FI, 3CE).
Specimens of K. chengjiangensis commonly occur as
dorsoventrally flattened moulds of valves (Text-figs 13),
but the quality of the preservation of shells that have been
replicated by clay minerals varies greatly. Soft-tissue preservation indicates that many of the complete shells represent carcasses buried alive, rather than accumulated
valves. In many cases, they appear to be preserved as
compressed composite dorsal ventral moulds (Textfigs 2AC, G, 3AG, 4AH, 5AC, E). When removing
the flattened dorsal valve, the ventral valve can be
revealed (Text-fig. 4DF). In specimen ELI BK-038A, the
dorsal and ventral valves are more or less displaced owing
to some factors of preservation (Text-figs 2B, E, 5C). In a
few cases, the lateral profile of a shell can be observed
(Text-fig. 4J). In specimen ELI BK-037A, B, the anterior
part of the shell has been distinctly compressed (Textfig. 4I). Intriguingly, when a mudstone containing the
fossil brachiopod is cleaved, the split is usually along the
layering plane that the dorsal valve surface dictates (Textfigs 12, 4AF). This may be due to differences in the
degree of convexity of dorsal and ventral valves; it is
always stronger in the dorsal valve (Text-fig. 4J). This
greater convexity allows the dorsal valve to be preserved
pressed into the finely laminated bedding planes, thereby
increasing the potential for the emergence of this valve
when the mudstone is split open.
Finer details of shell morphology, such as micro-ornamentation, are not preserved in the available specimens
(Text-fig. 4DL), probably because of the relatively coarse
replication of the shells by clay minerals. Internal
characters, such as the disposition of the lophophore
(Text-figs 2AH, 4AC, 5AD), the mantle canal system

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(Text-figs 3FG, 5E) and the pedicle (Text-figs 2AC, G,

3AF, 4DH, 5) are, however, well preserved. It is worthy
of note that the pedicles of K. chengjiangensis do not
extend parallel to the bedding plane but commonly bend
downward into the sediment (Text-figs 2AC, G, 3AF,
4DH, 5AC, E). This arrangement could indicate in situ
burial of the brachiopods in their original life position.
As most of the pedicles were only partly visible after
crackout (Text-fig. 2AC, G, 3AF, 5AC), mechanical
preparation with fine needles and small brushes was necessary. The lophophores of K. chengjiangensis are visible
either directly (Text-fig. 4AB), as a result of cleavage
approximately along the commissural plane, or as paired
spiral impressions seen through the compressed dorsal valve as a result of post-depositional flattening
(Text-figs 2AH, 5AD). The alimentary canals are also
preserved as reddish-brown impressions on the internal
moulds of dorsal valves (Text-figs 2C, FI, 3CE, 5B).
The preservation of the setal fringe (Text-figs 3FG, 5E)
is weaker than those seen in Cambrian lingulid taxa
(Zhang, Z. F. et al. 2005, 2006).

SYSTEMATIC PALAEONTOLOGY
Subphylum RHYNCHONELLIFORMEA Williams, Carlson,
Brunton, Holmer and Popov, 1996
Class KUTORGINATA Williams, Carlson, Brunton, Holmer and
Popov, 1996
Superfamily KUTOGINOIDEA Schuchert, 1893
Family KUTORGINIDAE Schuchert, 1893
Genus KUTORGINA Billings, 1861

Type species. Kutorgina cingulata Billings, 1861, from the Lower

Cambrian of Labrador, Canada.

Diagnosis. See Popov et al. 1997, p. 346.

Kutorgina chengjiangensis sp. nov.

Text-figures 25

Derivation of name. After the Chengjiang Lagerstatte, Yunnan

Province, southern China, and implies soft-tissue preservation.
Holotype and occurrence. ELI BK-042 (Text-figs 2A, 5A), from
the Yuanshan Member (Eoredlichia-Wudingaspis Zone), Early
Cambrian Heilinpu Formation, Yunnan, southern China.

Diagnosis. Shell strongly dorsibiconvex, suboval or transversely oval in outline; anterior margin rectimarginate;
surface strongly lamellose peripherally, no visible prominent micro-ornamentation; ventral valve with a possible

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PALAEONTOLOGY, VOLUME 50

apical foramen; dorsal valve with straight posterior

margin and a moderate median fold developed anteriorly
from mid-valve. Ventral interarea apsacline, dorsal interarea narrow; dorsal lateral mantle canal pinnate, and dorsal vascula media bifurcate at midline; muscle scars

poorly impressed; lophophore a simple spiral lacking any

support structures. Pedicle stout and elongate, with a centric coelomic cavity. Digestive tract composed of a
mouth, oesophagus, enlarged stomach, intestine and a
dorsoterminal functional anus.

D
F

Kutorgina chengjiangensis sp. nov. from the Chengjiang Lagerstatte, South China, showing lophophore imprints (single
arrows) and digestive tract (tailed arrows). Scale bars represent 5 mm. A, D, holotype, ELI BK-042. A, general view of the holotype
showing the lophophore imprints and the visceral region and pedicle (see also Text-fig. 5A). D, enlargement of the lophophore and
visceral region. B, E, ELI BK-038A, laterally distorted specimen with conjoined and displaced valves. B, general view; note the
proximal lophophore imprints and the proximal pedicle (see also Text-fig. 5C). E, close-up view of the lophophore. C, F, ELI BK-001.
C, flattened specimen affected by lateral compression; note the imprints of paired brachial arms and digestive canal (see also Textfig. 5B). F, details of the lophophore and gut. GH, ELI BK-002A, flattened dorsal internal mould, showing the impression of the
alimentary canal and ?lophophore. G, general (see also Text-fig. 5D), and H, enlarged views. I, ELI BK-003A, flattened dorsal internal
mould, showing the remnants of the alimentary canal.

TEXT-FIG. 2.

ZHANG ET AL.: RHYNCHONELLIFORMEAN BRACHIOPODS WITH SOFT-TISSUE PRESERVATION

different specimen. The ratio of shell length to width ranges

from 072 to 097 (average 084; see Dimensions below). Dorsal
valve strongly convex with the maximum height at mid valve;
ventral valve moderately convex with the highest point at about
posterior quarter of the valve length (Text-fig. 4IJ). From the
three-dimensional preservation of the ventral valve (Text-fig. 4I)

Description
Shell. Shell dorsobiconvex and subelliptical to subquadrate in
outline; the maximum length is 15 mm and the maximum width
of 17 mm occurs at about the anterior third of shell length in a

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T E X T - F I G . 3 . Kutorgina chengjiangensis sp. nov. from the Chengjiang Lagerstatte, South China, showing the pedicle (black arrows),
putative pedicle cavity (white arrows), mantle canals (double-headed arrows) and possible dorsal-terminal anal openings (tailed arrows).
Scale bars represent 5 mm. A, ELI BK-010, flattened specimen; note the pedicle extending downwards. B, ELI BK-051A, dorsal exterior
with pedicle preserved and its presumed cavity replicated by pyrite. C, ELI BK-037B, crushed dorsal internal mould with a threedimensional pedicle and linear lumen (white arrow); note the darkish scar of an anal opening. DE, ELI BK-037A. D, general, and E,
enlarged views of an anal opening and pedicle lumen (white arrow). FG, ELI BK-036. F, general view of a flattened specimen with a
flattened elongate pedicle, showing the dorsal vascula (see also Text-fig. 5E). G, close-up view of the mantle canals in F.

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PALAEONTOLOGY, VOLUME 50

it seems likely that it bears a supra-apical opening. Ornament of

shells consists of high concentric growth lamellae spaced c. 06
08 mm apart medially; they are strongly developed on the dorsal valves (Text-fig. 4DF) and usually weaker on the ventral
valves (Text-fig. 4GJ). No radial ornamentation has been
observed (Text-fig. 4KL).
Ventral interarea apsacline and slightly elevated from the valve
floor, with a broadly triangular, convex pseudodeltidium (Textfigs 2AC, 5AC). Dorsal interarea comparatively small with a
straight hinge line (Text-figs 2AC, G, 3AD, 5AD). Dorsal
and ventral interareas appear as flattened triangular imprints in
strongly compressed shells (Text-fig. 4DF). Dorsal hinge furrows are two distinct, obliquely orientated, striped imprints on
the inner side of the interarea bounded by the hinge line (Textfig. 4E).
Pedicle. Pedicle protrudes between delthyrium and notothyrium
and is always preserved as a flattened impression, usually bent
steeply into the sediments (Text-figs 2AC, G, 3AF, 4DH, 5).
It arises from the posterior margin of the shell, continues as a
stalk of constant diameter, is ornamented with transverse
grooved annulations, and terminates in a flattened annulated
disc. Distally the pedicle does not bear any of the rootlet-like
structures seen in many Recent articulates, and no other shell
has been found to have anchorage as in Chengjiang lingulids
(Zhang, Z. F. et al. 2006, 2007a). The maximum length of the
pedicle is c. 13 mm, up to c. 31 mm in diameter in specimen
ELI BK-037A, B (Text-fig. 4I). It appears to be much more
robust than that of the Chengjiang lingulids (Jin et al. 1993;
Zhang, Z. F. et al. 2005, 2006, 2007a, b). Its surface in some
specimens shows pronounced concentric annular discs disposed
at intervals of 0610 mm. That this robust kutorginid pedicle
was filled by connective tissue is uncertain, but it contains a
putative coelomic cavity. This is suggested by a median darkish
lineation (Text-fig. 3CE), which is here interpreted as a coelomic lumen akin to the pedicle cavity seen in the fossil lingulids
from the Chengjiang Lagerstatte. In specimen ELI BK-051A, this
pedicle cavity seems to be preserved as a yellowish-brown pyrite
string, extending some 5 mm posterior to the posterior shell
margin (Text-fig. 3B).
Visceral region and digestive tract. The visceral cavity appears in
several specimens (Text-figs 2AI, 5A) as a reddish-brown,
recessed, pyriform imprint on the internal mould of the dorsal
valve in a posteromedian position; it extends anteriorly over
one-third of the valve length. The complete alimentary canal of
K. chengjiangensis is revealed in Text-figure 2, and is completely
shown in Text-figure 5B, D. The mouth is presumed to be
located at the base of the lophophore. A posterodorsally extending strand is interpreted as the oesophagus (Text-fig. 5B), an
enlarged, dark-stained pouch represents the stomach, a narrow
intestine is impressed as a dark red strand, and a putative dorsoposterior anus represented by a circular scar is located near the
proximal end of the pedicle (Text-figs 2C, FI, 3CE).
Lophophore. The preservation of the lophophore varies among
the specimens. The imprints of the paired brachial (lophophoral)
arms in specimen ELI BK-042 run anterolaterally from the ante-

rior of the median visceral area and bend inward (Text-fig. 5A)
symmetrically to the midline; this disposition has been observed
in many specimens (Text-figs 2AH, 4AC, 5AD). In specimen
ELI BK-016A-B, the lophophore appears three-dimensionally
preserved inside the valve (Text-fig. 4AC). As seen in Text-figure 2C, F, the brachial arms leave a pair of asymmetrical impressions with a faint colour contrast on the flattened dorsal valve as
a result of laterally compressed preservation of the shell valves
(Text-figs 2C, 5B). In addition, some specimens show only the
proximal part of paired brachial imprints on a specimen that is
strongly obliquely compressed (Text-figs 2B, E, 5C). The apparent flexibility shown by these paired imprints (Text-figs 2C, F,
5B) in the fossil state, and their less intricately spiralled configuration (Text-figs 2A, 4A, 5A) demonstrate that they are most
likely allied with brachial arms rather than any type of lophophore support structures. The simple coiling of brachial imprints
indicates that the lophophore of K. chengjiangensis has attained
an early spirolophe development stage.
Although tentacles on a Cambrian lingulid lophophore are
known from the Chengjiang deposits (Zhang X. G. et al. 2003;
Zhang, Z. F. et al. 2004a, b, 2005), such structures cannot be
confidently demonstrated in the available specimens. Continuing
investigation of further material from these deposits may yield
information bearing on this issue.
Mantle canals. The mantle canals of fossil brachiopods are commonly preserved as grooves and ridges more or less symmetrically disposed on either side of the longitudinal midline of the
valves. The dorsal mantle canals of K. chengjiangensis are preserved as reddish-brown impressions on the internal mould of
the dorsal valve (Text-fig. 3FG). On the left side of one laterally
compressed specimen (Text-figs 3FG, 5E), three linear impressions arise from the anterior body wall at an anterolateral position, while on the right side they are weakly visible, presumably
congruent with those on the left. The dorsal vascula media
appears to be bifurcate. No information on the ventral mantle
canals is detectable in our specimens.
Setae. Setae are a characteristic feature of all brachiopods. In
the group, they show significant differences in length and
width, as well as in their arrangement along the margin. All
described Chengjiang lingulids bear setae. The poorly preserved
setae of K. chengjiangensis are preserved as reddish linear
impressions; they are spaced equidistantly, and radiate outward
from the mantle margin with lengths of up to 17 mm
(Text-fig. 4AC).
Dimensions (in mm)

Valve length
Valve width
L W ratio

Max
15
17
097

Min
644
522
072

N
15
19
15

Mean
97
1112
084

SD
238
269
0082

Remarks. The Kutorginidae is one of the most common

components of Cambrian calcareous-shelled brachiopod

ZHANG ET AL.: RHYNCHONELLIFORMEAN BRACHIOPODS WITH SOFT-TISSUE PRESERVATION

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Kutorgina chengjiangensis sp. nov. from the Chengjiang Lagerstatte, South China: note that the proximal pedicles
(tailed arrows) extend posteriorly. Scale bars represent 5 mm except for K (1 mm) and L (20 lm). A, ELI BK-016A, partial dorsal
interior, showing the brachial arm preserved in three dimensions. BC, counterpart of A. B, view, and C, close-up view of marginal
setae (single arrows). D, ELI BK-062, dorsal view of a dorsal mould with proximal part of pedicle. E, ELI BK-056A, dorsal internal
mould showing the hinge furrow. F, ELI BK-039A, dorsal external mould with proximal part of pedicle. G, ELI BK-050A, ventral view
of conjoined valves, with proximal part of pedicle. H, ELI BK-051A, an incomplete specimen with a pedicle protruding between
valves. I, ELI BK-014A, external exterior mould. J, ELI BX-027, a laterally preserved specimen showing the profile of shell valves. KL,
ELI BX-045, SEM photographs of shell surface.

TEXT-FIG. 4.

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PALAEONTOLOGY, VOLUME 50

AE, interpretative drawings of Kutorgina chengjiangensis illustrated in Text-figures 2A, 2C, 2B, 2G and 3F,
respectively. Scale bars represent 5 mm. Abbreviations: ?Ao, anal opening; Dv, dorsal valve; Dvm, ?dorsal vascula media; Dvl, dorsal
vascula lateria; Es, oesophagus; ?Fm, ?faecal material; In, intestine; Lo, lophophore; St, stomach; Pe, pedicle; Vc, visceral cavity; Vv,
ventral valve.

TEXT-FIG. 5.

faunas. The strong concentric growth lamellae and putative foramen in the fossils dealt with herein suggest that
the organism is probably affiliated to the kutorginide brachiopods. Furthermore, species of Kutorgina are usually
very variable in their morphology (Popov et al. 1997);
thus, we refer these fossils provisionally to this genus.
Kutorgina chengjiangensis differs from the other four
described species of the genus in its relatively large size,
in having a much more strongly convex dorsal valve and
a moderately developed ventral valve, as well as in terms
of a lack of any discernible micro-ornamentation on the
shell surface. In contrast, the four previously described
species have a strongly convex ventral valve and a moderately developed dorsal valve with fine micro-ornamentation. K. reticulata was first described by Poulsen (1932,
p. 29) from the Ella Island Formation of north-east
Greenland. It is distinguished from the other species of
the genus by the supposedly unique micro-ornamentation
of hexagonal pustules. K. cingulata Billings, 1861 is similar to K. catenata Koneva, 1979 from the Lower Cambrian
of Kazakhstan and Kirgizia in having a granular microornamentation (Popov et al. 1997), but is distinguished
from it in having a ventral sulcus, a well-defined notothyrial platform, and strongly developed ridges bounding the
inner sides of the grooves in the dorsal pseudointerarea.
The fourth species is K. perugata Walcott, 1905 (Walcott
1912; Rowell 1977). Its valves are ornamented with minute rhomboid granules. In addition, Trematosia undulata
(Cooper, 1976), from the Early Cambrian Nimra Formation of southern Negev, Israel, was also considered to
have an affinity with Kutorgina because of its lamellose
shell, minute apical foramen, broadly triangular, convex
pseudodeltidium and poorly defined propareas on an
apsacline ventral interarea (Popov et al. 1997).

DISCUSSION AND COMPARISON

Although lophophores are known from Cambrian linguliformean and Silurian articulated brachiopods, we present

here the first detailed description of the lophophores of

Cambrian articulated brachiopods. Intriguingly, K. chengjiangensis has a relatively large mantle cavity and a small
visceral cavity, whilst the brachial arms discussed here are
less intricately coiled or spiraled, and occupy a little of
the mantle cavity. The simple spirals of the lophophores
perhaps indicate that the feeding currents they produced
were relatively weaker and perhaps less effective in providing for gas exchange. Thus, it is a prerequisite that
Cambrian brachiopods possessed a relatively larger mantle
space for gas exchange than extant forms, as the transport
of oxygen in brachiopods into the body tissues takes place
predominantly through the epithelia of the lophophore
and mantle lobe (Williams et al. 1997). In addition, the
Cambrian atmospheric environmental oxygen concentration was rather lower, approximately 15 per cent of current O2 levels (Holland 1994). Therefore, the higher ratio
of the mantle cavity to body cavity of Early Cambrian
brachiopods appears to be reasonable for oxygen demand.
In this respect, the calcareous-shelled brachiopod is similar to its coeval lingulid cousins (Zhang, Z. F. et al.
2004a, 2005, 2006, 2007a, b), probably reflecting similar
environmental constraints.
It is clear that K. chengjiangensis bears no trace of any
skeletal lophophore support. The coiled lophophore corresponds to an early spirolophe developmental stage. Therefore, it is assumed that the lophophores of Cambrian
kutorginids were supported by a hydrostatic skeleton as in
Recent lingulides. This lophophore shows significant similarities with those of CambrianRecent lingulids (Emig
1992; Zhang X. G. et al. 2003; Zhang, Z. F. et al. 2004a) in
both a comparable configuration that comprises a pair of
spirals arranged symmetrically about a midline, and in the
absence of any skeletal support. These similarities support
the view that lophophores in phosphatic- and calcareousshelled brachiopods are homologous. The finding of the
lophophore in calcareous-shelled brachiopods, in conjunction with the description of Cambrian lophophores in
various lingulid taxa (Zhang X. G. et al. 2003; Zhang, Z. F.
et al. 2004a, b, 2005, 2006, 2007a, b) demonstrate that an

ZHANG ET AL.: RHYNCHONELLIFORMEAN BRACHIOPODS WITH SOFT-TISSUE PRESERVATION

early spirolophe has been the most common lophophore

configuration since the onset of Cambrian times. The
lophophores of Cambrian lingulids, e.g. Lingulella chengjiangensis and Lingulellotreta malongensis (Zhang, Z. F.
et al. 2004a, b, 2005), include trocholophes, schizolophes
and the less intricately coiled spirolophes. This development of lophophores is mirrored in the ontogeny of
Recent lingulids. Thus, the early stages of spirolophous
lophophore ontogeny and development appear to be
plesiomorphic characters inherited from an ancestral form.
The trocholophe-schizolophe-early spirolophe development of the lophophore has been universal throughout
the history of the phylum (Emig 1992; Zhang, Z. F. et al.
2004b). The spirolophe is the final stage of development
among the Linguliformea and the Craniiformea, while in
the Rhynchonelliformea, three stages have evolved from
the schizolophe stage, respectively: the spirolophe, the
more efficient plectolophe (Rudwick 1970; Emig 1992)
and the lobate ptycholophe (Rudwick 1970; Grant 1972).
In brachiopods the presence or absence of an anus was
formerly taken to be a difference of the highest importance, differentiating inarticulate from articulate brachiopods. Although, as discussed above, alimentary canals
are known from Cambrian linguliformean brachiopods,
there is no direct fossil evidence that a digestive tract was
present in articulate stocks. The only putative fossil
evidence from rhynchonelliformean brachiopods was
deduced from the silicified kutorginid Nisusia sulcata of
the Middle Cambrian of the Marjum Limestone of western Utah, USA. Because of some silicified, sausage-like
objects protruding posteriorly through the gap between
shell valves of Nisusia sulcata (Rowell and Caruso 1985;
Popov and Williams 2000), which were misinterpreted as
faecal material or coprolites, Rowell and Caruso (1985)
concluded that Nisusia possessed a functional anus. However, these sausage-like objects bore markedly transverse
grooves on their surface, and the maximum observed
length was up to 6 mm (Rowell and Caruso 1985; Cohen
et al. 2003). Their gross form and the way they emerged
from between the delthyrium and notothyrium suggest
that they represent pedicles. Indeed, Cohen et al. (2003)
postulated that the sausage-like structures identified as
faecal material could represent a pedicle, and this is corroborated by the finding of the pedicle in the material
described here. The pedicle of K. chengjiangensis has a
general resemblance to the sausage-like, transversely
grooved projections illustrated by Rowell and Caruso
(1985). Therefore, fossil evidence bearing on an opening
digestive tract at an anus in articulate stocks no longer
appears to be tenable.
The fossils described here provide the oldest direct evidence of the disposition of the digestive tract in carbonate-shelled brachiopods. In K. chengjiangensis it is
undoubtedly directed posteriorly from a mouth within

1399

the lophophore, and is presumed to terminate in a functional anus located near the proximal end of the pedicle.
Although the possibility of a blind ending may not be
completely eliminated because of the location of the end
of the intestine in the fossils, it is obvious that there is a
circular scar on the internal mould of the dorsal valve
and ferruginous matter scattered along the posterior dorsal margin. In addition, the imprint of the digestive canal
with a low relief unequivocally terminates at a darkish
rounded opening situated anterior to the posterior valve
margin. The weight of evidence reviewed above leads us
to reject the possibility of a blind-ending intestine, and
conversely argues for the existence of a dorsoposterior
anus in kutorgindes, as in Recent craniids.
All extant rhynchonelliformean taxa have been
described with a blind-ending intestine. Consequently, the
occurrence of an anus in kutorginids allows us to state
that in the Brachiopoda this is a plesiomorphic character
inherited from an ancestral group common to both linguliformean and craniiformean taxa, all of which have a
functional anus; the organization of the alimentary canal
of linguliformean brachiopods is known from the Cambrian. Thus, the blind intestine among the Rhynchonelliformea must be regarded as an apomorphic evolutionary
novelty.
The Kutorginidae and Nisusiidae, being alike in possessing an extremely primitive articulation that lacks teeth
(Popov and Tikhonov 1990; Popov et al. 1997), were considered to be related and thus to belong to the same
order, Kutorginida. Studies of the articulation of Kutorgina and Nisusia (Rowell and Caruso 1985; Popov and
Tikhonov 1990) suggested that kutorginids may represent
one of the most primitive types of articulate brachiopods
(Popov et al. 1997). The distinctive features of the
kutorginate stocks are the possession of a large convex
pseudodeltidium and the presence of a minute supra-apical foramen. The traditional view is that this supra-apical
opening is the pedicle foramen, an aperture for the egress
of the pedicle. However, the fossils figured here demonstrate that K. chengjiangensis has a massive, stout pedicle
to provide a reliable anchor. Nevertheless, it is difficult to
imagine such a massive pedicle could emerge through
such a minute supra-apical opening that was well illustrated in the type species Kutorgina cingulata (see Popov
et al. 1997; pl. 1, figs 112). Therefore, we conclude that
the small supra-apical opening was not the aperture for
pedicle egress in kutorginates. This conclusion is consistent with silicified three-dimensional specimens of Nisusia
from the Middle Cambrian of western Utah (Rowell and
Caruso 1985; Popov and Williams 2000) in which the
silicified pedicles, originally misinterpreted as faecal material (see above), distinctly protruded posteriorly through
the gap defined by the notothyrium and the dorsal surface of the pesudodeltidium (see Rowell and Caruso 1985,

1400

PALAEONTOLOGY, VOLUME 50

figs 5, 6, 8.1, 9.4, 9.68, 9.7, 9.11). Furthermore, the

small, supra-apical opening was evidently recognizable in
the western Utah material. The cases reviewed above
therefore argue against the traditional view that the
supra-apical opening is the pedicle foramen. Crucial in
this respect is how to interpret and understand the function of the minute apical opening in the kutorginate lineages. It is probably difficulties in reconstructing this
function that led Rowell and Caruso (1985, p. 1234) to
reject the identification of the sausage-like projection in
their material as the pedicle. One possibility is that this
opening may represent a rudiment of a hydrodynamic
shell-opening mechanism (Popov 1992).
Almost all brachiopods are attached to the substratum
by a pedicle, but the pedicles of articulated and inarticulated brachiopods differ in structure, function and embryonic origin (Williams et al. 1997). The pedicle of
inarticulated brachiopods develops as an outgrowth of the
posterior body wall and is associated only with the ventral
valve, whereas the pedicle of articulated brachiopods is
correlated with the body wall of both valves because their
pedicle rudiment is continuous with the mantle rudiment
that produces both the ventral and the dorsal valves. It is
not at all clear how this difference should be interpreted
phylogenetically. When compared with pedicles of Cambrian lingulids (Jin et al. 1993; Zhang, Z. F. et al. 2005,
2006, 2007a; Holmer and Caron 2006), the pedicle of K.
chengjiangensis is markedly stout and stiff, possibly filled
with connective tissue and containing a clomic cavity;
thus it is rather similar to those of Recent lingulides (Williams et al. 1997). Although some pedicles in extant
rhynchonellate brachiopods are as robust as that of
K. chengjiangensis, they are shorter (Richardson 2000).
Many of them bear holdfast papillae with distal rootlets
that are absent in K. chengjiangensis. By contrast, the pedicle of the Cambrian species is relatively larger, lacks distal rootlets and has a median clomic cavity. Although it
was not possible to determine the presence or not of the
pedicle lumen in other fossil articulates (Sutton et al.
2005) the pedicle of K. chengjiangensis resembles that of
Silurian articulated brachiopods in gross morphology and
surface ornamentation with concentric laminae or subtransverse ridges. The similarities in the configuration of
the lophophore, the digestive tract and pedicle anatomy
in the Cambrian rhynchonelliformean brachiopods to that
of the linguliformean branch give additional support for
the monophyly of the Brachiopoda (Hyman 1959; Rowell
1982; Emig 1997), which has been corroborated recently
from molecular perspectives (see Cohen et al. 1998; Passamaneck and Halanych 2006).
Acknowledgements. This work was supported by the National
Natural Science Foundation of China (Grant 40332016 and
40602003), National Basic Research Programme of China (Grant

2006CB806401), the Program for Changjiang Scholars and Innovative Research Team in University (PCSIRT), and the Research
Fund for the Doctoral Program of Higher Education (to Z. F.
Zhang and J. N. Liu). Z. F. Zhang is indebted to Dr Leonid
Popov (Cardiff) for valuable discussion and advice in classification. We thank Drs S. X. Hu (Kunming), G. X. Li (Nanjing) for
technical assistance, H. X. Guo and Y. C. Yao for help with
fieldwork, J. P. Zhai, M. R. Cheng for preparation of the fossils,
and H. J. Gong for SEM photographs. We are grateful to Nestor
J. Sander (USA) for the language improvement and comments
on the earlier draft, and also thank two anonymous referees for
their critical comments, which greatly improved this paper.
Dr P. D. Lane completely redrafted the text.

REFERENCES
B E N G T S O N , S., C O N W A Y M O R R I S , S., C O O P E R , B. J.,
J E L L , P. A. and R U N N E G A R , B. N. 1990. Early Cambrian
fossils from South Australia. Memoir of the Association of Australasian Paleontologists, 9, 1364.
B I L L I N G S , E. H. 1861. On some new or little known species
of Lower Silurian fossils from the Potsdam Group (Primordial
zone). Palaeozoic fossils. Volume 1, No. 1. Canadian Geological
Survey, Dawson Brothers, Montreal, pp. 118.
B R I G G S , D. E. G., E R W I N , D. H., F R E D E R I C K , J. and
C O L L I E R , F. J. 1994. The fossils of the Burgess Shale. Smithsonian Institution Press, Washington, DC, 236 pp.
C O H E N , B. L. 2000. Monophyly of brachiopods and
phoronids, reconciliation of molecular evidence with Linnaean classification (the subphylum Phoroniformea nov.).
Proceedings of the Royal Society of London, Series B, 267, 225
231.
G A W T H R O P , A. and C A V A L I E R - S M I T H . T. 1998.
Molecular phylogeny of brachiopod and phoronids based on
nuclear-encoded small subunit ribosomal RNA gene
sequences. Proceedings of the Royal Society of London, Series B,
353, 20392061.
T E R , C. 2003. The brachiopod
H O L M E R , L. E. and L U
fold, a neglected body plan hypothesis. Palaeontology, 46,
5965.
and W E Y D M A N N . A. 2005. Molecular evidence that
phoronids are a subtaxon of brachiopods (Brachiopoda,
Phoronata) and that genetic divergence of metazoan phyla
began long before the early Cambrian. Organism, Diversity and
Evolution, 5, 253273.
C O O P E R , G. A. 1976. Lower Cambrian brachiopods from the
Rift Valley (Israel and Jordan). Journal of Paleontology, 50,
269289.
E M I G , C. C. 1992. Functional disposition of the lophophore in
living brachiopods. Lethaia, 25, 291302.
1997. Les Lophophorates constituent-ils un embranchement?
Bulletin de la Societe Zoologique de France, 122, 279288.
G R A N T , R. E. 1972. The lophophore and feeding mechanism
of the Productidina (Brachiopoda). Journal of Paleontology, 46,
213249.
H O L L A N D , H. D. 1994. Early Proterozoic atmospheric
change. 237244. In: B E N G T S O N , S. (ed.). Early life on

ZHANG ET AL.: RHYNCHONELLIFORMEAN BRACHIOPODS WITH SOFT-TISSUE PRESERVATION

Earth. Nobel Symposium no. 84. Columbia University Press,

New York, NY, 517 pp.
H O L M E R , L. E. and C A R O N , J. B. 2006. A soft-shelled spinose stem group brachiopod with pedicle from the Middle
Cambrian Burgess Shale. Acta Zoologia, 87, 273290.
M , J.,
H O U , X. G., A L D R I D G E , R. J., B E R G S T R O
S I V E T E R , DAVID J., S I V E T E R , DEREK J. and F E N G ,
X. H. 2004. The Cambrian fossils of Chengjiang, China: the flowering of early animal life. Blackwell Publishing, Oxford, 233 pp.
H U , S. X. 2005. Taphonomy and palaeoecology of the Early
Cambrian Chengjiang Biota from eastern Yunnan, China.
Berliner Palaobiologische Abhandlungen, 7, 1197.
H Y M A N , L. H. 1959. Brachiopoda. 517609. In H Y M A N ,
L. H. (eds). The invertebrates: smaller coelomate groups; Chaetognatha, Hemichordata, Pogonophora, Phoronida, Ectoprocta,
Brachiopoda, Sipunculida, the Coelomate Bilateria, 5.
MacGraw-Hill, New York, NY, 783 pp.
J I N , Y. G., H O U , X. G. and W A N G , H. Y. 1993. Lower Cambrian pediculate lingulids from Yunnan, China. Journal of
Paleontology, 67, 788798.
K O N E V A , S. P. 1979. Stenothecoids and inarticulate brachiopods
from the Lower and lower Middle Cambrian of central Kazakhstan. Nauka, Alma-Ata, 123 pp. [In Russian].
L U O , H. L., H U , S. X., C H E N , L. Z., Z H A N G , S. S. and
T A O , Y. H. 1999. Early Cambrian Chengjiang fauna from
Kunming Region, China. Yunnan Science and Technology
Press, Kunming, 129 pp. [In Chinese, English abstract].
J I A N G , Z. W., W U , X. C., S O N G , X. L., Q U , Y. L.,
X I N G , Y. S., L I U , G. Z., Z H A N G , S. S. and T A O , Y. H.
1984. Sinian-Cambrian boundary stratotype section at Meishucun, Jinning, China. Peoples Publishing House, Yunnan, 154
pp. [In Chinese, English summary].
P A S S A M A N E C K , Y. and H A L A N Y C H , K. M. 2006.
Lophotrochozoan phylogeny assessed with LSU and SSU data.
Evidence of lophophorate polyphyly. Molecular Phylogenetics
and Evolution, 40, 2028.
P O P O V , L. E. 1992. The Cambrian radiation of brachiopods.
399423. In L I P P S , J. H. and S I G N O R , P. W. (eds). Origin
and early evolution of the Metazoa. Plenum Press, New York,
NY, 570 pp.
R O W E L L , A. J. and P E E L . J. S. 1997. Early Cambrian
brachiopods from North Greenland. Palaeontology, 40, 337
354.
and T I K H O N O V , Y. A. 1990. Early Cambrian brachiopods from southern Kirgizia. Paleontologichesky Zhurnal, 3,
3346. [In Russian].
and W I L L I A M S , A. 2000. Kutorginata. H208H215. In
K A E S L E R , R. L. (ed.). Treatise on invertebrate paleontology,
Part H, Brachiopoda, vol. 2, Revised. Geological Society of
America, Boulder, CO, and University of Kansas Press, Lawrence, KS, 423 pp.
P O U L S E N , C. 1932. The Lower Cambrian faunas of East
Greenland. Meddeleser om Grnland, 87, 166.
Q I A N , Y. and B E N G T S O N , S. 1989. Palaeontology and biostratigraphy of the Early Cambrian Meishucunian Stage in
Yunnan Province, South China. Fossils and Strata, 24, 1156.
R I C H A R D S O N , J. R. 2000. Ecology of articulated brachiopods. 441471. In K A E S L E R , R. L. (ed.). Treatise on inverte-

1401

brate paleontology, Part H, Brachiopoda, vol. 1, Revised.

Brachiopoda (Introduction). Geological Society of America,
Boulder, CO, and University of Kansas Press, Lawrence, KS,
539 pp.
R O W E L L , A. J. 1977. Early Cambrian brachiopods from the
southwestern Great Basin of California and Nevada. Journal of
Paleontology, 51, 6885.
1982. The monophyletic origin of the Brachiopoda.
Lethaia, 15, 299307.
and C A R U S O , N. E. 1985. The evolutionary significance
of Nisusia sulcata, an early articulate brachiopod. Journal of
Paleontology, 59, 12271242.
R U D W I C K , M. J. S. 1970. Living and fossil brachiopods.
Hutchinson, London, 199 pp.
S C H U C H E R T , C. 1893. Classification of the Brachiopoda.
American Geologist, 11, 141167, 5 pls.
S H U , D. G., C O N W A Y M O R R I S , S., H A N , J., C H E N , L.,
Z H A N G , X. L., Z H A N G , Z. F., L I U , H. Q. and L I U , J. N.
2001. Primitive deuterostomes from the Chengjiang Lagerstatte (Lower Cambrian, China). Nature, 414, 419424.
L I , Y., Z H A N G , X. L., H U A , H., Z H A N G ,
Z. F., L I U , J. N., G U O , J. F., Y A O , Y. and Y A S U I , K.
2006. Lower Cambrian vendobionts from China and early diploblast evolution. Science, 312, 731734.
Z H A N G , Z. F. and L I U , J. N. 2004. Ancestral
echinoderms from the Chengjiang deposits of China. Nature,
430, 422428.
Y A S U I , K., J A N V I E R , P., C H E N , L.,
Z H A N G , X. L., L I U , J. N., L I , Y. and L I U , H. Q. 2003.
Head and backbone of the Early Cambrian vertebrate Haikouichthys. Nature, 421, 526529.
S K O V S T E D , C. B. and H O L M E R , L. E. 2005. Early Cambrian brachiopods from north-east Greenland. Palaeontology,
48, 325345.
S U T T O N , M. D., B R I G G S , D. E. G., S I V E T E R , DAVID J.
and S I V E T E R , DEREK J. 2005. Silurian brachiopods with
soft-tissue preservation. Nature, 436, 10131015.
W A L C O T T , C. D. 1905. Cambrian Brachiopoda with descriptions of new genera and species. United States National
Museum, Proceedings, 25, 669695.
1912. Cambrian Brachiopoda. Monograph of the United
States Geological Survey, 51 (two volumes), 872 pp., 104 pls.
W I L L I A M S , A., C A R L S O N , S. J., B R U N T O N , C. H. C.,
H O L M E R , L. E. and P O P O V , L. E. 1996. A supra-ordinal
classification of the Brachiopoda. Philosophical Transactions of
the Royal Society of London, Series B, 351, 11711193.
J A M E S , M., E M I G , C. C., M A C K A Y , S. and
R H O D E S , M. C. 1997. Anatomy. 7188. In K A E S L E R ,
R. L. (ed.). Treatise on invertebrate paleontology, Part H,
Brachiopoda, vol. 1. Revised. Brachiopoda. Geological Society of
America, Boulder, CO, and University of Kansas Press,
Lawrence, KS, 539 pp.
Z H A N G , X. G., H O U , X. G. and E M I G , C. C. 2003. Evidence of lophophore diversity in Early Cambrian Brachiopoda.
Proceedings of the Royal Society of London, Series B, 270, S65
S68.
Z H A N G , Z. F., H A N , J., Z H A N G , X. L., L I U , J. N. and
S H U , D. G. 2003. Pediculate brachiopod Diandongia pista

1402

PALAEONTOLOGY, VOLUME 50

from the Lower Cambrian of South China. Acta Geologica

Sinica. (English Edition), 77, 288293.
2004a. Soft tissue preservation in the
Lower Cambrian linguloid brachiopod from South China.
Acta Palaeontologica Polonica, 49, 259266.
S H U , D. G., H A N , J. and L I U , J. N. 2004b. New data
on the lophophore anatomy of Early Cambrian linguloids
from the Chengjiang Lagerstatte, southwest China. Carnets de
Geologie Notebooks on Geology, Cg2004_L04, 17.
2005. Morpho-anatomical differences of the
Early Cambrian Chengjiang and Recent lingulids and their
implications. Acta Zoologia, 86, 277288.
2006. New data on the rare Chengjiang
(Lower Cambrian, South China) linguloid brachiopod Xianshanella haikouensis. Journal of Paleontology, 80, 203211.

2007a. A gregarious lingulid brachiopod

Longtancunella chengjiangensis from the Lower Cambrian,
South China. Lethaia, 40, 1118.
H A N , J., Z H A N G , X. L., L I U , J. N., S H U , D. G. and
G U O , J. 2007b. Note on the gut preserved in the Lower Cambrian Lingulellotreta (Lingulata, Brachiopoda) from South
China. Acta Zoologica, 88, 6570.
Z H U , M. Y., L I , G. X., Z H A N G , J. M., S T E I N E R , M.,
Q I A N , Y. and J I A N G , Z. W. 2001a. Early Cambrian stratigraphy of east Yunnan, southwestern China. A synthesis. Acta
Palaeontologica Sinica, 40 (Supplement), 439.
Z H A N G , J. M. and L I , G. X. 2001b. Sedimentary environments of the Early Cambrian Chengjiang biota. Sedimentology
of the Yuanshan Formation in Chengjiang County, eastern
Yunnan. Acta Palaeontologica Sinica, 40 (Supplement), 80105.