rhynchonelliformean brachiopods with soft-tissue...

RHYNCHONELLIFORMEAN BRACHIOPODS WITH

SOFT-TISSUE PRESERVATION FROM THE EARLY

CAMBRIAN CHENGJIANG LAGERSTATTE OF SOUTH

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, Xi’an 710069, China; e-mail: [email protected] or, [email protected]

�Centre d’Oceanologie de Marseille, Rue de la Batterie-des-Lions, 13007 Marseille, France

�College of Earth Science and Land Resources, Chang’an University, Xi’an 710054, China

Typescript received 13 July 2006; accepted in revised form 30 November 2006

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 fos-

sils of which the soft parts have been preserved in excep-

tional detail. A new brachiopod, Kutorgina chengjiangensis

sp. nov., from the Early Cambrian Chengjiang Lagerstatte

of southern China, is described here. It is the first articu-

lated 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-

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 cœlomic 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.

Key words: Early Cambrian, Chengjiang Lagerstatte, bra-

chiopoda, lophophore, digestive tract, pedicle, soft-tissue

preservation.

Although only minor members in present-day mar-

ine communities, brachiopods have an extensive fossil

record, exhibiting morphological diversity and geological

continuity that reflect their dominance in the marine ben-

thos 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 Rhyn-

chonelliformea. 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 exclu-

sively 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 Cheng-

jiang Lagerstatte is an exceptional mudstone deposit

acclaimed for yielding one of the earliest, most abundant

and diverse faunas of soft-bodied organisms in the Phan-

erozoic (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

[Palaeontology, Vol. 50, Part 6, 2007, pp. 1391–1402]

ª The Palaeontological Association doi: 10.1111/j.1475-4983.2007.00725.x 1391

of inarticulated brachiopods, often with fine preservation

of soft parts, notably lophophores, digestive tracts and

mantle canal system, which are very rarely fossilized else-

where. 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 (Text-

fig. 1A–B), 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 mar-

ginal setal fringe. Although soft parts in Silurian articu-

lated 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. 520–525 Ma fossils provide evi-

dence about the state of anatomical characters of the

rhynchonelliformean stock of brachiopods, a first step in

elucidating the radiation of brachiopods during the Cam-

brian explosion and the evolution of their functional

morphology.

MATERIAL AND PRESERVATION

The majority of the specimens were recovered from Jian-

shan Hill at Haikou (Text-fig. 1A–B), 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 speci-

mens 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 Yu’an-

shan Member (Eoredlichia-Wudingaspis Zone), i.e. the

A B

TEXT -F IG . 1 . 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.

1392 P A L A E O N T O L O G Y , V O L U M E 5 0

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, Xi’an, 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 2A–C, G, 3A–F,

4D–H, 5A–C); six with partial or paired lophophoral

imprints (Text-figs 2A–H, 5A–D), which in a few cases

have a little relief and marginal setae (Text-fig. 4A–C);

and five specimens have an exceptionally preserved diges-

tive tract, dorsally curved, with a putative dorso-terminal

anus located near the proximal end of a pedicle (Text-

figs 2C, F–I, 3C–E).

Specimens of K. chengjiangensis commonly occur as

dorsoventrally flattened moulds of valves (Text-figs 1–3),

but the quality of the preservation of shells that have been

replicated by clay minerals varies greatly. Soft-tissue pres-

ervation indicates that many of the complete shells repre-

sent carcasses buried alive, rather than accumulated

valves. In many cases, they appear to be preserved as

compressed composite dorsal ⁄ ventral moulds (Text-

figs 2A–C, G, 3A–G, 4A–H, 5A–C, E). When removing

the flattened dorsal valve, the ventral valve can be

revealed (Text-fig. 4D–F). 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 (Text-

fig. 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 (Text-

figs 1–2, 4A–F). 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-orna-

mentation, are not preserved in the available specimens

(Text-fig. 4D–L), probably because of the relatively coarse

replication of the shells by clay minerals. Internal

characters, such as the disposition of the lophophore

(Text-figs 2A–H, 4A–C, 5A–D), the mantle canal system

(Text-figs 3F–G, 5E) and the pedicle (Text-figs 2A–C, G,

3A–F, 4D–H, 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 2A–C, G, 3A–F,

4D–H, 5A–C, 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. 2A–C, G, 3A–F, 5A–C), mechanical

preparation with fine needles and small brushes was nec-

essary. The lophophores of K. chengjiangensis are visible

either directly (Text-fig. 4A–B), as a result of cleavage

approximately along the commissural plane, or as paired

spiral impressions seen through the compressed dor-

sal valve as a result of post-depositional flattening

(Text-figs 2A–H, 5A–D). The alimentary canals are also

preserved as reddish-brown impressions on the internal

moulds of dorsal valves (Text-figs 2C, F–I, 3C–E, 5B).

The preservation of the setal fringe (Text-figs 3F–G, 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 2–5

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 Yu’anshan Member (Eoredlichia-Wudingaspis Zone), Early

Cambrian Heilinpu Formation, Yunnan, southern China.

Diagnosis. Shell strongly dorsibiconvex, suboval or trans-

versely oval in outline; anterior margin rectimarginate;

surface strongly lamellose peripherally, no visible promi-

nent micro-ornamentation; ventral valve with a possible

Z H A N G E T A L . : R H Y N C H O N E L L I F O R M E A N B R A C H I O P O D S W I T H S O F T - T I S S U E P R E S E R V A T I O N 1393

apical foramen; dorsal valve with straight posterior

margin and a moderate median fold developed anteriorly

from mid-valve. Ventral interarea apsacline, dorsal inter-

area narrow; dorsal lateral mantle canal pinnate, and dor-

sal vascula media bifurcate at midline; muscle scars

poorly impressed; lophophore a simple spiral lacking any

support structures. Pedicle stout and elongate, with a cen-

tric coelomic cavity. Digestive tract composed of a

mouth, oesophagus, enlarged stomach, intestine and a

dorsoterminal functional anus.

A B C

D

G H I

E

F

TEXT -F IG . 2 . 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 Text-

fig. 5B). F, details of the lophophore and gut. G–H, 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.


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

different specimen. The ratio of shell length to width ranges

from 0Æ72 to 0Æ97 (average 0Æ84; 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. 4I–J). From the

three-dimensional preservation of the ventral valve (Text-fig. 4I)

A B C D

G

F E

TEXT -F IG . 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 three-

dimensional pedicle and linear lumen (white arrow); note the darkish scar of an anal opening. D–E, ELI BK-037A. D, general, and E,

enlarged views of an anal opening and pedicle lumen (white arrow). F–G, 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.


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

shells consists of high concentric growth lamellae spaced c. 0Æ6–

0Æ8 mm apart medially; they are strongly developed on the dor-

sal valves (Text-fig. 4D–F) and usually weaker on the ventral

valves (Text-fig. 4G–J). No radial ornamentation has been

observed (Text-fig. 4K–L).

Ventral interarea apsacline and slightly elevated from the valve

floor, with a broadly triangular, convex pseudodeltidium (Text-

figs 2A–C, 5A–C). Dorsal interarea comparatively small with a

straight hinge line (Text-figs 2A–C, G, 3A–D, 5A–D). Dorsal

and ventral interareas appear as flattened triangular imprints in

strongly compressed shells (Text-fig. 4D–F). Dorsal hinge fur-

rows are two distinct, obliquely orientated, striped imprints on

the inner side of the interarea bounded by the hinge line (Text-

fig. 4E).

Pedicle. Pedicle protrudes between delthyrium and notothyrium

and is always preserved as a flattened impression, usually bent

steeply into the sediments (Text-figs 2A–C, G, 3A–F, 4D–H, 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. 3Æ1 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 0Æ6–1Æ0 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. 3C–E), which is here interpreted as a coelo-

mic 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 2A–I, 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 extend-

ing 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 dorso-

posterior anus represented by a circular scar is located near the

proximal end of the pedicle (Text-figs 2C, F–I, 3C–E).

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 2A–H, 4A–C, 5A–D). In specimen

ELI BK-016A-B, the lophophore appears three-dimensionally

preserved inside the valve (Text-fig. 4A–C). As seen in Text-fig-

ure 2C, F, the brachial arms leave a pair of asymmetrical impres-

sions 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 appar-

ent flexibility shown by these paired imprints (Text-figs 2C, F,

5B) in the fossil state, and their less intricately spiralled configu-

ration (Text-figs 2A, 4A, 5A) demonstrate that they are most

likely allied with brachial arms rather than any type of lopho-

phore 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 com-

monly preserved as grooves and ridges more or less symmetri-

cally disposed on either side of the longitudinal midline of the

valves. The dorsal mantle canals of K. chengjiangensis are pre-

served as reddish-brown impressions on the internal mould of

the dorsal valve (Text-fig. 3F–G). On the left side of one laterally

compressed specimen (Text-figs 3F–G, 5E), three linear impres-

sions arise from the anterior body wall at an anterolateral posi-

tion, 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 1Æ7 mm

(Text-fig. 4A–C).

Dimensions (in mm)

Max Min N Mean SD

Valve length 15 6Æ44 15 9Æ7 2Æ38

Valve width 17 5Æ22 19 11Æ12 2Æ69

L ⁄ W ratio 0Æ97 0Æ72 15 0Æ84 0Æ082

Remarks. The Kutorginidae is one of the most common

components of Cambrian calcareous-shelled brachiopod


A B C

D

G

J K L

H I

E F

TEXT -F IG . 4 . 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 (¼1 mm) and L (¼20 lm). A, ELI BK-016A, partial dorsal

interior, showing the brachial arm preserved in three dimensions. B–C, 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. K–L,

ELI BX-045, SEM photographs of shell surface.


faunas. The strong concentric growth lamellae and puta-

tive foramen in the fossils dealt with herein suggest that

the organism is probably affiliated to the kutorginide bra-

chiopods. 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 moder-

ately developed dorsal valve with fine micro-ornamenta-

tion. 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 simi-

lar to K. catenata Koneva, 1979 from the Lower Cambrian

of Kazakhstan and Kirgizia in having a granular micro-

ornamentation (Popov et al. 1997), but is distinguished

from it in having a ventral sulcus, a well-defined notothy-

rial 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 min-

ute rhomboid granules. In addition, Trematosia undulata

(Cooper, 1976), from the Early Cambrian Nimra Forma-

tion 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 linguli-

formean and Silurian articulated brachiopods, we present

here the first detailed description of the lophophores of

Cambrian articulated brachiopods. Intriguingly, K. cheng-

jiangensis 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 pro-

viding 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 concentra-

tion was rather lower, approximately 15 per cent of cur-

rent 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 simi-

lar 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 corre-

sponds to an early spirolophe developmental stage. There-

fore, it is assumed that the lophophores of Cambrian

kutorginids were supported by a hydrostatic skeleton as in

Recent lingulides. This lophophore shows significant simi-

larities with those of Cambrian–Recent 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 calcareous-

shelled brachiopods are homologous. The finding of the

lophophore in calcareous-shelled brachiopods, in conjunc-

tion 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

A B C D E

TEXT -F IG . 5 . A–E, 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.


early spirolophe has been the most common lophophore

configuration since the onset of Cambrian times. The

lophophores of Cambrian lingulids, e.g. Lingulella cheng-

jiangensis and Lingulellotreta malongensis (Zhang, Z. F.

et al. 2004a, b, 2005), include trocholophes, schizolophes

and the less intricately coiled spirolophes. This develop-

ment 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 develop-

ment 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 impor-

tance, differentiating ‘inarticulate’ from ‘articulate’ bra-

chiopods. 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 wes-

tern 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. How-

ever, 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 cor-

roborated 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 evi-

dence of the disposition of the digestive tract in carbon-

ate-shelled brachiopods. In K. chengjiangensis it is

undoubtedly directed posteriorly from a mouth within

the lophophore, and is presumed to terminate in a func-

tional 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 dor-

sal 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 lin-

guliformean and craniiformean taxa, all of which have a

functional anus; the organization of the alimentary canal

of linguliformean brachiopods is known from the Cam-

brian. Thus, the blind intestine among the Rhynchonelli-

formea must be regarded as an apomorphic evolutionary

novelty.

The Kutorginidae and Nisusiidae, being alike in pos-

sessing an extremely primitive articulation that lacks teeth

(Popov and Tikhonov 1990; Popov et al. 1997), were con-

sidered to be related and thus to belong to the same

order, Kutorginida. Studies of the articulation of Kutor-

gina 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-api-

cal 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 demon-

strate 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 illus-

trated in the type species Kutorgina cingulata (see Popov

et al. 1997; pl. 1, figs 1–12). Therefore, we conclude that

the small supra-apical opening was not the aperture for

pedicle egress in kutorginates. This conclusion is consis-

tent 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 mate-

rial (see above), distinctly protruded posteriorly through

the gap defined by the notothyrium and the dorsal sur-

face of the pesudodeltidium (see Rowell and Caruso 1985,


figs 5, 6, 8.1, 9.4, 9.6–8, 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 func-

tion of the minute apical opening in the kutorginate lin-

eages. 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 inarticu-

lated brachiopods differ in structure, function and embry-

onic 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 Cam-

brian 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 cœlomic cavity;

thus it is rather similar to those of Recent lingulides (Wil-

liams 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 ped-

icle of the Cambrian species is relatively larger, lacks dis-

tal rootlets and has a median cœlomic 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 sub-

transverse 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; Pass-

amaneck 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 Inno-

vative 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 classifica-

tion. 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.

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