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A possible larval roundworm from the Cambrian ‘Orsten’ and
its bearing on the phylogeny of Cycloneuralia
ANDREAS MAAS, DIETER WALOSZEK, JOACHIM T. HAUG &
KLAUS J. MÜLLER
ROUNDWORMS (= Nemathelminthes sensu Ax
2003) are a taxon of bottom-living animals with
a exible cuticle and a sac-like to elongate body.
The taxon comprises a set of morphologically
diverse taxa including minute interstitial taxa
such as gastrotrichs and kinorhynchs, elongate to
extremely slim worms including the nematomorphs
(horse-hair worms) and nematodes, the priapulids,
as well as the loriciferans (Ahlrichs 1995;
Ax 2003). In traditional systems, the Rotifera
and Acanthocephala are also included within
Nemathelminthes (= Aschelminthes), which
are closely related to Plathelminthes (Ahlrichs
1995). Yet, because neither the systematics
within the Nemathelminthes, nor composition of
its taxa has been entirely claried or generally
accepted, it is not surprising that, likewise, no
consensus has been reached on the systematic
position of the Nemathelminthes within the entire
Bilateria. The most signicant and encompassing
morphological features of the Nemathelminthes
are the cuticle and muscular pharynx (Ax 2003).
Excepting their putative sister taxon Gastrotricha,
all other Nemathelminthes (Neuhaus 1994,
1997; Lemburg 1999; Ax 2003) share a ring-
shaped nerve mass (circum-pharyngeal brain,
MAAS, A., WALOSZEK, D., HAUG, J.T. & MÜLLER, K.J., 2007:12:21. A possible larval
roundworm from the Cambrian ‘Orsten’ and its bearing on the phylogeny of Cycloneuralia.
Memoirs of the Association of Australasian Palaeontologists 34, 499-519. ISSN 0810-8889.
Herein, we describe a 145 µm long, three-dimensionally preserved fossil from Middle Cambrian
rocks collected in 1986 in the Duchess Embayment, Queensland, Australia. The new, possibly
immature form is formally named Shergoldana australiensis gen. et sp. nov. It shares features
with minute taxa among the Recent Nemathelminthes, such as the gastrotrichs and kinorhynchs
and to the larval stages of certain cycloneuralians such as nematomorphs and priapulids.There
are similarities in body tagmosis as well as structural details. The tubular annulated anterior part
of the body of S. australiensis resembles, for example, that of extant nematomorph larvae, with
the difference that the accordion-like annulated region of the fossil is somewhat irregular. In
nematomorph larvae this region can be contracted but not intruded, which is also assumed to be
so for the fossil. A comparable region exists in the scalidophoran cycloneuralian kinorhynchs,
priapulids and loriciferans, but which can be extruded and intruded. The annulated part, called
the neck, is short. Other similarities of S. australiensis with cycloneuralians concern a ring of
structures located around the frontal opening, the presumed mouth area, possibly representing a
pharyngeal armature consisting of inwardly pointing tooth-like outgrowths. Backwardly pointing
spines on plates on the region behind the annulations resemble structures found on different
parts of the body of priapulids. At least some shared features may represent plesiomorphies with
regard to the ground pattern of Nemathelminthes, such as the bifurcated tail end. Shergoldana
australiensis is presented here as possibly the rst record of a free-living immature cycloneuralian
from the Cambrian, even if it remains uncertain whether it has closer afnities to the one or
other in-group. The new data provided by S. australiensis are expected to enlighten further the
systematic status of the various macroscopic, 2D- and 3D-preserved Cambrian fossils previously
described as roundworms or even priapulids, including the slim, but cm long, palaeoscolecids
and the embryonic Markuelia sp., both co-occurring with S. australiensis.
Andreas Maas (andreas.maas@uni-ulm.de), Dieter Waloszek & Joachim T. Haug, Biosystematic
Documentation, University of Ulm, Helmholtzstrasse 20, D-89081 Ulm, Germany; Klaus J.
Müller, Palaeontological Institute, University of Bonn, Nussallee 8, D-53115 Bonn, Germany.
Received 12 November 2007.
Keywords: Scanning electron microscopy, phylogeny, tagmosis, homologies, phylogenetic
systematics, larvae, 3D reconstructions.
AAP Memoir 34 (2007)
500
the feature leading Ahlrichs (1995) to propose
the name Cycloneuralia for this group) around
the oesophagus, their cuticle contains β-chitin,
is layered and moulted from time to time. There
is no evidence of a ring-shaped anterior nerve
mass in Gastrotricha (e.g., Schmidt-Rhaesa et
al. 1998; Schmidt-Rhaesa 2002), but such has
been postulated for Gastrotricha by Nielsen
(1995, 2001), which led him to use the name
Cycloneuralia instead of Nemathelminthes.
CONFLICTING HYPOTHESES
A layered, chitinous cuticle and moulting are
also features of Arthropoda, which is the major
argument for the hypothesis that arthropods
represent the sister group of the Cycloneuralia
within a taxon Ecdysozoa (e.g., Aguinaldo et al.
1997; Schmidt-Rhaesa et al. 1998; Garey 2001,
2003; Budd 2003 – though some have proposed
only an arthropod-nematode relationship,
see, e.g., Eernisse et al. 1992; Manuël et al.
2000). Proponents of this hypothesis interpret
Gastrotricha, if they discuss them, either as
the sister group of Ecdysozoa or the sister
group of Cycloneuralia. Others, mainly making
inferences from molecular studies, deny any
relationships of gastrotrichs to ecdysozoans/
cycloneuralians at all (e.g., Todaro et al. 2006).
It is beyond the scope of this paper to discuss
the validity of the Ecdysozoa hypothesis in
detail, but any placement of Arthropoda within
the traditional Nemathelminthes, or afliation
of Arthropoda with any of the nemathelminth
subtaxa has, of course, a strong bearing on the
position of Gastrotricha and the ground pattern
of Cycloneuralia.
Another uncertainty concerns the situation within
the Cycloneuralia. One view is that Cycloneuralia
consist of two sister taxa, the Scalidophora,
embracing Kinorhyncha and Vinctiplicata (=
Priapulida + Loricifera), and the Nematoida,
with Nematoda and Nematomorpha as sister
taxa (e.g., Lemburg 1999; Ax 2003). Nematoida
lack, autapomorphically, ring musculature in their
subepidermal muscle layer (a basal character
of Bilateria and retained in Nemathelminthes
and Cycloneuralia) and also protonephridia
(another basal character of Bilateria and retained
in Nemathelminthes and Cycloneuralia), but
possess, instead, inwardly oriented epidermal
ridges or cords (“Seitenleisten”). Yet, the two
taxa, nematomorphs and nematodes, are quite
distinctive morphologically and ecologically. For
example, adult nematomorphs do not feed and lack
a developed digestive system and consequently
lack structures for food intake, but their larvae
bear a toothed, expansible frontal structure called
a proboscis (e.g., Schmidt-Rhaesa 1998; Nielsen
2001). Remarkably, Malakhov (1980) included
nematomorphs and scalidophorans within a taxon
Cephalorhyncha, but set off nematodes completely
from the entire cycloneuralians, not mentioning
any shared features between nematodes and
other cycloneuralians (see also Malakhov 1994;
Malakhov & Adrianov 1995). Besides the features
mentioned, shared between nematomorphs and
nematodes, the latter do possess early larvae
and seem to lack the characteristic features of
Cycloneuralia, particularly chitin within the
cuticle and a tooth-bearing anterior pharynx
region. However, both features have been proven
to exist in Nematoda, either very locally (chitin
in the pharynx region, cf. Neuhaus et al. 1997)
or in some (basal?) taxa (pharynx, cf. Lorenzen
1985; Nielsen 1995, 2001). This may indicate
that a tooth-bearing anterior pharynx region was
already present in the cycloneuralian ground
pattern, and there is no foundation for a dismissal
of nematodes from the nemathelminths.
NEMATHELMINTH FOSSIL RECORD
Despite the general softness of nemathelminth
bodies, they have a remarkably good fossil record.
Surprisingly, the record is almost exclusively from
the Cambrian (Conway Morris 1985) besides some
much younger discoveries in early Cretaceous
(120 Million years; e.g., Poinar et al. 2005) to
Cenozoic amber (e.g., Weitschat & Wichard 2002)
and the newly discovered nematodes in the early
Devonian Rhynie Chert from Scotland (Kerp et
al. 2007). The rst fossil putative scalidophoran
described was the 10 cm long Ottoia prolica
Walcott, 1912, from the Burgess Shale in Canada,
approximately 510 million years old (Conway
Morris 1977), occasionally preserved even with
shells of its favourite food, hyolithids, in the gut
(Chen et al. 2007, g. 4). More cycloneuralians
were recovered subsequently from the famous
Chengjiang biota in China, some of them
occurring in huge quantities (reviews in, e.g., Hou
et al. 2004; Huang et al. 2006). However, besides
the general body form and aspects of armature
with pharyngeal teeth and spines behind, much
of the anatomy of the fossils remains uncertain
because of their two-dimensional and rather
coarse preservation. Since many of the current
hypotheses raised around the systematics of
Nemathelminthes/Cycloneuralia have been based
largely on ultrastructural features, attempts to
establish closer afnities of the fossil taxa with
in-groups (Huang et al. 2004a, b, 2006; Hou et al.
2006) are unsubstantiated (Maas et al. 2007).
Lower Cambrian to Lower Ordovician
limestones have yielded minute three-dimensional
arthropod fossils, preserved as a result of
phosphate impregnation of their cuticle aiding in
AAP Memoir 34 (2007) 501
an extremely ne replication of the body surface,
with details down to less than 1 micrometer. These
fossils allow a completely new view of ancient
marine life. Their exceptional preservation is
called ‘Orsten’-type preservation because of its
discovery in limestone nodules from Sweden
(summary in Maas et al. 2006). Subsequent
enclosure within a limestone matrix protected
the fossils from any diagenetic compaction. The
only drawback is that such fossils are, at least
so far, size-limited: No specimen, complete or
fragmentary, larger than a millimetre has been
found.
Besides arthropods, other metazoan fossils also
in a similar type of phosphatic preservation – not
necessarily from limestones but from phosphate
rock (requiring different processing techniques)
– have been discovered subsequently. One group
are the embryonic cleavage stages of uncertain
metazoans, now also known from Precambrian
rocks (e.g., Xiao et al. 1998). The second group
comprises cycloneuralians. Late embryos within
the egg case and unrolled, about 2 mm in length,
described as species of Markuelia Valkov, 1984,
represent the rst ‘Orsten’-type cycloneuralian
described so far (e.g., Dong et al. 2004; Donoghue
et al. 2006a, b). Two specimens of Markuelia have
been discovered also in Middle Cambrian material
collected by one of us (DW) in 1986 in Australia in
the Duchess Embayment, therefore co-occurring
with the specimen described here. Several results
from this eldwork have already been published
in the early 1990s, i.e., on palaeoscolecid
cycloneuralians with preserved cuticular remains
(Müller & Hinz-Schallreuter 1993), another group
of nemathelminths interesting in this respect,
on arthropod remains with preserved soft parts
(Walossek et al. 1993), and on problematic fossils
(Müller & Hinz 1992).
NEW DATA ON FOSSIL
NEMATHELMINTHS
This article is a further report on material reported
initially by Müller & Hinz (1992) and Walossek
et al. (1993) from the Duchess Embayment
of Australia, and again on cycloneuralian
nemathelminth fossils. We are happy to dedicate
the paper and the new fossil we present herein,
to the late John Shergold. John was not only
well known for his immense work on agnostid
euarthropods, the geology of Australia, as well
as phosphate deposits, but was also Dieter
Waloszek’s companion during eldwork in the
Duchess Embayment in 1986, and he was the
rst to make us consider that agnostids might be
more closely related to crustaceans than to the
trilobites.
The new fossil is considerably much smaller
than an unrolled embryo of Markuelia. Its
different morphology and apparent free-living
nature readily demonstrate it cannot be simply a
younger Markuelia stage. Yet, its design clearly
points to cycloneuralian relationships, as also
proposed for Markuelia (Dong et al. 2004).
Based on SEM work, the best established tool
for documenting ‘Orsten’ material, the specimen
is described here as a new fossil cycloneuralian,
most likely a juvenile. Accordingly, it represents
not only a further record of Cycloneuralia in
the Cambrian, but also the first free-living
immature stage of a cycloneuralian ever found
in the early fossil record. Due to its exceptional
preservation, this single specimen provides
important details for direct comparisons with
extant representatives, showing significant
similarities particularly to nematomorph larvae
(e.g., Bohall et al. 1997; Malakhov & Adrianov
1995). These data will, in future, be applied to a
wider comparison of macroscopic 2D-preserved
Cambrian cycloneuralians – often described
as priapulids – and the minute 3D-preserved
Markuelia.
MATERIAL AND METHODS
Material. The single specimen of Shergoldana
australiensis gen. et sp. nov. (type specimen
CPC 23065) is from a collection of phosphatised
fossils extracted from ne-grained limestone. The
limestones had been collected in 1986 on a eld
trip by one of the authors (DW) together with
Raimond Below, Cologne, at the eastern edge
of the Georgina Basin, Queensland, Australia.
The locality (type locality, sample 7323) is in
the Monastery Creek Formation of the Duchess
Embayment, approximately 1 km north of Mt.
Murray (coordinates E 139° 58’ 27.6” S 21° 48’
50.4”, see Müller & Hinz-Schallreuter 1993 for
details and stratigraphical data). The age has
been determined to be late Templetonian (Middle
Cambrian).
Processing. The specimen was etched from the
rock and processed using the method described
by Müller (1990) for the ‘Orsten’-type fossil
material. Initial scanning was undertaken in the
Palaeontological Institute in Bonn. Scanning
of images illustrated herein was done with a
Zeiss DSM 962 at the Zentrale Einrichtung
Elektronenmikroskopie, University of Ulm. The
specimen was mounted on its presumed left side.
Any attempt to release it from the surface of the
stub would have caused its destruction or loss, and,
hence, this side had to be reconstructed. Further
computer-aided image processing was made using
ADOBE Photoshop CS™, GIMP 2.2 (freely
available software) and ADOBE Illustrator™.
AAP Memoir 34 (2007)
502
Some images are fusion products of two images
of the same area but with a different focus.
For image-fusion the freely available software
CombineZM was used. Schematic line drawings
and phylograms were done in ADOBE Illustrator
and Inkscape (freely available software).
Preservation, orientation. The 145 µm long
specimen of Shergoldana australiensis gen. et
sp. nov. is nearly complete and only very slightly
deformed. Cuticular preservation is comparable
to that of other Australian material described
(Walossek et al. 1993), but is slightly coarser than
that of the majority of discoveries from Sweden,
e.g., as compared to the similarly sized type-
A-larvae of Swedish ‘Orsten’ material (Müller
& Walossek 1986a). We regard the truncate
annulated region of the specimen as being anterior
and the bid end being posterior. The position
of the paired terminal outgrowths is regarded as
ventral. It seems that the front end was softer than
the rest of the body and its margin is slightly rolled
into the presumed mouth, preventing a better view
into the mouth area/pharynx. Not all of the ridges
of the annular region are equally well preserved,
some are eroded distally, therefore appearing to be
open. Folds around spine-bearing plates indicate
slight shrinkage of the cuticle in this area, while
the plates are somewhat stiffer. On the cuticle,
various spines or setae and microhairs (diameter
< 1 µm) were developed, but in most cases broken
off distal to their insertions. Two setae or spines
arose from the bid tail end but likewise have
been broken off distally. Yet the diameter of the
preserved remains point to their prominence – this
is a feature of many ‘Orsten’ fossils, which helps
in reconstructing the number and size of setae and
setules with a certain degree of condence. The
specimen is slightly bent into an S-shape (see Fig.
1). The size of the fossil indicates it is an early
juvenile, but since some of the cycloneuralians
are extremely small as adults, this must be left
unresolved (see discussion below).
Terminology. Most of the terminology used
has been adopted from that currently in use for
cycloneuralians. However, there are problems,
specifically concerning the term ‘introvert’.
The anterior body region of cycloneuralians
(only the larvae of nematomorphs; adults do not
feed, so lack any of the anterior features) shows
spine-like structures and can be withdrawn.
Some authors term this the ‘introvert’, regarding
it as a homologous body region throughout or
within cycloneuralians and, hence, they use
it as an apomorphy (Nielsen 1995; Ax 2003).
Nematomorph larvae have two systems of
longitudinal musculature. The main part of the
anterior half of the body, termed praeseptum in
nematomorph terminology (Müller et al. 2004),
is a region with strong folds; the accordion-like
region. Oblique muscles cause retraction of the
accordion-like region, which leads to eversion of
the spine-bearing region (this only being termed
the introvert) and the mouth cone or proboscis.
Proboscideal muscles cause retraction of introvert
and proboscis, which is accompanied by the
eversion of the accordion-like region (see Müller
et al. 2004, g. 1B). In Scalidophora, which lack
an accordion-like region, the spine-bearing region
termed the introvert is withdrawn by shortening
of longitudinal musculature. Its eversion occurs
by relocation of body uids. Due to two different
functional systems in nematomorphs and
scalidophorans, the original function of the
‘introvert’ of Cycloneuralia is unclear. Structural
differences between nematomorph larval spines
and scalidophoran introvert spines (see Schmidt-
Rhaesa 1998) do not support homology between
these structures: Nematomorph larval hooks are
solid, while the introvert spines of Scalidophora
generally possess ciliary receptors (the name-
giving ‘scalids’; Higgins et al. 1993; Neuhaus
1994; Lemburg 1999). This structure requires re-
investigation and thorough comparison to clarify
the phylogenetic origin of the scalidophoran and
nematomorph ‘introverts’ and hooks (scalids).
Likewise, nematodes, some of which have been
described as being able to withdraw a spine-
bearing anterior part (Riemann 1972), should be
considered in any such investigation.
Reconstructions. Reconstructions made of
the fossil were based on a large set of SEM
micrographs taken of the single specimen around
the body except for the part on which the specimen
rests. In order to get a better idea of the detailed
morphology of the specimen, and also to be able to
view the animal from all sides, we produced a 3D
model using the open source software BLENDER
(version Mac OS X 2.43).
Phylogenetic analysis and the usefulness of
ontogenies. For our phylogenetic analysis,
we strictly apply the method of phylogenetic
systematics developed by Hennig (1950, 1966)
and advanced by Ax (1996), but which we
attempt to develop further, mainly to also
include palaeontological evidence, which in
our view, has not been considered sufciently
by Hennig and Ax. The main aspects of this
method are summarised here. Representatives of
a monophylum share a common ancestor called
the stem species (see also Ax 1996 for discussion
of phylogenetic systematics in general). This stem
species existed prior to the rst speciation event
AAP Memoir 34 (2007) 503
of the monophylum and gave rise to the rst set
of sister taxa. The complete set of morphological,
molecular, physiological and behavioural features
of the stem species equals the so-called ground
pattern of the monophylum. A ground pattern (the
German term Grundmuster; not ground plan!)
consists of: 1) distinguishing characters, the
autapomorphies, acquired by the stem species in
its life span; 2) characters shared with its sister
taxon, the synapomorphies; and 3) characters
retained from ancestors along the evolutionary
line of this monophylum, the plesiomorphies (the
vast majority of features). A ground pattern does
not contain any apomorphic characters of lineages
having branched off from the evolutionary lineage
toward the stem species.
Consequences of this are: 1) No features of any
unrelated taxon or autapomorphic features of any
of the descendant taxa can be part of the ground
pattern of a monophylum; 2) Autapomorphic
characters of its stem species or autapomorphies
of in-group taxa cannot be part of the ground
pattern of earlier ancestors; 3) Species are
genetically connected, directly in one ancestral
lineage, and, indirectly, through those ancestors
shared with species of branched lineages; 4)
Each species has the potential to become a stem
species of a set or more successor species; 5) For
each species – no matter if fossil or Recent – a
ground pattern with character distinctions can,
and even should, be presented – for fossil species
this can only be reconstructed. However, the
stem species is not a hypothetical ancestor but a
real species that once lived, developed, ate and
reproduced. The advantage of this strict method
is that not only autapomorphies are given for
a species, for discriminating it from other taxa
(roughly equal to a differential diagnosis in the
traditional terminology), but the plesiomorphic
characters are essential for completing the
data set and achieving a picture of the animal.
These plesiomorphies were developed in earlier
branching events forming a differentiated pattern
of older characters (autapomorphies of earlier stem
species). Accordingly, the information content
provided by the presentation of a ground pattern is
important for any further comparative systematic-
phylogenetic investigation, particularly if it also
contains the synapomorphies shared only with
the sister taxon. Consequently, this method of
characterising ground patterns is superior to any
other cladistic approach since they do not yield
ground patterns but only branching nodes based
on various statistical methods rather than on
evolution.
Another aspect is that not only the adult
morphology, i.e., the reproductive stage, is
important for the characterisation of a species but
each individual developmental stage (semaphoront
in the sense of Hennig 1966) contributes to the
character set or ground pattern of a species (so
being equally specic for each species). We,
therefore, have decided to give the new fossil a
taxonomic name with a formal morphological
description and documentation of reconstructable
features, even if we are aware of its putative
immature character.
SYSTEMATIC PALAEONTOLOGY
NEMATHELMINTHES Gegenbaur, 1859 (=
Aschelminthes Grobben, 1910)
CYCLONEURALIA Ahlrichs, 1995 (= Introverta
Nielsen, 1995)
Shergoldana australiensis gen. et sp. nov.
Holotype and horizon. Total length 140–145 µm,
possibly an early semaphoront of the species. Age:
late Templetonian (Middle Cambrian). Locality:
Monastery Creek Formation, approximately 1
km north of Mt Murray 139° 58’ 27.6’’ E, 21°
48’ 50.4’’ S, Duchess Embayment, Queensland,
Australia (sample 7323). The specimen is
housed in the Commonwealth Palaeontological
Collection of Geoscience Australia, Canberra
(Repository Number CPC 23065). It was
temporarily kept in the collection of ‘Orsten’
fossils at the Palaeontological Institute in Bonn,
Germany, under the repository no. UB W 277.
Etymology. After the late John H. Shergold,
dedicated Australian palaeontologist and leader
of the eld trip in 1986, during which the sample
was collected, and after the continent in which
the holotype has been found.
Diagnosis. Body tubular, almost circular in cross
section except tail end, which attens abruptly
caudally into a pair of conical outgrowths,
presumably each extending into a spine. Body
divided into four regions from anterior to
posterior: first region, terminal mouth area,
surrounded by two rings; inner ring with seven
soft radial folds, each forming a triangular cushion
with a medially pointing spine dipping into it;
outer ring of 18–19 shallow humps forming the
frontal margin; second region, accordion-like,
with 12–13 sharply ridged helical folds (pseudo-
annulation); third region with 12 cuticular, more
or less pentagonal plates, each bearing an oval
hump with a central, posteriorly curved spine
(primary spine) and a pair of shorter spines on
either side (secondary spines). The anterior slope
bears another, slightly crescentic row of at least
three ner spines anteriorly (tertiary spines). The
AAP Memoir 34 (2007)
504
Fig. 1. SEM micrograph of Shergoldana australiensis gen. et sp. nov., view from left side (UB W 277; total
length 145 µm; image ipped horizontally to get anterior to the left) to show the four body regions: 1, anterior
region with cushions; 2, region with sharp annulations; 3, region with three quartets of plates with spine-bearing
humps; 4, tail end continuing into two ventro-terminal spines. Short black arrows point to irregularities in the
fold system of the second body region. Abbreviations: csp, caudal spine or seta.
Fig. 2. SEM views of Shergoldana australiensis gen. et sp. nov. A, complete view of the specimen in latero-
ventral aspect (image ipped horizontally to get anterior to the left). B–C, anterior body region. B, anterior end
with an inner ring of cushion-like folds, each bearing one tooth-like structure (black arrows) nested in between
two lateral folds and pointing inwards into the central anterior opening, the presumably intruded mouth/pharynx
region (more inwardly located structures arranged in rings not detectable); white black arrows point to possibly
18–19 round humps surrounding the ring of cushions. C, magnied view of two cushions marked by the two
upper black arrows in B, image slightly twisted against B. Note the spine nested within each cushion (black
arrow). White arrows point to three of the outer humps.
AAP Memoir 34 (2007) 505
plates are arranged into four sets; two plates/
spines oppose each other; rst set in the same
axial position approximately 50° off the dorso-
ventral axis right up and left down; second set
almost 90° offset against the foregoing one; these
four seem to form one ring; subsequent two sets
arranged accordingly; plates surrounded by less
well sclerotised cuticle; fourth region drawn
out ventro-caudally into two humps, each with
one spine pointing backwards, giving the end
a bid appearance. The two posterior regions
covered irregularly with microhairs; ventrally
on the hind body some microhairs appear to be
arranged in slightly oblique rows. Annulated and
plated region makes up 80% of the entire body,
i.e., 40% each.
Description
Body shape and size. The body of the holotype is
elongate and cylindrical (circular cross section),
being slightly bent ventrally (Fig. 2A). It is clearly
subdivided into four regions, a short frontal part,
an annulated region, making up approximately
1/3 of the body, a plated region of about the same
length, and a caudal end, making up about 20%
of the entire length. The anterior end is truncated,
whereas the posterior end is drawn out into two
posteroventrally pointing cones (see Material
and Methods for orientation) that form sockets
for spines.
Frontal region. The anterior end is truncate and
bears a central depression or opening, which
we interpret as the mouth area. The frontal rim
appears soft and bears a ring of approximately
18–19 shallow, soft, circular humps that surround
an inner ring of seven triangular, cushion-like
humps (Fig. 2B-C). With its pointed end, each
cushion reaches into the frontal depression and
comprises a central fold of tooth-like appearance
resting between anking lobes and pointing into
the depression (Fig. 2B-C). It appears as if the
structure was rather pliable and that the median
fold was not fully developed morphogenetically,
therefore not being fully functional. We could
not conrm whether a further ring of similar
structures is located further inwards of the
putative mouth.
Accordion-like region. The frontal region is
followed by a cylindrical region, which is nely
annulated in an accordion-like (Fig. 3A) manner.
The sharply dened folds are approximately 5 µm
high, run around the body in a helix and mostly
terminate after one or two turns (Fig. 3B). A
new fold starts in the sharp furrow next to the
termination or the preceding fold merges into a
succeeding one. It seems as if the majority of folds
start close to the ventral side so that one counts
more folds ventrally than dorsally (13 against 12).
Accordingly, the fold system is neither regular,
consisting of ring-shaped annulations, nor does
it reect any kind of segmentation. Small knobs
occur on the crests of some of the folds, but they
are considered to be phosphatic granules due
to preservation rather than reecting original
surface structures. If reecting original structures,
they could have been faint radial wrinkles on
the accordion folds facilitating stretching and
compressing of the region.
Spine-plate region. The third, equally distinct
body region bears 12 more or less pentagonal
cuticular plates embedded within apparently
softer cuticle forming narrow membrane-like
bands connecting the plates (Figs 1, 2A, 4A-D).
The single specimen at hand is slightly collapsed
in dorso-ventral aspect, as is indicated by the
slight depression of some of the pentagonal
plates, which are sunken into the surrounding
membrane (Fig. 4D). The anterior margin of a
plate is at a right angle to the body axis, the two
Fig. 3. SEM micrograph of Shergoldana australiensis gen. et sp. nov., anterior region with radial folds followed
by the accordion-like region (images ipped horizontally to get anterior to the left respectively above). The
ring-like folds start sharply dened; some folds split after one round (white arrows), with others fade out
between the gaping valley folds (black arrows). A, lateral view. B, close-up, anterior above.
AAP Memoir 34 (2007)
506
adjacent sides diverge slightly, and posteriorly the
two remaining sides form an obtuse angle. There
are three sets of four plates from the anterior
toward the posterior, but their arrangement is
not bilaterally symmetrical, but is bisymmetrical.
The rst of three sets consists of two rows of
two plates each: the anteriormost two plates are
slightly set off from the dorso-ventral axis, so
being located right dorso-laterally and left ventro-
laterally, while the next two plates are located
left dorso-laterally and right ventro-laterally. The
arrangement of the second and third set of plates
is similar to that of the rst set (Fig. 2A; see also
Fig. 5A-B). Each plate is approximately 10-12 µm
wide and long and bears a transversely elongated
hump with a slightly convex anterior side and a
slightly concave posterior side. The posterior side
is slightly more steeply sloping than the anterior
side (Fig. 4C).
The humps taper conically into a central
‘primary’ spine pointing postero-distally
originally (Fig. 4B). Although all humps are
broken off distally in the specimen, some of the
elongations are still preserved to such a length to
allow reconstruction of at least a minimum length
for the spine (see reconstruction in Figure 6).
Additionally, a smaller ‘secondary’ spine anked
the central spine on either side also pointing
postero-distally, and three, possibly up to ve ner
‘tertiary’ spines arise from the anterior slope of
the hump (Fig. 4C, see also the reconstruction in
Fig. 6). The whole plate is covered irregularly by
ne microhairs; one distinct, slightly crescentic
row of them is located anterior of the tertiary
spines (Fig. 4D). Additional microhairs also occur
on the membranous areas. Preservation of these
microhairs ranges from tiny knoblets to lengths
of about 3-4 µm (Fig. 4C-D). Their difference
to the tertiary spines is evident from their even
diameter of about 0.5 µm, whereas the spines
Fig. 4. A, SEM micrograph of Shergoldana australiensis gen. et sp. nov., lateral view of the two posterior
regions. Note the central humps that extend into prominent postero-distally pointing primary spines (arrows).
Image ipped horizontally to get anterior to the left (also in other such views). B, close-up of the most anterior
of the spine-bearing humps marked by a white arrow in A. Base of secondary spine (ssp) well preserved,
but spine broken off distally. C, close-up of one of the pentagonal plates carrying a central oval hump with
a primary spine anked by two secondary spines on either side. Some of the microhairs are at least partly
preserved. D, microhairs covering the plated region, some still preserved to some length. Small white arrows
mark possible beginning and end of the crescentic row of microhairs in front of the humps. Abbreviations other
than in previous gures: mh, microhairs; psp, primary spine; ssp, secondary spine; tsp, tertiary spine.
AAP Memoir 34 (2007) 507
have a wider base.
Hind body. The caudal end tapers from an
approximately circular cross section to an
oval cross section at the very end, with the
ventral side remaining straight but decreasing
in dorsoventral extension. The entire posterior
region is covered with numerous microhairs,
which, at rst sight, seem to be arranged in a
spiral around the body (Fig. 5A). In detail, the
microhairs are rather irregularly arranged except
for two more distinct rows (Fig. 5A). The caudal
end terminates into two outgrowths that appear
to continue into spines, as can be deduced from
the remaining sockets (Fig. 5A). An anus could
not be observed. An almost slit-like terminal
opening on the holotype (marked by an arrow
in Fig. 5B) is considered to be a preservational
artefact (incomplete phosphatisation).
DISCUSSION
Assignment of Shergoldana australiensis to
Nemathelminthes
Preservation of S. australiensis is of the ‘Orsten’
type and very much comparable to the preservation
of various arthropods described so far (Walossek
et al. 1993; Maas et al. 2006). This implies
preservation of the cuticle alone without any
internal details left. From this we think there
is good reason to assume that S. australiensis
belongs to a cuticle-bearing group of animals,
most likely to those animals that have an
arthropod-like cuticle. If so, this restricts afnities
of S. australiensis to two taxa, arthropods and
cycloneuralian nemathelminths rather than to
any other bilaterian group – and regardless of
currently disputed hypotheses about arthropod
and cycloneuralian relationships, which cannot be
discussed here at length (for further reading see:
e.g., Aguinaldo et al. 1997; Schmidt-Rhaesa et al.
1998; Wägele & Misof 2001; Zrzavý 2001; Garey
2001, 2003; Scholtz 2003; Mallatt et al. 2004).
No obvious shared characters between S.
australiensis and arthropods have been be found
that could substantiate possible afnities with
arthropods or a particular in-group (see, e.g.,
Maas et al. 2004 and Waloszek et al. 2005 for a
discussion of early arthropod characters). Besides
other features, the major differences are the
frontal mouth with a ring of inwardly pointing
structures (Figs 2B, 6B), the backwardly pointing
spines arising from plates (Figs 4A-D, 6A-B)
and the bid tail end (Figs 5A-B, 6A-B), which
is not a basal arthropod character. Structures that
resemble the microhairs of S. australiensis occur
on various other ‘Orsten’ fossils indicating that
the microhairs may have been longer originally.
Such structures on the arthropod cuticle might
have been developed earlier than at the level of
Crustacea, but we can detect them so far only in
Labrophora (Phosphatocopina + Eucrustacea;
see Siveter et al. 2003), and here only at very
specic sites. Denticles, for example, are common
epicuticular spike-like structures on the outer
distal edge of appendages of tiny crustaceans, and
minute setulae, also epicuticular structures, occur
on the surface of the sternum, at the sides of the
labrum, on enditic surfaces (see, e.g., Maas et al.
2003, pl. 8E, 10B), or as subordinate ornaments
of setae of a diameter of 0.2 µm and lengths of
3 to more than 10 µm (e.g., on swimming setae
and on filter setae; e.g., Müller & Walossek
Fig. 5. SEM micrograph of Shergoldana australiensis gen. et sp. nov., tail end. A, ventral view displaying
the paired ventroterminal outgrowths extending into spines or setae (csp). Image ipped horizontally. The
microhairs (mh) are mostly irregularly arranged but two distinct rows can be determined, marked by white
arrows. B, view from the posterior. Part of the specimen sunken into the glue. Slit-like opening (white arrow)
may be caused by breakage rather than representing an original anal opening. Abbreviations as in previous
gures.
AAP Memoir 34 (2007)
508
1988, pl. 10, g. 11; Walossek 1993). These
are among the smallest structures preserved on
‘Orsten’ fossils. By contrast, the microhairs of S.
australiensis are about twice as thick, but this may
be a preservational artefact caused by secondary
accretion of phosphatic matter, as known from
specimens of Skaracarida (Müller & Walossek
1985, pls 7.3, 16.6).
Several characters of S. australiensis could be
detected that appear comparable, if not shared with
cycloneuralians. These are mainly those features
not developed in any arthropods (including stem
taxa such as the fossil lobopodians): the radially
arranged spine row around the mouth (Figs 2B,
6A-B), the accordion-like anterior body region
(Figs 3A-B, 6A-B; cf. that of nematomorph
larvae: Bohall et al. 1997; Müller et al. 2004) and
the cuticular plates that extend into a spine with
anking spinules (Figs 4A, 6A-B; cf. pharyngeal
spines of priapulids: Merriman 1981). The body
ending in paired structures as observed in S.
australiensis (Figs 5A, 6A-B) occurs only in
nemathelminths among the Bilateria, not only in
kinorhynch and larval loriciferan Cycloneuralia,
but also in gastrotrichs, the putative sister
group of Cycloneuralia (cf. Kristensen 2002;
Neuhaus & Higgins 2002; Schmidt-Rhaesa
2002). Also, the larvae of nematomorphs have
caudal structures (Bohall et al. 1997, g. 2).
Yet, gastrotrichs have a very soft cuticle without
chitin and with cilia underneath, and they do not
have a frontal mouth with surrounding structures.
This appears to rule out affinities between
gastrotrichs and S. australiensis but points to S.
australiensis representing, at least, a member of
the Cycloneuralia and therefore Ecdysozoa.
If so, and in the light of the terminology in use
for cycloneuralians and their larvae, the frontal
region of S. australiensis could be homologised
with the introvert/mouth area, the prominent
annulated region would best correspond to that of
nematomorph larvae. The remaining two regions
comprise the trunk of cycloneuralians, and the
post-septum of nematomorph larvae. Spine-
bearing plates are, however, a feature resembling
structures developed in a strikingly similar way
only in priapulids. Another remarkable aspect is
the presence of cushion-like structures along the
outermost ring of spines of nematomorphs that
strongly resemble those seen in S. australiensis
(Fig. 2B-C; cf. Fig. 9A). Also, the base of
the nematomorph teeth strongly resemble
those of S. australiensis, which are similarly
nested within a cushion (Fig. 2B-C). The major
difference between these two structures is the
prominent backwardly directed spine arising
from the same structure within the cushion-like
socket in Nematomorphs. This long spine of
the nematomorph larva is most likely engaged
in locomotion, functioning as an anchoring
device. Since it arises from the opposite side
to the simple spine pointing toward the mouth,
we regard this outgrowth as a spur peculiar to
nematomorph larvae. Shergoldana australiensis
possesses only the inwardly pointing tooth-like
structure. In contrast to the seven cushions of S.
australiensis, nematomorph larvae possess six
cushions, in which the spines with long posterior
spurs are nested, the ventral one being split into
two spurs. So there are actually seven spurs. If the
interpretation of the posteriorly pointing structure
as a spur is correct, the difference would involve
only the presence of a spur arising from the tooth
in nematomorph larvae and slight differences in
locomotion: S. australiensis might rather have
used its spines on plates of the third body region
for such a purpose, while those of the oral circle
of S. australiensis are little developed and may
not have been functional.
This difference in the arrangement of the body
regions between S. australiensis and any of the
cycloneuralian taxa in question makes closer
afnities to the one or other group difcult to
justify (see below). Therefore, afnities of S.
australiensis lie, in our view, at best with the
Cycloneuralia, but it seems premature to make
Fig. 6. Restoration of Shergoldana australiensis gen. et sp. nov. using the 3D computer software Blender. A,
almost lateral view. B, antero-lateral view exposing the armature supposed to surround the frontal pharyngeal
opening.
AAP Memoir 34 (2007) 509
any further statement concerning specic alliance
to the one or other taxon. Consequences of the
mixed occurrence of features in the different
cycloneuralian taxa are discussed below.
Immature status of the available specimen of
Shergoldana australiensis
Size alone is not a very reliable character
when judging the developmental state of an
animal, but it can give a hint. All larvae of those
cycloneuralian nemathelminths with such a stage
(nematomorphs, loriciferans and priapulids)
match the size of S. australiensis. Adult forms of
all subtaxa of nemathelminths, with the possible
exception of the miniaturised Loricifera, are about
1 mm in length. Hence, we can assume that the
stem species of Nemathelminthes, and also that of
Cycloneuralia, Nematoida and Scalidophora was
at least 1 mm in length – their young accordingly
being smaller. A form of only 145 µm in length
can, therefore, be most parsimoniously regarded
as immature or possibly larval.
Yet, there is further, but admittedly
indirect, evidence of the immature status of S.
australiensis:
1. Preservation: the best-preserved animals in an
‘Orsten’-type preservation are certainly larvae, for
instance the 100 µm long type-A larvae of hitherto
unknown eucrustaceans (Müller & Walossek
1986a; Walossek & Müller 1989) or 125 µm long
head larvae of phosphatocopine crustaceans, of
which the adults achieve a shield length of several
millimetres (Maas et al. 2003). Also, the other
earliest larvae of Rehbachiella kinnekullensis
Müller, 1983, Bredocaris admirabilis Müller,
1983 or Martinssonia elongata Müller &
Walossek, 1986b, are less than 190 µm long, and
larger specimens can clearly be identied as a
more advanced ontogenetic stage by increased
segment and/or limb numbers (Walossek 1993;
Müller & Walossek 1988; Müller & Walossek
1986b; Zhang et al. 2007).
2. The possible lack of an anal opening in a
well preserved fossil: In all investigated ‘Orsten’
fossils, the tissue around the anal opening is
signicantly bulged, so that the anus is always
very conspicuous (Müller & Walossek 1986b, g.
8A; see also Müller & Walossek 1988, pl. 14.1;
Walossek 1993, pls. 19.1, 22.2). Type-A-larvae,
apparently inated by yolk and having only tiny
setae on their limbs, have neither a mouth nor
an anal opening (Müller & Walossek 1986a).
In Martinssonia elongata Müller & Walossek,
1986b, the earliest two stages lack mouth and
anus, indicative of their non-feeding status. We
therefore consider the slit-like opening at the
rear of S. australiensis as preservational. The
situation in Nematomorpha, in which the adults
have a reduced digestive system and parasitic
larvae, is clearly secondary and incomparable
with regard to the ground pattern situation of
Nemathelminthes or Nematoida.
3. The embryos of Markuelia sp. (Fig. 7A)
are much more than one millimetre long when
unrolled. They are characterised by a blunt frontal
region with possibly soft spines, an annulated
Fig. 7. Examples of other Nemathelminthes. A. The fossil Markuelia sp. from the same time and area in Australia
as Shergoldana australiensis (own material); white arrows point to the fronto-marginal, posteriorly pointing
soft spines. Black arrow points to caudal spines, which are arranged in two sets on either side. B. Extant
macrodasyid gastrotrich Dactylopodola baltica (Remane, 1926) from the Isle of Sylt, Germany. Arrows point to
the paired caudal extensions. C. Extant homalorhagid kinorhynch Paracentrophyes praedictus Higgins, 1983,
from Belize. Arrows point to the paired tail end with setae (B and C, kindly provided by B. Neuhaus, Berlin).
AAP Memoir 34 (2007)
510
body and short caudal region with a paired set
of distally curved spines ventrocaudally (Fig.
7A). In light of this morphology, our fossil seems
even to be an ontogenetically younger stage than
the embryo of Markuelia – but is clearly free-
living. Likewise, this rules out the possibility
that S. australiensis represents a younger stage
of Markuelia. The Recent Gastrotricha (Fig. 7B)
and Kinorhyncha (Fig. 7C) both are extremely
small (70 to 1500 µm). Species about the same
size as S. australiensis bear many more features
indicative of their developed status, e.g., mouth,
anus and the genital opening (see Maas et al.
in press for an example of the preservation of a
genital opening in an ‘Orsten’ fossil).
Systematics within Nemathelminthes
Ax (2003), in the third volume of his series on
the phylogenetic system of multi-cellular animals,
the Metazoa, comprehensively presented a
phylogenetic hypothesis for the Nemathelminthes,
which has been based mainly on works concerning
ultrastructural observations of Ahlrichs (1995),
Ehlers et al. (1996), Schmidt-Rhaesa (1995) and
Lemburg (1995a, b, 1999). According to this
hypothesis, the Gastrotricha represent the sister
taxon to the rest of the Nemathelminthes (for
autapomorphies of Nemathelminthes and the two
sister taxa, see Ax 2003), for which Ax adopted
the name Cycloneuralia introduced by Ahlrichs
(1995). Sister taxa within the Cycloneuralia
are the Nematoida – with nematomorphs and
nematodes – and the Scalidophora – with
kinorhynchs, loriciferans and priapulids (Ax
2003). The relationships of cycloneuralian in-
group taxa proposed by the workers mentioned
above is generally followed and also used by
other workers (e.g., Petersen & Eernisse 2001;
Kristensen 2002; Dong et al. 2004, 2005), only the
character assignment to specic ground patterns
may deviate from the system proposed by Ax
(e.g., Nielsen 1995, 2001).
A signicant character of the Scalidophora are
cuticular outgrowths, called scalids (Fig. 8A),
which are hollow and enclose sensory cells (Ax
2003) – a feature impossible to check in fossils
(see below). Besides this and more (see Lemburg
1999 for details), Scalidophora are characterised
by a special anterior body region, the introvert,
which is armed with regular rings of scalids, being
oriented towards the posterior. The introvert can
be extruded and intruded and its scalids are used
as anchoring devices for locomotion. The introvert
continues anteriorly into the pharyngeal region.
The pharynx is also protractible and bears rings
of tooth-like structures arranged in a pentaradial
symmetry, but the spines are oriented towards
the mouth opening (Lemburg 1999). Between the
rings of pharyngeal teeth and introvert scalids,
there may occur rings of radially arranged papillae
(Malakhov & Adrianov 1995, e.g., g. 2.19 for a
priapulid). Teeth and scalids usually are not the
same distance from each other in one single ring.
Adrianov & Malakhov (2001a, b) emphasised the
quite complex symmetry of the arrangement of
pharyngeal teeth and scalids within these rings.
Arrangement and number of pharyngeal teeth and
introvert scalids may change during ontogeny
(Higgins & Storch 1991; Higgins et al. 1993;
Adrianov & Malakhov 2001a, b).
Inwards pointing, but triradially arranged
tooth-like structures (also called stylets) in the
mouth area (at the tip of the mouth cone) and rings
of posteriorly directed spines also occur in the
larvae of nematomorphs (Malakhov & Adrianov
1995), but there are obvious differences:
1. The appearance of these structures is quite
distinct in Nematomorpha and Scalidophora:
Nematomorph larvae have simple, cone-like
spines, whereas in scalidophoran pharynges – in
both larvae and adults – a main spine arises from a
basal plate and shows smaller anking spinules on
either side (Fig. 8B). Additionally, nematomorphs
have only three rows of spine-like structures,
while scalidophorans have seven (Kinorhyncha)
or more scalids (Vinctiplicata) (Adrianov &
Malakhov 2001a, b).
2. Another difference is how these spines are
used in the mechanism of locomotion:
a. Nematomorph larvae have longitudinal
muscles that are contracted to shorten the
accordion-like area of the so-called preseptum.
This everts the spine-bearing frontal region
(“proboscis”, “mouth cone”, see scheme in
Müller et al. 2004). Inversion of the spine-bearing
region results from relaxation of the muscles
and relocation of body uids. The spurs of the
spines of the anterior region spread out when the
proboscis moves forwards. Proboscis and spines
mainly function to penetrate the soft membranous
cuticle of the arthropod host.
b. By contrast, in Scalidophora, relocation of
body uids results in an eversion of the pharynx,
while inversion of the pharynx results from specic
longitudinal muscles that especially accomplish
this purpose. In contrast to Nematomorpha,
inversion and eversion of the introvert also
occurs by the interaction of the muscles and
relocation of body uids, but this procedure is
independent of movements of the pharynx, while
in nematomorphs this is coupled. The scalids of
the introvert function as anchoring devices for
forward movement of the animal (e.g., Hammond
1970; Huang et al. 2004a, b).
Regardless of the striking differences between
Nematomorpha and Scalidophora, Malakhov
AAP Memoir 34 (2007) 511
(1980), Adrianov & Malakhov (1995) and
Malakhov & Adrianov (1995) homologised the
entire anterior body area of nematomorph larvae,
i.e., the mouth cone and the preseptum, with
the introvert of scalidophorans. Consequently,
assuming that Nematomorpha, Priapulida,
Kinorhyncha and Loricifera share an introvert,
they proposed the name Cephalorhyncha
Malakhov, 1980, for this taxon, excluding the
nematodes. However, Ax (2003), following
Schmidt-Rhaesa (1998) and Lemburg (1999),
convincingly argued for a monophylum Nematoida
embracing Nematomorpha and Nematoda on
the basis of several autapomorphies, such as
lack of ring musculature, elongate shape, lack
of protonephridia, dorsal and ventral cords
(thickenings of the epidermis, in which the nuclei
are concentrated), sperm cell lacking a cilium and
an accessory centriole.
Nielsen (1995) excluded the Nematomorpha
from the Cephalorhyncha of Malakhov (1980) and
adopted the name Cephalorhyncha as a synonym
of Scalidophora sensu Lemburg (1995) – because
he did not want to create new names. Lorenzen
(1985) discussed nemathelminth relationships and
stressed that the nematode Kinonchulus sattleri
Riemann, 1972 shows a protractible pharynx
and an introvert-like structure with hexagonally
arranged cuticular spines in several circles
(Riemann 1972; see also Nielsen 1995), located
anterior to the three rings of head sensilla arranged
in a 6+6+4 pattern, a character autapomorphic
for Nematoda. Nielsen (1995, 2001) regarded
the cuticular spines as evidence of a protractible
introvert being retained from a common ancestor
of nematodes, nematomorphs, kinorhynchs,
loriciferans and priapulids, an assemblage, for
which Nielsen (1995) erected the name Introverta
(= Cycloneuralia of Ahlrichs 1995), but his
proposed relationships within Nemathelminthes
(called Cycloneuralia by Nielsen 2001) are
exactly the same as those of Ax (2003). The two
systems differ in the taxon names and, more
important, in the assignment of characters to the
specic ground patterns.
A recent molecular study of several ecdysozoan
taxa (Park et al. 2006; gastrotrichs were,
regrettably, not considered) based on nearly
complete 18S rRNA data resulted in some
conicts with relationships proposed earlier (cf.
Todaro et al. 2006). Apart from other problems,
priapulids showed up to be non-monophyletic
and the only loriciferan studied was very unstable
in its position in the resulting trees. The authors
concluded that the results suggest that 18S rRNA
alone is insufcient to reconstruct relationships
within Ecdysozoa.
There are also aspects which seem to have been
rather underestimated in previous studies. The
rst is the above-mentioned presence of teeth at
the tip of the mouth cone of nematomorph larvae,
which may be homologised with the pharyngeal
teeth of scalidophorans (as suggested by Adrianov
& Malakhov 1995; Malakhov & Adrianov 1995),
particularly priapulids.
The second is the functional aspect of the
“introvert” (see above), also mentioned already.
The exact locomotory mechanics has, although
extremely important in our view, never been
investigated in detail, particularly in small
cycloneuralians, such as kinorhynchs and
loriciferans or small-sized priapulids or their
larvae. Accordingly, much of the locomotion
and feeding mechanism seen in the large
epibenthic priapulids has been thought to
represent the ground pattern condition at least of
scalidophorans, and it has also been used when
judging fossil cycloneuralians (e.g., Huang et
al. 2004b). But, the musculature and associated
structures supporting locomotion point to
alternative interpretations. A third aspect is the
presence of cushions, in which the circumoral
spines are nested, observed in the specimen
presented here for S. australiensis (Fig. 2A) and
in nematomorph larvae (see below).
Shergoldana australiensis and its implications
for the phylogeny within Nemathelminthes
Availability of a stable phylogeny with a stable
assumption about character evolution within
Nemathelminthes, especially Cycloneuralia,
is essential for any positioning of new taxa,
regardless if living or fossil. The controversial
interpretations listed above, the uncertainty about
structural homologies, neglect of functional
aspects (see above), and the use of characters not
observable in fossils, makes it even more difcult
Fig. 8. Examples of surface structures in
Nemathelminthes. A, postero-distally pointing scalids
of the rst three circlets of the introvert of a Halicryptus
spinulosus larva (from Lemburg 1995b, g. 3A; by
kind permission of the author). B, pharyngeal cuticular
plate with central postero-distally pointing spine from
the second row (pentagon) of the extant priapulid
Halicryptus spinulosus (from Merriman 1981, g. 7).
Abbreviations as in previous gures.
AAP Memoir 34 (2007)
512
to assign fossil taxa to the one or another group.
The situation has not improved on account of
exciting new discoveries of Lower Cambrian
fossils (Hou et al. 2006; Huang et al. 2006),
because they are, although very complete, still too
coarsely preserved to identify those ne details
necessary for a deeper insight to phylogeny. A
further difculty is the systematic positioning of
several of these fossils to Priapulida, although
characters used to judge this are, most likely,
nothing more than plesiomorphies retained
from the scalidophoran ground pattern, which
hinders any visualisation of the true situation
within scalidophorans (see Maas et al. 2007 for
discussion).
When comparing S. australiensis and
cycloneuralian taxa in a phylogenetic perspective,
two more difculties remain to be mentioned,
1) the phylogeny of cycloneuralians is strongly
based on ultrastructural characters, which are
not available in a fossil, 2) the unclear situation
of the anterior body region, as noted above, and
3) the mixture of characters shared between S.
australiensis and the different cycloneuralian
taxa respectively in their larvae. Shergoldana
australiensis possesses a short frontal area with
inwardly pointing structures arranged in rings
(Fig. 2A), at least one as tooth-like humps, as in
various cycloneuralians, but nematomorph larvae
also have frontal structures. If the cushions and
simple tooth-like structures around the mouth
opening of S. australiensis can be homologised,
the spurs of the nematomorph larvae may be
specic modications of a simple type of an
inconspicuous tooth that draws out posteriorly
into a prominent spur. Most parsimoniously, the
simple spine as developed in the fossil represents,
possibly, a plesiomorphy. Although the short
circum-oral area is similar in S. australiensis
and nematomorphs, the seven circumoral tooth-
like structures in S. australiensis differs slightly
from the six in nematomorphs. However, this is
not quite that different because the ventral spurs
of nematomorphs are a double structure, i.e., the
basal part is posteriorly drawn out into a double
spur (Fig. 9A), so the number of spurs is actually
seven. Whether the double spur is a product of
fusion of two original, separate ventral spurs or
whether it is a specialisation of the ventral spur
cannot yet be determined.
Another similarity is the annulated region of
S. australiensis and nematomorph larvae. As in
extant larvae, it seems likely that this second
region can be contracted but not intruded also in
the fossil. The folds in the fossil have two equal-
sized slopes, while those of nematomorph larvae
are subequal: the anterior slope is shallower and
larger than the steeper posterior slope. Two more,
but likewise minor differences exist between
the annulation of these two taxa: the folds are
helical in S. australiensis while they are complete
circles in nematomorphs (Fig. 9B-C). This
Fig. 9. A, SEM of the anterior view of the larva of the nematomorph Chordodes morgani Montgomery, 1901
(re-scanned from Bohall et al. 1997, g. 2; by kind permission of Blackwell Publishers, Oxford). The arrow
points to the accordion-like region. B–D, schematic view of cycloneuralian larvae and our hypothesis about
functionally similar (= also homologous?) body regions (not to scale). B, Nematomorpha larva. C, Shergoldana
australiensis gen. et sp. nov. D, Preloricate larva of (certain?) Priapulida (see also Higgins et al. 1993). 1,
anterior region with teeth and spines (including pharynx area); 2, annulated region (neck of priapulid larvae;
1 + 2 = preseptum, of nematomorph larvae); 3, trunk; 4, tail end, conspicuous in S. australiensis, more or less
part of the trunk in nematomorph larvae, therefore 3+4 in nematomorph larvae correspond to postseptum.
Possibly the smooth tail end of nematomorph larvae with the caudal spines is equivalent to the fourth region
of S. australiensis (marked by stippled line). Abbreviations other than in previous gures: cu, cushion of outer
ring; cui, cushion of inner ring; mc, mouth cone; pht, pharyngeal tooth; spu, spur; cs, caudal spine.
AAP Memoir 34 (2007) 513
region seems to be missing in scalidophorans,
but this is only because both nematomorph
larvae and S. australiensis lack the prominent,
scalid bearing anterior region of scalidophorans
(the introvert), which in this taxon follows the
pharyngeal armature. In fact, the homologue
of the annulated region seems to be in the neck
region of scalidophorans (Fig. 9D). This short
part is similarly ornamented with rings and
surface structures in priapulids, kinorhynchs and
loriciferans, and leads to the trunk. In priapulid
loricate larvae, this neck forms a lid, which when
the entire anterior part, the introvert, is intruded
into the body, closes the lorica.
The third region with plates bearing posteriorly
pointing spines of S. australiensis seems not
to match any of the cycloneuralian adult or
larval morphologies, although posteriorly
pointing spines occur all over the trunk of
priapulids subsequent to the loricate larval
stages. Remarkably, the spines on plates with
their anking spinules of S. australiensis are
strikingly similar to the pharyngeal teeth of
priapulids, but they are positioned, in exactly
the reverse manner, i.e., pointing towards the
mouth (compare Figs 4C and 8B). By contrast,
the scalids of priapulids, are simple, curved,
postero-distally pointing spines (Fig. 8A). From
the preservation of the fossil specimen we cannot
state whether the spines were hollow or solid
originally, which would improve comparability.
Yet it may well be that all spines mentioned in
this context originate from a more simple spine
type, where scalids are no more than a modied
type of such simple spines. These spines, i.e., the
anteriorly and medially pointing spines, have the
function of grasping food or hindering its escape,
while the posteriorly pointing spines originally
had the function of being involved in locomotion
as anchoring devices. With this, scalids, as
sensory organs, are an exclusive characteristic of
Scalidophora (autapomorphy). However, if trying
to include fossil taxa, we have to depart from
such ultrastructural evidence, but use correlative
features observable on fossils. These include, for
example, the regions, the spines themselves and
also the functional aspects of the regions in the
locomotory and feeding systems.
The trunk (postseptum) of nematomorph
larvae consists of two similarly wide portions,
which differ in length. The long anterior part is
annulated but otherwise smooth, while the smooth
end piece bears two pairs of short spines ventrally
(Fig. 9A-B). The tail end of Markuelia sp. also
shows paired groups of spines, with two or three
in each group (Fig. 7A). If the set-off tail end
of S. australiensis could be compared with this,
the postseptum would equal the third and fourth
regions of S. australiensis together. Likewise, the
entire body behind the neck of priapulids would
be the same region (Fig. 9B–D).
Concerning the bid caudal end, comparable
structures to those of S. australiensis occur in
nematomorph larvae, and also in gastrotrichs and
several cycloneuralians. In many gastrotrichs,
the tail ends in paired outgrowths (Fig. 7B)
bearing several adhesive glands (Schmidt-Rhaesa
2002). Paired paddles occur in loriciferan larvae
and in kinorhynchs (Fig. 7C; Kristensen 2002;
Neuhaus & Higgins 2002). In kinorhynchs, the
outgrowths represent cuticular spines. The toes
of the Higgins larva of Loricifera may enclose
adhesive glands in benthic forms (Kristensen
2002). It is unclear whether the structures in S.
australiensis are hollow or solid, a terminal pore
of a possible gland could not be observed. The
appearance of paired terminal outgrowths among
nemathelminths could, therefore, be interpreted
as a symplesiomorphy, but it is premature to
make a statement on the original morphology. In
summary, S. australiensis shares body regions
with all Recent Nemathelminthes, and even
more with the cycloneuralians, but these body
regions have no exact correspondent in any of the
Recent taxa, hence S. australiensis has its own
arrangement (cf. Fig. 9B–D).
Two consequences can be drawn from this:
1. The term ‘introvert’ should be restricted
to the scalid-bearing region of scalidophorans
documenting a different specialisation of the
anterior body and the locomotory system, in line
with a specialisation of the pharynx region and
related shortening of the accordion-like region
(‘neck’); hence it is regarded as a complex
autapomorphy of this taxon, which also might be
useful when comparing fossil taxa in the future.
2. The name ‘Introverta’ should be abandoned
since it refers to a feature present only in
particular in-group taxa of Cycloneuralia, such
as Kinorhyncha, Loricifera and Priapulida,
included within the Scalidophora by Lemburg
(1999). ‘Introverta’ originally included also
non-scalidophoran taxa (nematodes and
nematomorphs).
With regard to the different hypotheses
presented for the phylogeny of Nemathelminthes,
the system and character evolution put forward by
Lemburg (1999) seems, according to our study, the
most convincing at present (Fig. 10). Shergoldana
australiensis cannot be assigned convincingly
to any in-group cycloneuralian taxon because
it shares no feature with one or other taxon
that are denitely synapomorphic rather than
being simply symplesiomorphic. The spine ring
around the mouth may just represent an ancient
character present already in the cycloneuralian
AAP Memoir 34 (2007)
514
ground pattern. The same may hold true for the
plates with spines on the trunk, which cannot be
scalids but may be a simpler precursor structure.
The paired terminal outgrowths are possibly
even a nemathelminth ground pattern character.
Therefore, it seems to be equally possible that
S. australiensis represents the sister taxon to
Cycloneuralia (1 in Fig. 10), or the sister taxon
to each of its two daughter taxa (2 and 3 in Fig.
10). In any case, due to the mix of characters and
body regions of S. australiensis compared with
Recent Cycloneuralia, S. australiensis cannot
serve easily as a model for ancestral Cycloneuralia
or cycloneuralian larvae.
Lastly, the uncertain position of Arthropoda and
the proposed relationships within Cycloneuralia
demands an open mind, although there is, as stated
above, not a single character shared between
Arthropoda and S. australiensis. The proposed
Ecdysozoa hypothesis creates a new scenario, in
which arthropods and nemathelminths are very
close together and which has to be thoroughly
evaluated in future and, preferably, should
include a discussion on the arthropod ground
pattern, considering both autapomorphies and
plesiomorphies.
A final aspect concerns the occurrence of
larvae as a character in nemathelminth phylogeny.
Nielsen (1995) did not use this character, while Ax
(2003) assumed direct development – no larvae
– in the ground patterns of Nemathelminthes and
Cycloneuralia, which has been retained in the
Nematoda and Kinorhyncha (cf. Neuhaus 1995).
Accordingly, he regarded the life cycle including
larvae in Nematomorpha as an autapomorphy of
this taxon. Likewise, he regarded the occurrence
of larvae with a longitudinally folded lorica as a
synapomorphy of Priapulida and Loricifera and
used this feature to characterise his Vinctiplicata
(he regarded the single priapulid species without
larvae as secondarily derived). The possible larval
nature of the only specimen of S. australiensis
indicates it could have acquired larval development
independent of the other taxa. This implies that
larval development – also termed ‘indirect
development’ – could have evolved at least three
times convergently within Nemathelminthes.
The more parsimonious explanation is, in our
view, the acquisition of indirect development
only once in nemathelminth phylogeny, i.e.,
single evolution of a larva in the ground pattern
of Cycloneuralia, therefore represents an
autapomorphy of its stem species. Gastrotrichs
have no larvae originally, a plesiomorphy retained
from the bilaterian ground pattern, while inside
cycloneuralians, kinorhynchs and nematodes
wo u ld hav e modif i ed th e ir dev e lopment
convergently into direct development (nematodan
‘larvae’ are just small juveniles that moult
three times into the nal stage = adult). Also,
the priapulid Meiopriapulus fijiensis Morse,
1981 shows, unlike all other priapulids, direct
development (Higgins & Storch 1991). Although
it is uncertain that the specimen of S. australiensis
is a larva, if it is, it has the potential to add
evidence to the current discussion on phylogeny
and character evolution.
Fig. 10. Phylogenetic hypothesis of the systematic position of Shergoldana australiensis within the
Nemathelminthes and Cycloneuralia, combining the schemes of Ahlrichs 1995; Lemburg 1999; Ax 2003;
Nielsen 1995, 2001. The new taxon may be either a sister species to Cycloneuralia (1, autapomorphy: larva
with pharyngeal armature, short introvert and annulated zone) or the sister species to Scalidophora (2) or
Nematoida (3).
AAP Memoir 34 (2007) 515
Possible life habits of Shergoldana
australiensis
Primarily free-living (= non-parasitic) marine
cycloneuralian species are benthic or epibenthic:
the rather large priapulids crawl on the sea bottom
or dig at a shallow angle into the soft substrate, with
a particular order of muscle activities (Hammond
1970). Priapulus caudatus prefers to stay within
the soft bottom (Hammond 1970). Similarly,
the life habit of Chengjiang cycloneuralians has
been reconstructed generally as infaunal and the
species are considered to be burrowers (Huang et
al. 2004a, b). Han et al. (2004a, b) concluded from
their material that the animals were able to burrow
vertically. However, Maas et al. (2007) gave
reasons why early nemathelminths lived both on
the sea bottom and in the soft sediment, but were
restricted to the uppermost layer of the sediment,
i.e., were horizontal burrowers, just as are the
modern priapulids. Shergoldana australiensis was
not only very hairy but also had other remarkable
features, such as an antero-terminal mouth, the
pseudo-annulated region, indicating considerable
exure of this region, and the spiny region with
the remarkable orientation and possible use of
the spines to anchor the trunk, presumably in
conjunction with the contractible accordion-like
region. The caudal region may have added little to
movement of the animal, while the caudal spines
or setae may have served as sensory setae and/
or stabilisers.
Recent, free-living marine cycloneuralians
either feed on metazoans or on unicellular
organisms (Land 1970, 1972; Salvini-Plawen
1974; Kristensen 1983; Neuhaus & Higgins
2002). Recent scalidophorans feed by pulling their
prey into the gut by means of their pharynx, which
can be protracted and intruded, and, likewise, the
introvert can also be intruded, but this is a rather
crude picture, because the tiny kinorhynchs and
loriciferans each have a very special pharynx,
while the use of the introvert teeth is unclear at
best, at least for loriciferans. Only macroscopic
priapulids have strong, inwardly pointing
pharyngeal teeth (e.g., Merriman 1981). Escape
by their prey is difcult, if not impossible. The
situation is more difcult to estimate for the
Nematoida because most nematodes lack a
tooth-bearing pharynx region, and the ground
pattern condition remains unclear (see Lorenzen
1985; Nielsen 2001). Adult nematomorphs, on
the other hand, are non-feeding; only their larvae
absorb nutrients as internal parasites of various
arthropods (Schmidt-Rhaesa 2005).
CONCLUSIONS AND OUTLOOK
The morphology of the new fossil Shergoldana
australiensis indicates, in our view, close afliation
to cycloneuralian Nemathelminthes, a taxon
which is represented in the Cambrian not only
by various macroscopic taxa, but also embryonic
stages similarly preserved in an ‘Orsten’ type of
3D preservation by phosphate impregnation, as
in the new fossil form. Cycloneuralians are the
second group of animals besides the Arthropoda,
which have an all-enclosing cuticle that has to
be moulted, whether soft or rmly sclerotised.
Shergoldana australiensis possesses a remarkable
mixture of characters developed in different
cycloneuralian groups, but not in a single one of
them in this particular combination. Yet, the new
morphology has to t into the known scenario
of systematic relationships between the known
groups, which is still unsettled. Our morphology-
based phylogenetic analysis including the new
fossil (Fig. 10) conrms the system put forward
by Lemburg (1999; adopted by Ax 2003), but
detailed investigations, particularly of the anterior
body regions of the different cycloneuralian
taxa, with emphasis on its functional systems
for food intake and locomotion, is urgently
needed because of remaining inconsistencies
in description, terminology and alternative
systematic hypotheses. The information on the
new fossil is expected to aid in future, more
detailed consideration of the systematic status of
macroscopic 2D- and microscopic 3D-preserved
Cambrian putative roundworms.
ACKNOWLEDGEMENTS
We owe particular thanks to John H. Shergold,
who arranged cooperation with the Bureau of
Mineral Resources, Geology and Geophysics
(Canberra) and guided the field trip in 1986
enabling these exceptional nds. Our gratitude
also goes to Mrs. Annemarie Gossmann, Bonn,
who processed the Australian material, sorted
it and did much of the original SEM work
at the Palaeontological Institute in Bonn.
Thanks to the team of the Zentrale Einrichtung
Elektronenmikrsokopie of the University of Ulm.
Further thanks are due to Christian Lemburg,
Göttingen, Birger Neuhaus, Berlin, and Reinhardt
M. Kristensen, Copenhagen, for providing us
with literature, images, information on different
nemathelminths and discussion of the fossil
nd. Mr Ash Rahmani, Permissions Department,
Blackwell Publishing, Oxford kindly permitted us
to use an image published earlier (our Fig. 9A).
Andreas Schmidt-Rhaesa and Birger Neuhaus
reviewed the rst version and helped to improve
the manuscript. John Repetski, Reston, and
Euan Clarkson, Edinburgh, were kind enough
to improve the language of different versions of
the text. The Deutsche Forschungsgemeinschaft
DFG supported the eld survey in Australia and
AAP Memoir 34 (2007)
516
the ‘Orsten’ project over a long period.
REFERENCES
AdriAnov, A.v. & MAlAkhov, v. v. , 1995. The
phylogeny and classification of the phylum
Cephalorhyncha. Zoosystematica Rossica 3,
181–201.
Ad r i A n o v , A.v. & MA l A k h o v , v.v., 2001a. Symmetry
of priapulids (Priapulida). 1. Symmetry of adults.
Journal of Morphology 247, 99–110.
Ad r i A n o v , A.v. & MA l A k h o v , v.v., 2001b. Symmetry
of priapulids (Priapulida). 2. Symmetry of larvae.
Journal of Morphology 247, 111–121.
Ag u i n A l d o , A.M.A., Tu r b e v i l l e , J.M., li n f o r d , l.S.,
riverA, M.C., gArey, J.r., rAff, rudolph A. &
lA k e , J.A., 1997. Evidence for a clade of nematodes,
arthropods and other moulting animals. Nature 387,
489–493.
Ah l r i C h S , W.h., 1995. Ultrastruktur und Phylogenie von
Seison nebaliae (Grube 1859) und Seison annulatus
(Claus 1876): Hypothesen zu phylogenetischen
Verwandschaftsverhältnissen innerhalb der
Bilateria. Cuvillier, Göttingen, 310 p.
Ax, p., 1996. Multicellular Animals I. Springer, Berlin,
225 p.
Ax, p., 2003. Multicellular Animals III. Spektrum,
Heidelberg, 317 p.
bo h A l l , p.J., We l l S , M.r. & Ch A n d l e r , C.M., 1997.
External morphology of larvae of Chordodes
morgani (Nematomorpha). Invertebrate Biology
116, 26–29.
bu d d , g.e., 2003. Arthropods as ecdysozoans: the fossil
evidence. 479–487 in Legakis, A., Sfenthourakis, S.,
Polymeni, R. & Thessalou-Legaki, M. (eds), The
New Panorama of Animal Evolution. Proceedings
XVIII International Congress of Zoology, Athens,
2000. Pensoft Publishers, Soa.
Chen JunyuAn, WAloSzek, d., MAAS, A., brAun,
A., hu A n g di y i n g , WA n g xi u q i A n g & ST e i n , M.,
2007. Early Cambrian Yangtze Plate Maotianshan
Shale macrofauna biodiversity and the evolution of
predation. Palaeogeography, Palaeoclimatology,
Palaeoecology 254, 250–272.
Co n W Ay MorriS, S., 1977. Fossil priapulid worms.
Special Papers in Palaeontology 20, 1–159.
Co n WA y MorriS, S., 1985. Non-skeletalized lower
invertebrate fossils: a review. 343–359 in Conway
Morris, S., George, J.D., Gibson, R. & Platt, H.M.
(eds), The origins and relationships of lower
invertebrates. Clarendon Press, Oxford.
do n g xi p i n g , do n o g h u e , p.C.J., Ch e n g ho n g & li u
Ji A n b o , 2004. Fossil embryos from the Middle and
Late Cambrian of Hunan, South China. Nature
427, 237–240.
dong xiping, donoghue, p.C.J., CunninghAM, J.A.,
li u JiAnbo & Cheng hong, 2005. The anatomy,
afnity, and phylogenetic signicance of Markuelia.
Evolution & Development 7, 468–482.
do n o g h u e , p.C.J., be n g T S o n , S., do n g x ip i n g , go S T l i n g ,
n.J., huldTgren, T., CunninghAM, J.A., yi n
Ch o n g y u , yu e zh A o , pe n g fA n & STA M p A n o n i , M.,
2006b. Synchrotron X-ray tomographic microscopy
of fossil embryos. Nature 442, 680–683.
donoghue, p.C.J., kouChinSky, A., be n g T S o n , S.,
CunninghAM, J., dong xiping, repeTSki, J.e.,
vA l k o v , A.k. & WA l o S z e k , d., 2006a. Fossilized
embryos are widespread but the record is temporally
and taxonomically biased. Evolution & Development
8, 232–238.
ee r n i S S e , d.J., Al b e r T , J.S. & An d e r S o n , f.e., 1992.
Annelida and Arthropoda are not sister taxa:
A phylogenetic analysis of spiralian metazoan
morphology. Systematic Biology 41, 305-330.
eh l e r S , u., Ah l r i C h S , W.h., le M b u r g , C. & SC h M i d T -
rhAeSA, A., 1996. Phylogenetic systematization
of the Nemathelminthes (Aschelminthes).
Verhandlungen der Deutschen Zoologischen
Gesellschaft 89, 8.
gA r e y , J.r., 2001. Ecdysozoa: the relationship between
Cycloneuralia and Panarthropoda. Zoologischer
Anzeiger 240, 321–330.
gA r e y , J.r., 2003. Ecdysozoa: the evidence for
a close relationship between arthropods and
nematodes. 503–509 in Legakis, A., Sfenthourakis,
S., Polymeni, R. & Thessalou-Legaki, M. (eds., The
New Panorama of Animal Evolution. Proceedings
XVIII International Congress of Zoology, Athens,
2000. Pensoft Publishers, Soa.
ge g e n b A u r , C., 1859. Grundzüge der vergleichenden
Anatomie. Engelmann, Leipzig, 606 p.
hAMMond, r.A., 1970. The surface of Priapulus
caudatus (Lamarck, 1816) Nemathelminthes,
Priapulida. Zeitschrift für Morphologie der Tiere
68, 255–268.
hA n JiAn, Sh u de g A n , zhAng zhifei & li u JiAnni,
2004a. The earliest-known ancestors of Recent
Priapulomorpha from the Early Cambrian
Chengjiang Lagerstätte. Chinese Science Bulletin
49, 1860–1868.
hA n Ji A n , zh A n g z h i f e i & l i u J i A n n i , 2004b. Taphonomy
and ecology of the introverts in Chengjiang fauna.
Bul letin of Northwestern University (Natural
Science) 34, 207–212.
hennig, W., 1950. Grundzüge einer Theorie
der Phylogenetischen Systematik. Deutscher
Zentralverlag, Berlin, 250 p.
he n n i g , W., 1966. Phylogenetic Systematics. University
of Illinois Press, Urbana, 250 p.
hi g g i n S , r.p. & ST o r C h , v., 1991. Evidence for Direct
Development in Meiopriapulus jiensis (Priapulida).
Transactions of the American Microscopical Society
110, 37–46.
higginS, r.p., ST o r C h , v. & Shirley, T.C., 1993.
Scanning and Transmission Electron Microscopical
observations on the larvae of Priapulus caudatus
(Priapulida). Acta Zoologica 74(4), 301–319.
AAP Memoir 34 (2007) 517
ho u xiAnguAng, Aldridge, r.J., bergSTröM, J.,
Si v e T e r , dA.J., Si v e T e r , de.J., feng xiAnhuAn,
2004. The Cambrian fossils of Chengjiang, China
– The owering of early animal life. Blackwell,
Malden, 233 p.
ho u xi A n g u A n g , be r g S T r ö M , J. & yA n g Ji A n , 2006.
Distinguishing anomalocaridids from arthropods
and priapulids. Geological Journal 41, 259–269.
huAng diying, Ch e n JunyuAn & vAnnier, J., 2006.
Discussion on the systematic position of the Early
Cambrian priapulomorph worms. Chinese Science
Bulletin 51, 243–249.
hu A n g di y i n g , vA n n i e r , J. & Ch e n Ju n y u A n , 2004a.
Recent Priapulidae and their Early Cambrian
ancestors: comparisons and evolutionary
signicance. Geobios 37, 217–228.
hu A n g di y i n g , vA n n i e r , J. & Ch e n Ju n y u A n , 2004b.
Anatomy and lifestyles of Early Cambrian priapulid
worms exemplied by Corynetis and Anningvermis
from the Maotianshan Shale (SW China). Lethaia
37, 21–33.
kerp, h., hAAS, h. & kringS, M., 2007. Neue
bemerkenswerte Funde aus dem unterdevonischen
Rhynie Chert. Wissenschaftliche Mitteilungen des
Institutes für Geologie der Bergakademie Freiberg
36, 64–65.
kr i S T e n S e n , r.M., 1983. Loricifera, a new phylum with
Aschelminthes characters from the meiobenthos.
Zeitschrift für zoologische Systematik und
Evolutionsforschung 21, 163–180.
kr i S T e n S e n , r.M., 2002. An introduction to Loricifera,
Cycliophora, and Micrognathozoa. Integrative and
Comparative Biology 2, 641–651.
lA n d , J. v A n d e r , 1970. Systematics, zoogeography,
and ecology of the Priapulida. Zoologische
Verhandelingen 112, 4–117.
lA n d , J. v A n d e r , 1972. Priapulus from the deep sea
(Vermes, Priapulida). Zoologische Mededelingen
47, 358–368.
leMburg, C., 1995a. Ultrastructure of sense organs
and receptor cells of the neck and lorica of
the Halicryptus spinulosus larva (Priapulida).
Microfauna Marina 10, 7–30.
le M b u r g , C ., 1995b. Ultrastructure of the introvert and
associated structures of the larvae of Halicryptus
spinulosus (Priapulida). Zoomorphology 115,
11–29.
le M b u r g , C., 1999. Ultrastrukturelle Untersuchungen
an den Larven von Halicryptus spinulosus und
Priapulus caudatus – Hypothesen zur Phylogenie der
Priapulida und deren Bedeutung für die Evolution
der Nemathelminthes. Cuvillier, Göttingen, 393 p.
lorenzen, S., 1985. Phylogenetic aspects of
pseudocoelomate evolution. 210–223 in Conway
Morris, S., George, J.D., Gibson, R. & Platt, H.M.
(eds), The origins and relationships of lower
invertebrates. Clarendon Press, Oxford.
MAAS, A., brAun, A., dong xiping, donoghue,
p.C.J., Mü l l e r , k.J., ol e M p S k A , e., re p e T S k i , J.e.,
Si v e T e r , dA.J., ST e i n , M. & WA l o S z e k , d., 2006.
The ‘Orsten’ – more than a Cambrian Konservat-
Lagerstätte yielding exceptional preservation.
Palaeoworld 15, 266–282.
MA A S , A., hu A n g di y i n g , Ch e n Ju n y u A n , WA l o S z e k ,
d. & brAun, A., 2007. Benthic nemathelminth
predators, systematics, impact on the benthic
ecosystem and contribution to the discussion of
the Ecdysozoa hypothesis. Palaeogeography,
Palaeoclimatology, Palaeoecology 254, 288–306.
MA A S , A., MA y e r , g., kr i S T e n S e n , r.M. & WA l o S z e k ,
d., in press. A Cambrian micro-lobopodian and the
evolution of arthropod locomotion and reproduction.
Chinese Science Bulletin.
MA A S , A., WA l o S z e k , d., Ch e n Ju n y u A n , br A u n , A.,
WA n g xi q u i A n g & hu A n g di y i n g , 2004. Research
on Early Phylogeny of Arthropoda. Progress in
Natural Science 14, 158–166.
MAAS, A., WAloSzek, d. & Müller, k.J., 2003.
Morphology, ontogeny and phylogeny of the
Phosphatocopina (Crustacea) from the Upper
Cambrian ‘Orsten’ of Sweden. Fossils and Strata
49, 1–238.
MA l A k h o v , v.v., 1980. Cephalorhyncha, a new type of
animal kingdom uniting Priapulida, Kinorhyncha,
Gordiacea, and a system of Aschelminthes worms.
Zoologiceskij Zurnal 59, 485–499.
MAlAkhov, v.v., 1994. Nematodes. Structure,
Development, Classification, and Phylogeny.
Smithsonian Institution Press, Washington, 286 p.
MAlAkhov, v.v. & AdriAnov, A.v., 1995.
Cephalorhyncha – a new phylum of the animal
kingdom. KMK Scientic Press, Moscow, 199 p.
MAllATT, J.M., gArey, J.r. & ShulTz, J.W., 2004.
Ecdysozoan phylogeny and Bayesian inference:
rst use of nearly complete 28S and 18S rRNA
gene sequences to classify the arthropods and their
kin. Molecular Phylogenetics and Evolution 31,
178–191.
MAnuël, M., kr u S e , M., Müller, W.e.g. & le
pA r C o , y., 2000. The comparison of beta-thymosin
homologues among Metazoa supports an arthropod-
nematode clade. Journal of Molecular Evolution
51, 378–381.
Me r r i M A n , J.A., 1981. Cuticular structures of the
Priapulid Halicryptus spinulosus: A Scanning
Electron Microscopical Study. Zoomorphology 97,
285–295.
MorSe, M.P., 1981. Meiopriapulus jiensis n. gen.,
n. sp.: an interstitial priapulid from coarse sand in
Fiji. Transactions of the American Microscopical
Society 100, 239-252.
Mü l l e r , k.J., 1983
Müller, k.J., 1990. Upper Cambrian “Orsten”.
274–277 in Briggs, D.E.G. & Crowther, P.R. (eds),
Palaeobiology – A Synthesis. Blackwell, Boston.
Müller, k.J. & hinz, i., 1992. Cambrogeorginidae
AAP Memoir 34 (2007)
518
fam. nov., soft-integumented Problematica from
the Middle Cambrian of Australia. Alcheringa 16,
333-353.
Müller, k.J. & hinz-SChAllreuTer, i., 1993.
Palaeoscolecid worms from the Middle Cambrian
of Australia. Palaeontology 36, 549–592.
Mü l l e r , k.J. & WA l o S S e k , d., 1985. Skaracarida, a
new order of Crustacea from the Upper Cambrian
of Västergötland, Sweden. Fossils and Strata 17,
1–65.
Mü l l e r , k.J. & WA l o S S e k , d ., 1986a. Arthropod larvae
from the Upper Cambrian of Sweden. Transactions
of the Royal Society of Edinburgh: Earth Sciences
77, 157–179.
Mü l l e r , k.J. & WA l o S S e k , d., 1986b. Martinssonia
elongata gen. et sp. n., a crustacean-like euarthropod
from the Upper Cambrian`Orsten´ of Sweden.
Zoologica Scripta 15, 73–92.
Müller, k.J. & WAloSSek, d., 1988. External
morphology and larval development of the Upper
Cambrian maxillopod Bredocaris admirabilis.
Fossils and Strata 23, 1–70.
Müller, M.C.M., JoChMAnn, r., SChMidT-rhAeSA,
A., 2004. The musculature of horsehair worm
larvae (Gordius aquaticus, Paragordius varius,
Nematomorpha): F-actin staining and reconstruction
by cLSM and TEM. Zoomorphology 123, 45–54.
ne u h A u S , b., 1994. Ultrastructure of alimentary canal
and body cavity, ground pattern, and phylogenetic
relationships of the Kinorhyncha. Microfauna
Marina 9, 61–156.
neuhAuS, b., 1995. Postembryonic development of
Paracentrophyes praedictus (Homalorhagida):
neoteny questionable among the Kinorhyncha.
Zoologica Scripta 24, 179–192.
neuhAuS, b., 1997. Ultrastructure of the cephalic
sensory organs of adult Pycnophyes dentatus and of
the rst juvenile stage of P. kielensis (Kinorhyncha,
Homalorhagida). Zoomorphology 117, 33–40.
neuhAuS, b., breSCiAni, J. & peTerS, W., 1997.
Ultrastructure of the pharyngeal cuticle and
lectin labelling with wheat germ agglutinin-gold
conjugate indicating chitin in the pharyngeal cuticle
of Oesophagostomum dentatum (Strongylida,
Nematoda). Acta Zoologica 78, 205–213.
neuhAuS, b. & higginS, r.p., 2002. Ultrastructure,
biology, and phylogenetic relationships of
Kinorhyncha. Integrative and Comparative Biology
42, 619–632.
ni e l S e n , C., 1995. Animal Evolution: Interrelationships
of the living phyla. 1st Edition. Oxford University
Press, Oxford, 467 p.
ni e l S e n , C., 2001. Animal Evolution: Interrelationships
of the living phyla. 2nd Edition. Oxford University
Press, Oxford, 563 p.
pArk, J.-k., rh o , h.S., kriSTenSen, r.M., ki M , W.
& gi r i b e T , g., 2006. First molecular data on the
Phylum Loricifera – An investigation into the
phylogeny of Ecdysozoa with emphasis on the
positions of Loricifera and Priapulida. Zoological
Science 23, 943–954.
peTerSen, k.J. & eerniSSe, d.J., 2001. Animal
phylogeny and the ancestry of bilaterians: inferences
from morphology and 18S rDNA gene sequences.
Evolution & Development 3, 170–205.
po i n A r , g., Jr., lA C h A u d , J.-p., CA S T i l l o , A. & in fA n T e ,
f., 2005. Recent and fossil nematode parasites
(Nematoda: Mermithidae) of Neotropical ants.
Journal of Invertebrate Pathology 91, 19-26.
ri e M A n n , f. , 1972. Kinonchulus sattleri n. g.
n.sp. (Enoplida, Tripyloidea), an aberrant
freeliving nematode from the lower Amazonas.
Veröffentlichungen des Instituts für Meeresforschung
Bremerhaven 13, 317–326.
SA l v i n i -pl AW e n , l. von, 1974. Zur Morphologie
und Systematik der Priapulida: Chaetostephanus
praeposteriens; der Vertreter einer neuen Ordnung
Seticoronaria. Zeitschrift für zoologische Systematik
und Evolutionsforschung 12, 31–54.
SChMidT-rhAeSA, A., 1995. Zur Morphologie,
Biologie und Phylogenie der Nematomorpha.
Untersuchungen an Nectonema munidae und
Gordius aquaticus. Cuvillier, Göttingen, 276 p.
SC h M i d T -rh A e S A , A., 1998. Phylogenetic relationships
of the Nematomorpha – a discussion of current
hypotheses. Zoologischer Anzeiger 236, 203–216.
SChMidT-rhAeSA, A., 2002. Two dimensions of
biodiversity research exemplied by Nematomorpha
and Gastrotricha. Integrative and Comparative
Biology 42, 633–640.
SC h M i d T -rhAeSA, A., 2005. Morphogenesis of
Paragordius varius (Nematomorpha) during the
parasitic phase. Zoomorphology 124, 33–46.
SC h M i d T -rh A e S A , A., bA r T o l o M A e u S , T., le M b u r g , C.,
eh l e r S , u. & gA r e y , J.r., 1998. The position of the
Arthropoda in the phylogenetic system. Journal of
Morphology 238, 263–285.
SCholz, g., 2003. Is the taxon Articulata obsolete?
Arguments in favour of a close relationship
between annelids and arthropods. 489–501 in
Legakis, A., Sfenthourakis, S., Polymeni, R. &
Thessalou-Legaki, M. (eds), The New Panorama of
Animal Evolution. Proceedings XVIII International
Congress of Zoology, Athens, 2000. Pensoft
Publishers, Soa.
Si v e T e r , dA.J., WA l o S z e k , d. & Wi l l i A M S , M., 2003.
An Early Cambrian phosphatocopid crustacean
with three-dimensionally preserved soft parts
from Shropshire, England. S pecial Papers in
Palaeontology 70, 9-30.
TodAro, A., Telford, M.J., loCkyer, A.e . &
liTTleWood, d.T.k., 2006. Interrelationships of
the Gastrotricha and their place among the Metazoa
inferred from 18S rRNA genes. Zoologica Scripta
35, 251–259.
Wägele, J.-W. & MiSof, b., 2001. On quality of
AAP Memoir 34 (2007) 519
evidence in phylogeny reconstruction: a reply to
Zrzavý’s defence of the “Ecdysozoa”hypothesis.
Journal of Zoological Systematic and Evolutionary
Research 39, 165–176.
WA l C o T T , C.d., 1912. Cambrian Geology and
Paleontology II, Middle Cambrian Branchiopoda,
Malacostraca, Trilobita, and Merostomata.
Smithsonian Miscellaneous Collections 57,
145-228.
WA l o S S e k , d ., 1993. The Upper Cambrian Rehbachiella
kinnekullensis and the phylogeny of Branchiopoda
and Crustacea. Fossils and Strata 32, 1–202.
WA l o S S e k , d. & Mü l l e r , k.J., 1989. A second type
A-nauplius from the Upper Cambrian `Orsten´of
Sweden. Lethaia 22, 301–306.
WA l o S S e k , d., hi n z -SC h A l l r e u T e r , i., Sh e r g o l d , J.h. &
Mü l l e r , k.J., 1993. Three-dimensional preservation
of arthropod integument from the Middle Cambrian
of Australia. Lethaia 26, 7–15.
WAloSzek, d., Chen JunyuAn, MAAS, A. & WAng
xiuqiAng, 2005. Early Cambrian arthropods –
new insights into arthropod head and structural
evolution. Arthropod Structure & Development
34(2), 189–205.
We i T S C h A T , W. & Wi C h A r d , W., 2002. Atlas of Plants
and Animals in Baltic Amber. Pfeil, München,
256 p.
xi A o Sh u h A i , zh A n g y u n & kn o l l , A.h., 1998. Three-
dimensional preservation of algae and animal
embryos in a Neoproterozoic phosphorite. Nature
391, 553–558.
zhAng xiguAng, SiveTer, d.J., WAloSzek, d. &
MA A S , A ., 2007. An epipodite-bearing crown-group
crustacean from the Lower Cambrian. Nature 449,
595–598.
zrzAvý, J., 2001. Ecdysozoa versus Articulata:
clades, artifacts, prejudices. Journal of Zoological
Systematic and Evolutionary Research 39,
159–163.
