Resolving Details of the Nonbiomineralized Anatomy of Trilobites Using Computed
Tomographic Imaging Techniques
Thesis
Presented in Partial Fulfillment of the Requirements for the Master of Science in the
Graduate School of The Ohio State University
By
Jennifer Anita Peteya, B.S.
Graduate Program in Earth Sciences
The Ohio State University
2013
Thesis Committee:
Loren E. Babcock, Advisor
William I. Ausich
Stig M. Bergström
Copyright by
Jennifer Anita Peteya
2013
Abstract
Remains of two trilobite species, Elrathia kingii from the Wheeler Formation (Cambrian
Series 3), Utah, and Cornuproetus cornutus from the Hamar Laghdad Formation (Middle
Devonian), Alnif, Morocco, were studied using computed tomographic (CT) and
microtomographic (micro-CT) imaging techniques for evidence of nonbiomineralized
alimentary structures. Specimens of E. kingii showing simple digestive tracts are
complete dorsal exoskeletons preserved with cone-in-cone concretions on the ventral
side. Inferred stomach and intestinal structures are preserved in framboidal pyrite, likely
resulting from replication by a microbial biofilm. C. cornutus is preserved in nonconcretionary limestone with calcite spar lining the stomach ventral to the glabella.
Neither species shows sediment or macerated sclerites of any kind in the gut, which tends
to rule out the possibilities that they were sediment deposit-feeders or sclerite-ingesting
durophagous carnivores. Instead, the presence of early diagenetic minerals in the guts of
E. kingii and C. cornutus favors an interpretation of a carnivorous feeding strategy
involving separation of skeletal parts of prey prior to ingestion.
ii
Dedication
This manuscript is dedicated to my parents for encouraging me to go into the field of
paleontology and to Lee Gray for inspiring me to continue.
iii
Acknowledgments
I would like to thank Loren E. Babcock for providing most of the specimens used in this
study and providing guidance in the completion of the work. Daniel F. Merriam (Kansas
Geological Survey) provided specimens of Ditomopyge decurtata for study, but which
are not reported on here. I would also like to thank William Ausich and Matthew
Saltzman for their helpful advice through the completion of my studies and Stig
Bergström for his contribution to my thesis defense. Soo-Yeun Ahn from The University
of Akron supplied environmental scanning electron microscope images. Garrett Noble
and Kyle Bodnyk from The Ohio State University’s School of Biomedical Engineering
provided help and advice with the microtomography scans. Richard Hart provided access
to the microtomography facility in The Ohio State University’s School of Biomedical
Engineering and Ann Cook provided access to the computed tomography scanner in The
Ohio State University’s School of Earth Sciences. Funding for the project was provided
by Loren Babcock and the Friends of Orton Hall Fund of The Ohio State University.
iv
Vita
2010................................................................B.S. Geology, Mount Union College
2010 to present ...............................................Graduate Teaching Associate, School of
Earth Sciences, The Ohio State University
Field of Study
Major Field: Earth Sciences
v
Table of Contents
Abstract ..........................................................................................................ii
Dedication ......................................................................................................iii
Acknowledgments..........................................................................................iv
Vita.................................................................................................................v
List of Figures ................................................................................................vii
Chapter 1: Introduction ..................................................................................1
Chapter 2: Materials and Methods .................................................................4
Chapter 3: Scans of Elrathia kingii................................................................8
Chapter 4: Scans of Cornuproetus cornutus ..................................................17
Chapter 5: Discussion ....................................................................................20
References ......................................................................................................25
vi
List of Figures
Figure 1. Micro-CT scanner ...........................................................................5
Figure 2. Digestive structures in Elrathia kingii, PRI 0000A........................12
Figure 3, Digestive structures in Elrathia kingii, PRI 0000B ........................14
Figure 4. ESEM images of PRI 0000A and PRI 0000D ................................16
Figure 5. Digestive structures and traces in Cornuproetus cornutus .............18
Figure 6. Reconstruction of the morphology of the Elrathia kingii
alimentary canal, including the stomach in the anterior glabella and
intestine, in dorsal view .................................................................................24
vii
Chapter 1: Introduction
Much of the information about the nonbiomineralized anatomy of trilobites comes
from exceptionally preserved specimens representing a relatively small number of taxa.
Nonbiomineralized remains have been described from approximately 40 species, which
represents approximately 0.04% of the described species. Some of the more exquisite
examples of nonbiomineralized preservation are documented from specimens of Phacops
sp. (Stürmer and Bergström, 1973), Olenoides serratus (Whittington, 1975, 1980),
Triarthrus eatoni (Cisne, 1981), Agnostus pisiformis (Müller and Walossek, 1987),
Pterocephalia sp. (Chatterton et al., 1994), Buenellus higginsi (Babcock and Peel, 2007),
Isotelus maximus (Babcock, 2003; English and Babcock, 2007), Coosella kieri (Robison
and Babcock, 2011), Meniscopsia beebei (Robison and Babcock, 2011; Lerosey-Aubril et
al. 2012), Sphaerophthalmus? (Eriksson and Terfelt, 2012), Selenopeltis buchi, and
Biramites ingens (Fatka et al., 2013) from Konservat-lagerstӓtten (deposits of exceptional
preservation) in North America, Europe, and Asia. Preservation of nonbiomineralized
anatomy of trilobites varies. In some material, appendages are present and internal
structures are not. In others, internal structures are present and appendages are not, or
both appendages and internal structures are preserved. Trace fossils in sediment have
been used to supplement information on the ventral anatomy of trilobites (Jensen, 1990;
1
Brandt et al., 1995; Babcock, 2003; English and Babcock, 2007), but the information
provided by trace fossils is limited to details of external anatomy.
Exceptional preservation of trilobites and other marine organisms is inferred to
have occurred quickly after death (Briggs et al., 1994; Babcock and Chang, 1997;
Babcock et al., 2001; Butterfield, 2002; Zhu et al., 2005; Ciampaglio et al., 2006;
Robison and Babcock, 2011). Mineral replication of nonbiomineralized tissues was likely
mediated by microbial biofilms in most examples (see Borkow and Babcock, 2003; Maas
et al., 2006; English and Babcock, 2007; Lerosey-Aubril et al., 2010, 2012; Babcock and
Robison, 2011). Mineral replication or fill of various types has been described (e.g.,
Stürmer and Bergström, 1973; Whittington, 1980; Cisne, 1981; Müller and Walossek,
1987; Orr et al., 1998; Babcock, 2003; Zhu et al., 2005; English and Babcock, 2007;
Robison and Babcock, 2011). Among the preservational agents of nonbiomineralized
anatomy of trilobites are calcium phosphate (Chatterton et al., 1994; Robison and
Babcock, 2011; Lerosey-Aubril et al., 2010, 2012; Eriksson and Terfelt, 2012), calcium
carbonate (Chatterton et al., 1994; English and Babcock, 2007), iron sulfide (Stürmer and
Bergström, 1973; Cisne, 1982), aluminosilicates (Whittington, 1980), and silica (Babcock
and Peel, 2007).
Nonbiomineraized trilobite anatomy can be studied either through surface
examination of fortuitously broken or well-prepared specimens, or through non-invasive
imaging techniques. In comparatively rare examples, alimentary structures, limbs, or
other nonbiomineralized structures are evident in trilobites with surface examination (see
for example Chatterton et al., 1994; Babcock, 2003; Babcock and Peel, 2007; Robison
2
and Babcock, 2011; Fatka et al., 2013). Serial grinding and serial sectioning can reveal
nonbiomineralized anatomy (Walcott, 1881), but this leads to destruction of specimens
(Sutton et al., 2001). Non-invasive techniques (see for review Sutton, 2008), such as Xray imaging technology, have long been known to be effective for discerning
nonbiomineralized structures in unprepared and unexposed specimens (Stürmer and
Bergström, 1973; Cisne, 1981).
In recent years, standard x-ray imaging has been surpassed in utility by other noninvasive techniques, including computed tomography (CT), microtomography (microCT), and synchrotron radiation imaging. Such techniques make it possible to gain more
insight into the anatomy of various arthropods without destroying the specimens.
Computer-based imaging has revealed, for example, insect and arachnid inclusions in
opaque amber (Dierick et al., 2007; Penney et al., 2007; Soriano et al., 2010), external
anatomy of arthropods preserved in siderite (Garwood et al., 2009; Garwood and Sutton,
2010), and internal anatomy of the meraspid stage of a trilobite (Eriksson and Terfelt,
2012).
The purpose of this paper is to describe and interpret internal structures in two
species of Paleozoic trilobites from high-resolution CT images. Three specimens are
interpreted to have three-dimensionally preserved digestive structures. These are
compared to previous anatomical and ecological models, and the new information helps
to further constrain feeding strategies of the studied trilobite taxa.
3
Chapter 2: Materials and Methods
Materials – Several hundred Paleozoic trilobite specimens from various localities were
examined for evidence of possible nonbiomineralized anatomy and, from among them,
nine were selected for detailed study using CT scanning techniques. Selections were
made partly based on specimen size, as the samples were restricted by the 60 mm
diameter of the specimen chamber inside the micro-CT scanner. Small, complete,
inferred corpses were selected for micro-CT preview scans to determine if they could be
penetrated by an x-ray source and if a discernible image could be produced. Full microCT and CT scans were conducted on the specimens that fulfilled these criteria.
Seven Elrathia kingii (Meek, 1870) from the Wheeler Formation (Cambrian
Series 3), House Range, Utah, USA, and one Cornuproetus cornutus (Goldfuss, 1843)
from the Hamar Laghdad Formation (Middle Devonian) near Alnif, Morocco, were
scanned for evidence of nonbiomineralized anatomy. Five E. kingii specimens were later
rejected for further study due to lack of evidence of internal structures.
Repositories. – Illustrated specimens are deposited in the Paleontological
Research Institution, Ithaca, New York (PRI), USA.
4
Methods – Techniques used for study of trilobite specimens were microtomography
(micro-CT), computed tomography (CT), and environmental scanning electron
microscopy with energy-dispersive x-ray (ESEM/EDX).
Microtomography
Microtomography was conducted using a Skyscan 1172 high resolution micro-CT
scanner at The Ohio State University’s Department of Biomedical Engineering. The
micro-CT scanner produced hundreds of 0.8 to 27 μm resolution images at different
angles for each sample. Specimens were placed on a metal disk that rotated to expose all
parts of the specimen to a single X-ray source. Elrathia kingii specimens were wedged
between two pieces of styrofoam inside a plastic tube to reduce the effects of vibrations
of the machine on image quality (Figure 1). Quick scans were generated to see if a
discernible image could be produced from the specimen and if the specimen contained
internal fluctuations in density that could indicate the presence of
A
B
Figure 1. Micro-CT scanner. A, Skyscan 1172 micro-CT scanner with a trilobite
specimen in the sample chamber. B. Close-up of the sample chamber.
5
internal structures. Full scans were completed on trilobites that met these criteria using
an aluminum-copper filter to increase resolution. Some specimens contained too much
high density material in the matrix, resulting in black images in which structures of the
trilobite could not be differentiated from the matrix. Due to lack of visibility, these
specimens were rejected for further study.
The following settings were used to create micro-CT images for the three trilobite
specimens used in this study. Exposure time for PRI 0000A 260 ms, and source current
was 141 μA; exposure time for PRI 0000B was 180 ms; PRI 0000C was scanned using a
180 ms exposure time. The source current for PRI 0000B and PRI 0000C was 100 μA.
All three specimens were scanned using a frame averaging of 6 and an image pixel size
of 27.20 μm. More than one-thousand TIF files were generated for each specimen.
Raw images from the micro-CT scanner were uploaded to NRecon (Bruker
MicroCT, 2012) to be sectioned for later three-dimensional imaging. Transverse slices of
each raw image were generated at intervals of 27 μm, using a ring artifact reduction of 20
and a beam-hardening correction of 20% to decrease the effects of artifacts created by the
scanner. Images generated by NRecon were uploaded to CTvox (Bruker MicroCT, 2012)
to create three-dimensional computer reconstructions of each specimen that could be
rotated, sectioned at any angle, and enhanced.
Computed Tomography
A portable Neurologica CereTom CT scanner was used at The Ohio State
University School of Earth Sciences to create CT images of the specimens for
6
comparison with micro-CT images. The CereTom scanner has eight x-ray detectors that
rotate around a sample opposite an x-ray tube, generating hundreds of images that can be
compiled into interactive two-dimensional and three-dimensional models using the
machine’s software. Trilobites were scanned using an axial protocol at a resolution of
0.625 x 0.625 millimeters, which is the highest possible resolution generated by the
scanner. DIACOM images were captured directly from the CT scanner software and
uploaded to ImageJ (National Institutes of Health, 2011) for conversion from the
DIACOM files to jpeg files that are readable by a computer.
Scanning Electron Microscopy
A Quanta 200 Environmental Scanning Electron Microscope (ESEM) was used
by Soo-Yeun Ahn to study surface-exposed features of Elrathia kingii specimens,
including PRI 0000A and PRI 0000D, at The University of Akron’s Geology
Department. Whole specimens were initially scanned for evidence of bacterial
preservation. PRI 0000D, was cut between the thorax and cephalon for further imaging
and EDX (chemical) analysis. PRI 0000A was left uncut. No tomographic analyses were
conducted on PRI 0000D.
7
Chapter 3: Scans of Elrathia kingii
Two outstretched, complete dorsal exoskeletons of Elrathia kingii (Figure 2, 3)
were scanned for evidence of nonbiomineralized internal anatomy. These specimens were
previously discussed in an abstract by Babcock and Robison (2011) before CT scans
were obtained. The specimens, similar to many trilobites from the Wheeler and Marjum
formations of Utah, are compressed and preserved with white calcite cone-in-cone
structures on the undersides (see Bright, 1959; Robison, 1964, 1971; Hintze and Robison,
1987; Seilacher, 2001; Gaines and Droser, 2003; Robison and Babcock, 2011). These
cone-in-cone structures, which are geopetal indicators preserved on the stratigraphic
downward sides of polymerid trilobites and agnostoids (Bright, 1959; Robison, 1964;
Gaines and Droser, 2003, 2005; Brett et al., 2009; Robison and Babcock, 2011), are
interpreted as a form of concretionary calcite (Babcock and Robison, 2011; Robison and
Babcock, 2011). The glabella of PRI 0000A (Figure 2A) is crushed, presumably due to
the weight of overlying sediment on a gut that was not reinforced by sediment fill shortly
after the trilobite died (Robison and Babcock, 2011). Scouring on the exoskeleton of PRI
0000B suggests that the specimen was prepared prior to study and much of the anterior
glabella was removed, exposing a 2 mm long area with pyrite and limonite (Figure 3A).
8
When imaged using ESEM, PRI 0000A has a few pyrite framboids that may have
been associated with bacterial preservation of soft tissues (Figure 4A). Another E. kingii
specimen from the Wheeler Formation, PRI 0000D (Figure 4B), has many pyrite
framboids replicating inferred soft tissues in the axial lobe between the exoskeleton and
the ventral cone-in-cone calcification (Figure 4C, D). Framboidal pyrite is interpreted as
having a microbial origin, and it is likely that pyrite lining cracks in the glabella of PRI
0000A and the pyrite mass in the glabella of PRI 0000B resulted from the early
diagenesis of a microbial biofilm (see Borkow and Babcock, 2003; Babcock et al., 2005;
English and Babcock, 2007). Much of the pyrite has been replaced by iron oxide
(limonite).
CT and micro-CT images have revealed internal structures in both Elrathia kingii
specimens (Figure 2B-G, 3B-D). Bright, high density masses occur in the glabellas of
both PRI 0000A and PRI 0000B, which correspond to the pyrite visible on the surface
(Figures 2A-D, F, G, 3A-D). In PRI 0000B, the center of the glabellar mass is ventrally
convex. The convex area increases in width toward the center and tapers slightly
posteriorly, although not to a point. Two thin lateral structures occur on both sides of the
central mass and also gradually decrease in width toward the posterior (Figure 3C).
Another high density structure extends from the posterior glabella through the axial lobe
and gradually tapers in width to the tip of the axis of the pygidium of PRI 0000A (Figures
2F, G).
Pyritized material in the glabella of PRI 0000A and PRI 0000B is inferred to be
the result of early diagenetic mineralization of a biofilm-coated hypostome and presumed
9
stomach material. In PRI 0000A, pyrite is thickest in the cracks of the glabella (Figure
2B, D), suggesting that pyritization occurred shortly after the glabella and underlying
stomach were crushed by the weight of overlying sediment. Pyritization evidently
continued after this time, perhaps stimulated in part by fluid from the stomach that seeped
into the cracks. The pyritized mass in the anterior glabella of PRI 0000B includes the
hypostome in its original position. The mass is convex in the center on the ventral side
(Figures 3C, D). The thin, lateral, high density structures on either side of the convex
mass are not similar in size and appear to be connected to it anteriorly and ventrally
rather than projecting laterally from a single point, as would be expected if they were
foregut glands (see for example Babcock and Peel, 2007; Robison and Babcock, 2011;
Lerosey-Aubril et al., 2012; Fatka et al., 2013). It is possible that these structures are a
pyritized biofilm covering the hypostome.
The thoracic and pygidial axis of PRI 0000A is lined with pyrite, which appears
to connect to the pyrite in the glabella (Figures 3F, G), suggesting that both the intestine
and parts of the stomach are preserved in this specimen. Neither the stomach material
preserved in PRI 0000B (Figure 3E, F) nor the digestive tract preserved in PRI 0000A
(Figure 2H) contain sediment or evidence of skeletal material. There is also no evidence
of midgut glands and it is probable that the stomach, when inflated, was large and saclike (compare Harrington, 1959; Stürmer and Bergström, 1973; Cisne, 1981; LeroseyAubril et al., 2010; Robison and Babcock, 2011; Lerosey-Aubril et al., 2012).
Preservation of nonbiomineralized tissues in trilobites seems to follow two
endmember modes: 1, replication of external body parts such as appendages (as
10
expressed, for example in Orsten-type deposits; Müller and Walossek, 1987; Waloszek,
2003; Dong et al., 2005; Eriksson and Terfelt, 2012, and the Burgess Shale; Whittington,
1975, 1980; Briggs et al., 1994); and 2, mineral infilling of digestive structures (as
expressed, for example, in the the Sirius Passet Lagerstätte; Babcock and Peel, 2007, and
the Utah Lagerstätten; Robison and Babcock, 2011; Lerosey-Aubril et al., 2012). Some
occurrences of nonbiomineralized preservation in trilobites include a combination of the
two endmember modes (e.g., Stürmer and Bergström, 1973; Cisne, 1981; Babcock, 2003;
Babcock and Peel, 2007). The preservation of internal structures in specimens of E. kingii
described here follows the pattern of mineral infilling of digestive structures without
preservation of appendages or other external nonbiomineralized anatomy.
11
A
B
C
h
h
F
G
H
h
h
i
i
E
h
D
i
Figure 2
12
Figure 2. Digestive structures in Elrathia kingii, PRI 0000A. A, Dorsal view of the
specimen. B, micro-CT dorsal view. C, CT dorsal view. White areas in the trilobite axis
and around the periphery are an artifact reflecting the topography of the dorsal
exoskeleton and do not represent digestive structures. D. Slice across the center of the
glabella. Dorsal toward top. E. Slice across thoracic segment 2. Dorsal toward top. F,
Micro-CT MIP image. The calcite of the exoskeleton and ventral cone-in-cone structure
have been made transparent, making high density internal structures visible. G, Sagittal
slice through the axial lobe of the specimen. Dorsal toward the left and anterior toward
the top. Brightness of the anterior and posterior ends may be an artifact of the micro-CT
scanner. H, Interpretive drawing of internal structures in PRI 0000A based on CT and
micro-CT images. Hypostomal and stomach material is dark gray and intestinal material
is light gray. Abbreviations: h, structure ventral to the glabella interpreted as a biofilmcoated hypostome and possible stomach material; i, elongate structure ventral to the axis
interpreted as the intestine. Scale bars: 5 mm.
13
A
C
h
D
h
E
h
B
h
F
Figure 3
14
s
Figure 3. Digestive structures in Elrathia kingii, PRI 0000B. A, Dorsal view of the
specimen. B, Micro-CT dorsal view. C, Transverse slice across the anterior glabella.
Dorsal toward the top. D, Sagittal slice through the cephalon. Dorsal toward the top and
anterior toward the left. E, Interpretive drawing of the dorsal side of the cephalon with
the glabella outlined in a dotted line and internal structures illustrated in their positions
beneath the glabella. The hypostome is interpreted to be ventral to the stomach beneath
the anterior glabella. F, Interpretive drawing of the specimen. The hypostome, inferred to
have been biofilm-coated at the time of early diagenesis, and stomach are shown in gray.
Abbreviation: s, stomach. Scale bars: 5 mm.
15
A
C
ex
gt
cc
B
D
Figure 4. ESEM images made from specimens of Elrathia kingii, PRI 0000A and PRI
0000D. A, Surface of the thorax of PRI 0000A. B-D, Elrathia kingii, PRI 0000D, B, PRI
0000D before the specimen was cut for ESEM analysis. C, Axial lobe of thoracic
segment 1 showing the exoskeleton (ex), framboidal pyrite in the gut (gt), and the top of
the cone-in-cone structure (cc) on the ventral side of the trilobite D, Scale bars: A, 200
μm. B, 5 mm. C, 100 μm. D, 20 μm.
16
Chapter 4: Scans of Cornuproetus cornutus
A specimen of Cornuproetus cornutus (PRI 0000C; Figure 5A) is preserved
complete and partially enrolled in non-concretionary, medium gray limestone. The
glabella is inflated and the posterior 6 mm is lined with white calcite spar that extends 1
mm into the occipital ring, which may have resulted from early crystallization of a fluidfilled stomach (Figures 5A, B).
The stomach is visible on external examination, but is not expressed in CT and
micro-CT images (Figure 5 C-H), apparently because of minor density differences
between the calcite spar and limestone matrix. It appears to be the only preserved internal
structure in the C. cornutus specimen. There is a smaller high density mass visible in both
the CT and micro-CT images approximately 1.1 mm below the external surface of the
glabella (Figures 5D-I). However, the small mass cannot be positively linked to an
internal structure of the trilobite due to the presence of eight similar high density masses
that occur throughout the limestone matrix (Figures 5J, K). Additional masses inside the
matrix are also expressed as thin lines of pyrite visible on the surface (Figures 5L, M).
They appear to be pyritized burrows excavated shortly after final burial of the trilobite.
17
A
D
H
B
C
G
F
E
J
I
M
L
K
Figure 5
18
Figure 5. Internal structures in Cornuproetus cornutus. A, anterior dorsal view of
Cornuproetus cornutus, PRI 0000C. B, detail of calcite spar lining the stomach wall. C,
micro-CT anterior dorsal view of specimen. White material in the genal spines is likely
due to artifact from the micro-CT scanner. D-H, tomographic images of bright high
density mass ventral to the glabella. D, E, CT (D) and micro-CT (E) sagittal section,
anterior left. F, G, CT (F) and micro-CT (G) with dorsal 1.5 mm of the glabella removed.
Yellow material in F represents the topography of the specimen. H, transverse section
through center of glabella. Dorsal toward top. I, drawing illustrating size difference
between the calcite spar visible on the specimen (dark gray), interpreted as the stomach,
and the high density mass viewed in CT and micro-CT scans (light gray). J, K, CT scans
showing positions of trace fossils. Arrow points to high density mass in the glabella.
Insets show the position of specimen. L, M, posterior view of specimen (L) and
corresponding micro-CT image (M). Arrows indicate pyritized a trace fossil visible on
the surface of PRI 0000C and in the micro-CT scan. Scale bars: 10 mm.
19
Chapter 5: Discussion
Trilobite Feeding Strategies
Possible feeding strategies of trilobites were reviewed by Fortey and Owens
(1999). They include predation, both active carnivory and scavenging, parasitism, particle
feeding, and filter feeding. Non-durophagous predation is considered the primitive
feeding mode of trilobites (Fortey and Owens, 1999; Babcock, 2003). Active carnivory is
suggested by specimens of the trace fossil Rusophycus, which is typically inferred to have
been constructed by trilobites, shown to be intersecting Planolites-type traces, interpreted
to have been constructed by “worms” (Jensen, 1990; Brandt et al., 1995; Babcock, 2003,
2009; English and Babcock, 2007), spinose limb morphology that may have aided in the
grasping of prey (Stürmer and Bergström, 1973; Whittington, 1975, 1980; Hughes, 2001;
Babcock, 2003), and the presence of a diagenetically mineralized gut or crushed glabella
(Robison and Babcock, 2011). Rigid hypostomal attachment and a forked posterior
margin of the hypostome (Fortey and Owens, 1999; Babcock, 2003) have also been
attributed to a carnivorous habit, although longer forked morphologies (e.g.,
Hypodicranotus striatulus) may have been too cumbersome to have been used for the
manipulation of prey (Hegna, 2009). Pre-liquifying of prey before ingestion has been
inferred for trilobites with diagenetically mineralized digestive tracts, such as Buenellus
20
higginsi (Babcock and Peel, 2007). Due to their small size and possibly well-developed
digestive glands, agnostoids have been suggested to have had a parasitic feeding mode
like that of extant parasitic copepods (Bergström, 1973), however there is no confirmed
evidence of parasitism in any agnostoid (Fortey and Owen, 1999), and a parasitic mode
of feeding has not been inferred for polymerid trilobites. A particle feeding strategy
would be suggested by the presence of sediment in the alimentary canal similar to that in
the related nektaspid arachnomorph, Naraoia spinosa (Babcock and Chang, 1997;
Vannier and Chen, 2002; Bergström et al., 2007), but such a feature has not been
confirmed in a trilobite (confer Chatterton et al., 1994, who illustrated trilobites with
mineral-filled alimentary tracts), although it has not been ruled out for Deanaspis
goldfussi (Barrande, 1852). Having a hypostome that is not strengthened by attachment to
the cephalic doublure might also imply a particle-feeding strategy. Natant hypostomes
usually have a box-like or smooth posterior edge, rather than developing a forked margin,
which Fortey and Owens (1999) attributed to a particle-feeding strategy. Trilobites, such
as harpiids and trinucleiids, which have a large, convex cephalon that may have aided in
the circulation of currents around the trilobite are inferred to have been filter feeders
(Fortey and Owen, 1999).
Based on nonbiomineralized anatomical evidence (namely gut tracts preserved
through early diagenetic mineralization), Elrathia kingii and Cornuproetus cornutus are
here considered to have been non-sclerite-ingesting predators. E. kingii was previously
interpreted as a particle-feeder because of its natant, box-like hypostome (Fortey and
Owens, 1999; Gaines and Droser, 2003). However, many articulated specimens with
21
attached librigenae, including PRI 0000A, have crushed glabellas. A crushed glabella
suggests that the gut was fluid-filled rather than sediment-filled at the time of death
(Robison and Babcock, 2011). The lack of mud infill indicates that mud did not enter the
gut tract after death (see Butterfield, 2002) nor was it ingested during life (Babcock,
2003; Babcock and Peel, 2007).
It has been speculated that mineralization of the alimentary tract of trilobites and
the Leanchoilia (Butterfield, 2002; Babcock et al., 2012) has been associated with a fluidfilled gut, possibly resulting from a predatory habit similar to that of some modern
chelicerate arthropods, in which prey is liquefied and then consumed (Babcock, 2003;
Babcock and Peel, 2007). Alternatively, these ancient arthropods may have separated
sclerite pieces from digestible food before swallowing it (Robison and Babcock, 2011).
Alimentary structures in PRI 0000A and PRI 0000B are mineralized. Likewise, the
stomach of C. cornutus is lined with calcite spar rather than sediment, indicating this
trilobite was not a sediment-deposit feeder. Neither external examinations nor internal
scans of any of the trilobite taxa studied have revealed the presence of sclerites in
digestive structures, which is consistent with an interpretation of a prey-liquifying,
carnivorous feeding habit (Babcock, 2003; Babcock and Peel, 2007).
Models for the Trilobite Digestive System
Two models for the polymerid trilobite digestive system were discussed by
Lerosey-Aubril et al. (2012). One form is complex, consisting of a long, posteriorly
tapering alimentary canal with paired foregut and midgut glands (see for example
22
Chatterton et al., 1994; Babcock and Peel, 2007; Robison and Babcock, 2011; LeroseyAubril et al., 2012; Fatka et al., 2013). The other form is simple, with a round, sac-like
stomach ventral to the anterior glabella that is connected to a thin, posteriorly tapering
intestine that extends to the pygidial axis with no evidence of midgut glands (see for
example Stürmer and Bergström, 1973; Cisne, 1981, Fatka et al., 2013). A large stomach
is visible in the anterior glabella of PRI 0000B, and the ruptured(?) stomach of PRI
0000A was probably large and sac-like prior to compression. Micro-CT scans of PRI
0000A also have a posteriorly tapering intestine down the axis of the trilobite. Elrathia
kingii had a simple gut (Figure 6), making it the second Cambrian trilobite reported with
this presumably derived morphology (see Fatka et al., 2013).
The morphology in Cornuproetus cornutus is difficult to diagnose due to the lack
of preserved soft-parts in the thoracic axial lobe of PRI 0000C. However, the stomach
appears to be large compared to the overall size of the glabella, and there does not appear
to be evidence of foregut glands.
Eriksson and Terfelt (2012) illustrated a larval trilobite from the Cambrian of
Sweden that had a gut seemingly constricted lengthwise at the center. Robison and
Babcock (2011) and Lerosey-Aubril et al. (2012) also illustrated a trilobite from the
Cambrian of Utah (Coosella kieri) that has such a longitudinally constricted gut tract.
Specimens of E. kingii illustrated here do not have any obvious central constriction, and
the illustrated specimen of C. cornutus does not provide enough information to determine
whether it had a central constriction in the anterior part of the digestive system.
23
Figure 6. Reconstruction of the morphology of the Elrathia kingii alimentary canal,
including the stomach in the anterior glabella and intestine, in dorsal view.
24
References
Babcock, L.E. 2003. Trilobites in Paleozoic predator-prey systems, and their role in
reorganization of early Paleozoic ecosystems. In Kelley, P.H., Kowalewski, M.,
Hansen, T.A., eds., Predator-prey Interactions in the Fossil Record. Kluwer
Academic/Plenum Publishers. New York, p. 55-92.
Babcock, L.E., 2009. Visualizing Earth History. John Wiley & Sons. Hoboken, New
Jersey. 449 p.
Babcock, L.E., and Chang, W. 1997. Comparative taphonomy of two nonmineralized
arthropods: Naraoia (Nektaspida; early Cambrian, Chengjiang Biota, China) and
Limulus (Xiphosurida; Holocene, Atlantic Ocean). Bulletin of National Museum
of Natural Science 10:233-250.
Babcock, L.E., and Peel, J.S. 2007. Palaeobiology, taphonomy, and stratigraphic
significance of the trilobite Buenellus from the Sirius Passet Biota, Cambrian of
North Greenland. Memoirs of the Association of Australasian Palaeontologists
34:401-418.
Babcock, L. E., and Robison, R.A. 2011. Paleoecology and taphonomy of some new
trilobites from Cambrian (Series 3) Lagerstätten of Utah, USA. Museum of
Northern Arizona Bulletin 67:275-276.
Babcock, L.E., Zhang, W., and Leslie, S.A. 2001. The Chengjiang Biota: record of the
early Cambrian diversification of life and clues to exceptional preservation of
fossils. GSA Today 11:4-9.
Babcock, L.E., Zhao, Y.L., Peng, J., and Yang, X.L. 2012. A new Cambrian arthropod
Leanchoilia robisoni from the Kaili Lagerstӓtte, Guizhou, China. Journal of
Guizhou University (Natural Science) 29 Supplement 1:10-15.
Barrande, J. 1852. Système Silurien du Centre de la Bohême: Ière Partie, Crustacés,
Trilobites. Privately published. Prague & Paris. 935 p.
25
Bergström, J. 1973. Organization, life, and systematic of trilobites. Fossils and Strata 2:
1-69.
Bergström, J., Hou, X., and Hålenius, U. 2007. Gut contents and feeding in the Cambrian
arthropod Naraoia. GFF 129:71-76.
Borkow, P.S., and Babcock, L.E. 2003. Turning pyrite concretions outside-in: role of
biofilms in pyritization of fossils. The Sedimentary Record 1:4-7.
Brandt, D.S., Meyer, D.L., and Lask, P.B. 1995. Isotelus (Trilobita) “hunting burrow”
from Upper Ordovician strata, Ohio. Journal of Paleontology 69:1079-1083.
Brett, C.E., Allison, P.A., DeSantis, M.K., Lidell, W.D., and Kramer, A. 2009. Sequence
stratigraphy, cyclic facies, and lagerstӓtten in the middle Cambrian Wheeler and
Marjum Formations, Great Basin, Utah. Palaeogeography, Palaeoclimatology,
Palaeoecology 277:2-33.
Briggs, D.E.G., Erwin, D.H., and Collier, F.J. 1994. The Fossils of the Burgess Shale.
Smithsonian Institution. Washington, D.C. 238 p.
Bright, R. C. 1959. A paleoecologic and biometric study of the Middle Cambrian trilobite
Elrathia kingii (Meek). Journal of Paleontology 33:83–98.
Bruker MicroCT. 2012. CTvox: Volume Rendering (Version 2.4) [Computer Program].
Available at http://www.skyscan.be/products/downloads.htm (Accessed 6
December 2012).
Bruker MicroCT. 2012. NRecon Reconstruction (Version 1.6.8) [Computer Program].
Available at http://www.skyscan.be/products/downloads.htm (Accessed 6
December 2012).
Butterfield, N.J. 2002. Leanchoilia guts and the interpretation of three-dimensional
structures in Burgess Shale-type fossils. Paleobiology 28:155-171.
Chatterton, B.D.E., Johanson, Z., and Sutherland, G. 1994. Form of the trilobite
digestive system: alimentary structures in Pterocephalia. Journal of Paleontology
68:294-305.
Ciampaglio, C.N., Babcock, L.E., Wellman, C.L., York, A.R., and Brunswick, H.K.
2006. Phylogenetic affinities and taphonomy of Brooksella from the Cambrian of
Georgia and Alabama, USA. Palaeoworld 15:256-265.
Cisne, J.L. 1981. Triarthrus eatoni (Trilobita): anatomy of its exoskeletal,
skeletomuscular, and digestive systems. Palaeontographica Americana 9:95-142.
26
Dierick, M., Cnudde, V., Masschaele, B., Vlassenbroeck, J., van Hoorebeke, L., and
Jacobs, P. 2007. Micro-CT of fossils preserved in amber. Nuclear Instruments
and Methods in Physics Research A 580:641-643.
Dong, X., Donoghue, P.C.J., Liu, Z., Liu, J., and Peng, F. 2005. The fossils of Orstentype preservation from Middle and Upper Cambrian of Hunan, China. Chinese
Science Bulletin 50:1352-1357.
English, A.M., and Babcock, L.E. 2007. Feeding behaviour of two Ordovician trilobites
inferred from trace fossils and non-biomineralized anatomy, Ohio and Kentucky,
USA. Association of Australasian Palaeontologists Memoir 34:537-544.
Eriksson, M.E., and Terfelt, F. 2012. Exceptionally preserved Cambrian trilobite
digestive system revealed in 3D by synchrotron-radiation x-ray tomographic
microscopy. PLoS ONE 7:1-5.
Fatka, O., Lerosey-Aubril, R., Budil, P., and Rak, S. 2013. Fossilized guts in trilobites
from the Upper Ordovician Letná Formation (Prague Basin, Czech Republic).
Bulletin of Geosciences 88:95-104.
Fortey, R.A., and Owens, A.W. 1999. Feeding habits in trilobites. Palaeontology 42:429465.
Gaines, R. R., and Droser, M.L. 2003. Paleoecology of the familiar trilobite Elrathia
kingii: An early exaerobic zone inhabitant. Geology 31:941–944.
Gaines, R.R., and Droser, M.L. 2005. New approaches to understanding the mechanics
of Burgess Shale-type deposits: from the micron scale to the global picture. The
Sedimentary Record 3:4-8.
Garwood, R., Dunlop, J.A., and Sutton, M.D. 2009. High-fidelity X-ray microtomography reconstruction of siderite-hosted Carboniferous arachnids. Biology
Letters 5:841-844.
Garwood, R., and Sutton, M. 2010. X-ray micro-tomography of Carboniferous stemDictyoptera: new insights into early insects. Biology Letters 6:699-702.
Goldfuss, A. 1843. Systematische Übersicht der Trilobiten und Beschreibung einiger
neuen Arten derselben. Neues Jahrbuch für Mineralogie, Geognosie, Geologie
und Petrefakten-kunde 1843:537-567.
27
Harrington, H.J. 1959. General description of Trilobita. In R.C. Moore, ed., Treatise on
Invertebrate Paleontology, Part O, Arthropoda 1. Geological Society of America
University of Kansas Press. Boulder and Lawrence. p. 38-117.
Hegna, T.A. 2009. The function of forks: Isotelus-type hypostomes and trilobite feeding.
Lethaia 43: 411-419.
Hintze, L. F., and Robison, R.A. 1987. The House Range, western Utah: Cambrian
mecca. In S. S. Beus, ed., Rocky Mountain Section of the Geological Society of
America, Centennial Field Guide, vol. 2. Geological Society of America. Boulder,
p. 257–260.
Hughes, N.C. 2001. Ecologic evolution of Cambrian trilobites. In Zhuravlev, A.Y.,
Riding, R., eds., Perspectives in paleobiology and earth history. Columbia
University Press, New York. p. 370-403.
Jensen, S. 1990, Predation by early Cambrian trilobites on infaunal worms – evidence
from the Swedish Mickwitzia Sandstone. Lethaia 23:29-42.
Lerosey-Aubril, R., Hegna, T.A., Kier, C., Bonino, E., Habersetzer, J., and Carré, M.
2012. Controls on gut phosphatisation: the trilobites from the Weeks Formation
Lagerstӓtte (Cambrian; Utah). PLoS ONE 7:1-9.
Lerosey-Aubril, R., Hegna, T.A., and Olive, S. 2010. Inferring internal anatomy from the
trilobite exoskeleton: the relationship between frontal auxiliary impressions and
the digestive system. Lethaia 44:166-184.
Maas, A., Braun, A., Dong, X.P., Donoghue, P.C.J., Müller, K.J., Olempska, E.,
Repetski, J.E., Siveter, D.J., Stein, M., and Waloszek, D. 2006. The ‘Orsten’ –
more than a Cambrian Konservat-lagerstӓtte yielding exceptional preservation.
Palaeoworld 15:266-282.
Meek, F.B. 1870. Descriptions of fossils collected by the U.S. Geological Survey under
the charge of Clerence King, esq. Academy of Natural Sciences of Philadelphia
Proceedings14:54-64.
Müller, K. J., and Walossek, D. 1987. Morphology, ontogeny and life habit of Agnostus
pisiformis from the Upper Cambrian of Sweden. Fossils and Strata 19:1-124.
National Institute of Health. 2011. ImageJ (Version 1.45s) [Computer Program].
Available at http://rsbweb.nih.gov/ij/download.html (Accessed 25 April 2012).
Orr, P.J., Briggs, D.E.G., and Kearns, S.L. 1998. Cambrian Burgess Shale animals
replicated in clay minerals. Science 281:1173-1175.
28
Penney, D., Dierick, M., Cnudde, V., Masschaele, B., Vlassenbroeck, J., van Hoorebeke,
L., and Jacobs, P. 2007. First fossil Micropholcommatidae (Araneae), imaged in
Eocene Paris amber using X-ray computed tomography. Zootaxa 1623:47-53.
Robison, R. A. 1964. Late Middle Cambrian faunas from western Utah. Journal of
Paleontology 38:510-566.
Robison, R.A. 1971. Additional Middle Cambrian trilobites from the Wheeler Shale of
Utah. Journal of Paleontology 45:796-804.
Robison, R.A., and Babcock, L.E. 2011. Systematics, paleobiology, and taphonomy of
some exceptionally preserved trilobites from Cambrian Lagerstӓtten of Utah.
Paleontological Contributions 5:1-46.
Seilacher, A. 2001. Concretion morphologies reflecting diagenetic and epigenetic
pathways. Sedimentary Geology 143:41-57.
Soriano, C., Archer, M., Azar, D., Creaser, P., Delclòs, X., Godthelp, H., Hand, S., Jones,
A., Nel, A., Néraudeau, D., Ortega-Blanco, J., Pérez-de la Fuente, R., Perrichot,
V., Saupe, E., Kraemer, M.S., and Tafforeau, P. 2010. Synchrotron x-ray imaging
of inclusions in amber. Comptes Rendus de l’Académie des Sciences Palevol
9:361-368.
Stürmer, W., and Bergström, J. 1973. New discoveries on trilobites by X-rays.
Paläontologische Zeitschrift 47:104-141.
Sutton, M.D. 2008. Tomographic techniques for the study of exceptionally preserved
fossils. Proceedings of the Royal Society B 257:1587-1593.
Sutton, M.D., Briggs, D.E.G., Siveter, D.J., and Siveter, D.J. 2001. Methodologies for
the visualization and reconstruction of three-dimensional fossils from the Silurian
Herefordshire Lagerstӓtte. Paleontologia Electronica 4:1-17.
Vannier, J., and Chen, J. 2002. Digestive system and feeding mode in Cambrian naraoiid
arthropods. Lethaia 35:107-120.
Walcott, C.D. 1881. The trilobite: new and old evidence relating to its organization.
Bulletin of the Museum of Comparative Zoology at Harvard College, in
Cambridge 8:191-230.
Waloszek, D. 2003. The ‘Orsten’ window – a three-dimensionally preserved Upper
Cambrian meiofauna and its contribution to our understanding of the evolution of
Arthropoda. Paleontological Research 7:71-88.
29
Whittington, H.B. 1975. Trilobites with appendages from the Middle Cambrian, Burgess
Shale, British Columbia. Fossils and Strata 4:97-136.
Whittington, H.B. 1980. Exoskeleton, moult stage, appendage morphology, and habits of
the Middle Cambrian trilobite Olenoides serratus. Palaeontology 23:173-204.
Zhu, M.Y., Babcock, L.E., and Steiner, M. 2005. Fossilization modes in the Chengjiang
Lagerstӓtte (Cambrian of China): testing the roles of organic preservation and
diagenetic alteration in exceptional preservation. Palaeogeography,
Palaeoclimatology, Palaeoecology 220:31-46
30