The oral cone of Anomalocaris is not a classic ‘‘peytoia’’

Article (PDF Available)inThe Science of Nature 99(6):501-4 · April 2012with 476 Reads
DOI: 10.1007/s00114-012-0910-8 · Source: PubMed
Abstract
The Cambro-Ordovician anomalocaridids are large ecdysozoans commonly regarded as ancestors of the arthropods and apex predators. Predation is indicated partly by the presence of an unusual "peytoia"-type oral cone, which is a tetraradial outer ring of 32 plates, four of which are enlarged and in perpendicular arrangement. This oral cone morphology was considered a highly consistent and defining characteristic of well-known Burgess Shale taxa. It is here shown that Anomalocaris has a different oral cone, with only three large plates and a variable number of smaller and medium plates. Its functional morphology suggests that suction, rather than biting, was used for food ingestion, and that anomalocaridids in general employed a range of different scavenging and predatory feeding strategies. Removing anomalocaridids from the position of highly specialized trilobite predators forces a reconsideration of the ecological structure of the earliest marine animal communities in the Cambrian.
SHORT COMMUNICATION
The oral cone of Anomalocaris is not a classic ‘‘ peytoia’’
Allison C. Daley &Jan Bergström
Received: 10 November 2011 / Revised: 15 March 2012 /Accepted: 17 March 2012 /Published online: 5 April 2012
#Springer-Verlag 2012
Abstract The Cambro-Ordovician anomalocaridids are large
ecdysozoans commonly regarded as ancestors of the arthro-
pods and apex predators. Predation is indicated partly by the
presence of an unusual peytoia-type oral cone, which is a
tetraradial outer ring of 32 plates, four of which are enlarged
and in perpendicular arrangement. This oral cone morphology
was considered a highly consistent and defining characteristic
of well-known Burgess Shale taxa. It is here shown that
Anomalocaris has a different oral cone, with only three large
plates and a variable number of smaller and medium plates. Its
functional morphology suggests that suction, rather than bit-
ing, was used for food ingestion, and that anomalocaridids in
general employed a range of different scavenging and predato-
ry feeding strategies. Removing anomalocaridids from the
position of highly specialized trilobite predators forces a recon-
sideration of the ecological structure of the earliest marine
animal communities in the Cambrian.
Keywords Anomalocaridids .Cambrian .Oral cone .
Peytoia .Predation .Burgess Shale
Introduction
Anomalocaridids are some of the more controversial taxa
described from Cambrian fossil Lagerstätten, being character-
ized by an unusual morphology and complicated history of
description (see Collins (1996) for review). They possess a
segmented body with swim flaps, a plated oral cone, stalked
eyes, frontal appendages and cephalic carapaces (Whittington
and Briggs 1985). As ecdysozoans derived from lobopodians,
they are either part of a paraphyletic stem lineage leading to
the arthropods or in a sister group relationship to the arthro-
pods (see Edgecombe (2010) for review).
One of the most distinctive anomalocaridid features is their
oral cone. According to previous understanding, the oral cone
consists of 32 plates, with four large plates situated anteriorly,
posteriorly and laterally, 90° apart. The plates surround a
square or rectangular central opening into which short spines
protrude (Fig. 1a). This is the "peytoia" cone. Its distinct
morphology was used to unite the Burgess Shale taxa Anom-
alocaris (Anomalocaris canadensis), Laggania (Anomalocaris
nathorsti)(Fig.1a) (Whittington and Briggs 1985)andHurdia
victoria (Fig. 1b)(Daleyetal.2009) into order Radiodonta
(Collins 1996). The oral cone structure was thought to vary
little between these genera, with Hurdia being distinguished on
the presence of extra teeth within the central opening (Daley et
al. 2009)andAnomalocaris having a more diamond-shaped
and spiny oral cone than Laggania (Collins 1996).
Examination of whole-body specimens and disarticulated
assemblages of A. canadensis collected from the Burgess
Shale by the Royal Ontario Museum has revealed that the
oral cone of this species is not a 32-plate tetraradial
peytoia. This highlights a serious misunderstanding of
one of the most renowned anomalocaridids, which has
implications for the taxonomy, systematics and ecology of
the clade.
Communicated by: Sven Thatje
A. C. Daley (*)
Department of Palaeontology, Natural History Museum,
Cromwell Road,
London SW7 5BD, UK
e-mail: A.Daley@nhm.ac.uk
A. C. Daley
Department of Earth Sciences, University of Bristol,
Wills Memorial Building, Queens Road,
Bristol BS8 1RJ, UK
J. Bergström
Department of Palaeozoology,
Swedish Museum of Natural History,
P. O. Box 50007, 104 05 Stockholm, Sweden
Naturwissenschaften (2012) 99:501504
DOI 10.1007/s00114-012-0910-8
Materials and methods
A total of 44 specimens from the Royal Ontario Museum
(ROM 51213, 5121551216 and 6164261680), Geological
Survey of Canada (GSC 75535) and Smithsonian National
Museum of Natural History (USNM 189024) were exam-
ined. ROM and GSC specimens are from the Raymond
Quarry Member, and the USNM specimen from the Walcott
Quarry Member, of the Burgess Shale Formation on Fossil
Ridge in Yoho National Park in the Rocky Mountains of
British Columbia, Canada. The specimens were photo-
graphed digitally using polarising filters at the camera and
at the light source to increase contrast, and some were
submerged completely under water to accentuate reflective
structures. A Mejii Techno RZ stereomicroscope was used
for Camera lucida drawings.
The oral cone structure of Anomalocaris
The oral cone of Anomalocaris possesses three large plates
separated by medium-sized and small plates that are increas-
ingly furrowed or folded towards the outer margins. The
three large plates impose a bilateral symmetry to the mouth-
parts, with the largest plate anterior and separated by ap-
proximately 130140° from the two large posterolateral
plates, which are separated from each other by approximately
90100° (Fig. 2). Medium-sized plates are located adjacent to
the large plates or are alternating with smaller plates (Fig. 2b,
c), with at least eight medium plates in the most complete
specimens (e.g. Fig. 2i, j). Large and medium plates have
clusters of up to 16 small scale-like nodes on their surfaces
(Fig. 2d). The nodes have an asymmetric profile with the steep
side facing the central opening.
Distally, the large and medium plates have up to five
deep folds (Fig. 2j). These extend no more than one-
quarter of the total plate length. Small plates are narrow
and are also furrowed by folds (Fig. 2h, j) that extend no
more than half the plate length.
The oral cone of Anomalocaris is rounded, not diamond-
shaped as suggested by Collins (1996, p. 290, Fig. 9). The
central opening is small and irregular in shape, with variable
numbers of spines projecting into it. One specimen (Fig. 2f)
preserves four small spines on both of its well-preserved
larger plates and one or two poorly preserved spines on
adjacent medium-sized plates. One of the best preserved
oral cones (Fig. 2gi) has up to five spines on the largest
plate and single spines in intervening medium and small
plates.
This oral cone morphology is found in all published
assemblages and whole-body specimens of A. canaden-
sis where mouthparts are present, including the first
described assemblage (USNM 189024) (Figs. 7, 9 and
11 of Whittington and Briggs 1985) and body (GSC
75535) (Figs. 36, 8, 10 and 12 of Whittington and
Briggs 1985) specimens and two other body specimens,
ROM 51213 (Fig. 2e) (Fig. 4.3 of Collins 1996)and
ROM 51215 (Fig. 2a-d)(Fig.5.1ofCollins1996).
Collins (1996, Fig. 5.1) illustrated ROM 51215 as a mouth
cone belonging to A. canadensis but neither noted its
triradial symmetry (Fig. 2bd) nor showed the accom-
panying appendages (Fig. 2a) and partial body. Addi-
tionally, 34 previously unpublished disarticulated
assemblages show Anomalocaris appendages in close
association with triradial oral cones. Three disarticulated
assemblages show Anomalocaris appendages on the
same slab as tetraradial Peytoia mouthparts, but they
are either separated from each other by several centi-
meters (e.g. ROM 61677 and ROM 51216) (Fig. 5.2 of
Collins 1996) or are on different surfaces separated by
2 mm of rock (ROM 61676). These assemblages likely
represent composite fossil associations of two different
anomalocaridids, as seen in other mixed associations
bac
Fig. 1 Oral cone morphology of three Burgess Shale anomalocaridid taxa. Anterior at top. aPeytoia nathorsti, showing characteristic 32 plates. b
Hurdia victoria, with extra rows of plates within the central opening. cAnomalocaris canadensis, showing triradial plate arrangement
502 Naturwissenschaften (2012) 99:501504
(Daley and Budd 2010). Three isolated specimens of
Anomalocaris-type mouthparts have also been recog-
nized, one of which is well-preserved and complete
(Fig. 2j).
Discussion
The tetraradial structure of Peytoia nathorsti and the poorly
preserved body of Laggania cambria were described in the
same publication (Walcott 1911). Regarded as conspecific, P.
nathorsti was selected to have precedence over L. cambria
(Conway Morris 1978). Based on a specimen (Fig. 5.2 of
Collins 1996) with an isolated A. canadensis appendage
(Whiteaves 1892) and an oral cone morphologically the same
as the holotype of P. nathorsti(Collins 1996,p.288),P.
nathorsti was judged to be a junior synonym of A.canadensis.
As a consequence, the second species known from whole-body
specimens, A. nathorsti (Whittington and Briggs 1985), became
known as L. cambria. Morphological differences between A.
canadensis and this second taxon are significant enough to
warrant separate generic names (Whittington and Briggs
1985;Chenetal.1994), and this second taxon has been called
L. cambria (Collins 1996; Daley et al. 2009; Daley and Budd
2010), P. n a t h o r s t i (Chen et al. 1994;Houetal.2006)and
Laggania nathorsti (Briggs et al. 2008). As the specimen used
to identify P. n a t h o r s t i as a junior synonym of Anomalocaris
(Fig. 5.2 of Collins 1996) is a tetraradial oral cone, Peytoia is
actually a senior synonym of Laggania (Conway Morris 1978).
The correct term for the second taxon is Petyoia nathorsti.
Specimens of isolated oral cones with 32 plates show
variation in outline (rectangular, circular and diamond-
shaped), a feature that previously distinguished Anomaloca-
ris from Peytoia (Collins 1996). It is now unclear if differ-
ences in mouthpart outlines are due to taphonomy, ontogeny
or systematics. Hurdia mouthparts are identified by the
presence of extra rows of inner spines (Daley et al. 2009)
and a well-preserved Peytoia specimen (USNM 274143)
(Figs. 17 and 2024 of Whittington and Briggs 1985) has
a rectangular oral cone.
An isolated oral cone with folded plates indicates the
presence of the triradial oral cone type in a Chengjiang
species of Anomalocaris (Fig. 5A of Chen et al. 1994)and
another in a deformed specimen of the Chengjiang
Fig. 2 Oral cone of
Anomalocaris canadensis from
the Raymond Quarry, Burgess
Shale, Canada. Specimens
photographed under high-angle
cross-polarized lighting
directed from top left, unless
otherwise indicated. Scale bars
equal 10 mm in (a,g), 5 mm in
(b-f,h-j). aROM 51215,
assemblage with pair of
appendages and oral cone,
under low-angle lighting. b
Camera lucida drawing of oral
cone of ROM 51215. cOral
cone in ROM 51215, under
low-angle incident lighting. d
Close up of scale-like nodes on
surface of large plates of ROM
51215, under low-angle
incident lighting from top right.
eROM 51213, head region
showing oral cone with three
large plates (arrows). fROM
61669, oral cone. gROM
61652, appendages and oral
cone with superimposed
Leanchoilia.hROM 61652,
oral cone. iCamera lucida
drawing of oral cone of ROM
61652. jROM 61679, isolated
oral cone showing furrows/
folds in outer margins of large
plates (arrows)
Naturwissenschaften (2012) 99:501504 503
Anomalocaris saron (Fig. 6 of Hou et al. 1995). The only
other published specimen of an A. saron oral cone (Figs. 8.1
and9ofLieberman2003) from the Pioche Shale of Nevada
may adhere to the triradial morphology. Other Anomalocaris
species are preserved without closely associated oral cones.
Anomalocaridids have long been compared to arthropods
and an understanding of their morphology is crucial to
understanding the early evolution of this phylum. Despite
their global dispersal and importance to arthropod evolution,
the morphology of anomalocaridids, in particular A. cana-
densis, is actually poorly known. A clearer picture of anom-
alocaridid oral cone morphology is herein provided. Oral
structures in arthropods are modified limbs, never oral cones
(Bergström and Hou 2004). Undifferentiated oral plates are
found in the lobopodian taxon Pambdelurion (Budd 1998),
which some phylogenetic analyses (Daley et al. 2009; Budd
1996;Maetal.2009) place in a position basal to the
anomalocaridids. As features such as the oral cone are of
critical interest to phylogenetic studies, the systematics of
the anomalocaridid clade needs re-examination, pending a
complete re-description of Anomalocaris.
The recognition of a new oral cone morphology in Anom-
alocaris suggests that Cambrian anomalocaridid taxa were
employing a variety of different feeding strategies, corrobo-
rating what has also been shown from frontal appendages
(Daley and Budd 2010). Anomalocaris was previously con-
sidered as the highly specialized predator responsible for
W-shaped bite marksin Cambrian trilobites (Nedin 1999).
This view is challenged in two abstracts, where deformation
suggests that anomalocaridid oral cones were relatively soft
(Hagadorn 2009), and computer modeling shows that a biting
motion could not puncture trilobite exoskeletons (Hagadorn
2010). The work presented herein expands on this idea by
illustrating that the central opening of Anomalocaris oral
cones has an irregular shape and small size, making it unsuit-
able for strong biting motions. Instead, anomalocaridid oral
cones were stiff structures that may have employed suction to
bring soft food items towards the mouth. As opposed to being
highly specialized trilobite predators, anomalocaridids were
generalists occupying a range of ecological habits, from free-
swimming ambush predators to sediment-sifting scavengers.
The predatorprey relationship between Anomalocaris and
trilobites was formerly the best example of apex predation in
the Cambrian, and its removal suggests that ecological dynam-
ics in the Cambrian had not yet achieved a level of complexity
where highly specific prey exploitation was possible.
Acknowledgments We thank G. Budd and J-B. Caron for discussions.
Comments from G. Edgecombe, J. Esteve, B. Lieberman and an anony-
mous reviewer improved the manuscript. J. Dougherty provided access to
specimens at GSC and D. Erwin, J. Thompson and M. Florence provided
access to specimens at USNM. J-B. Caron and P. Fenton provided support
at the ROM. X. Ma is thanked for the photography of USNM specimens.
M. Stein provided photographs that led J.B. to this discovery. Burgess
Shale specimens were collected with permission from Parks Canada
Research (ROM, D. Collins, 1975 to 2000). Funding from the Swedish
Research Council and the Palaeontological Association to A. C. D is
gratefully acknowledged. This is Royal Ontario Museum Burgess Shale
Research Project 39.
References
Bergström J, Hou XG (2004) Arthropod origins. B Geosci 78:323334
Briggs DEG, Lieberman BS, Hendricks JR, Halgedahl SL, Jarrard RD
(2008) Middle Cambrian arthropods from Utah. J Paleontol
82:238254. doi:10.1666/06-086.1
Budd GE (1996) The morphology of Opabinia regalis and the recon-
struction of the arthropod stem-group. Lethaia 29:114.
doi:10.1111/j.1502-3931.1996.tb01831.x
Budd GE (1998) Stem group arthropods from the Lower Cambrian
Sirius Passet fauna of North Greenland. In: Fortey RA, Thomas RH
(eds) Arthropod relationships. Systematics Association Special
Volume, London, pp 125138
Chen JY, Ramsköld L, Zhou GQ (1994) Evidence for monophyly and
arthropod affinity of Cambrian giant predators. Science
264:13041308. doi:10.1126/science.264.5163.1304
Collins D (1996) The evolutionof Anomalocaris and its classifica-
tion in the arthropod class Dinocarida (Nov.) and order Radio-
donta (Nov.). J Paleontol 70:280293
Conway Morris S (1978) Laggania cambria Walcott: a composite
fossil. J Paleontol 52:126131
Daley AC, Budd GE (2010) New anomalocaridid appendages from the
Burgess Shale, Canada. Palaeontology 53:721738. doi:10.1111/
j.1475-4983.2010.00955.x
Daley AC, Budd GE, Caron J-B, Edgecombe GD, Collins D (2009)
The Burgess Shale anomalocaridid Hurdia and its significance for
early Euarthropod evolution. Science 323:15971600. doi:10.1126/
science.1169514
Edgecombe GD (2010) Arthropod phylogeny: an overview from the
perspectives of morphology, molecular data and the fossil record.
Arthropod Struct Dev 39:7487. doi:10.1016/j.asd.2009.10.002
Hagadorn JW (2009) Taking a bite out of Anomalocaris. Walcott 2009
International Conference on the Cambrian Explosion, abstract
volume, 3334.
Hagadorn JW (2010) Putting Anomalocaris on a soft-food diet? Geol
Soc Am Abstr Prog 42:320
Hou X, Bergström J, Ahlberg P (1995) Anomalocaris and other large
animals in the Lower Cambrian Chengjiang fauna of southwest
China. GFF 117:163183
Hou X, Bergström J, Jie Y (2006) Distinguishing anomalocaridids
from arthropods and priapulids. Geol J 41:259269
Lieberman BS (2003) A new soft-bodied fauna: the Pioche Formation
of Nevada. J Paleont 77:674690
Ma X, Hou X, Bergström J (2009) The morphology of Lulishania long-
icruris (Lower Cambrian, Chengjiang Lagerstätte, SW China) and
the phylogenetic relationships within lobopodians. Arthropod Struct
Dev 38:271291
Nedin C (1999) Anomalocaris predation on nonmineralized and min-
eralized trilobites. Geology 27:987990
Walcott CD (1911) Middle Cambrian holothurian and medusae. Smith
Misc Coll 57:4168
Whiteaves JF (1892) Description of a new genus and species of
Phyllocarid Crustacea from the Middle Cambrian of Mount Stephen.
BC Can Rec Sci 5:205208
Whittington HB, Briggs DEG (1985) The largest Cambrian animal
Anomalocaris, Burgess Shale, British Columbia. Philos T Roy
Soc B 390:569609
504 Naturwissenschaften (2012) 99:501504
  • ... 1d-i, S4a-c, 1l, S3c, d, S4f). Notably, the soft-bodied biotas from the middle Cambrian (Series 3) of Utah have yielded a large number of specimens previously identified as radiodontans in general, and usually Anomalocaris Whiteaves, 1892 or Peytoia Walcott, 1911 (Daley andBergstr?m, 2012) (e.g., Robison, 1982, 1988;Briggs and Robison, 1984;Robison, 1991;Briggs et al., 2008), but the systematic position of most of this material has not yet been reevaluated in light of the new discoveries on Hurdia. By analysis of appendages and mouthparts originally described by Conway Morris and Robison (1988), Daley et al. (2013a) were able to conclude that Hurdia was in fact present in the middle Cambrian (Series 3) of Utah alongside Peytoia, and they described four new specimens from the Spence Shale. ...
    ... The total number of smaller plates is not clear, as the outer edge of the oral cone is not well preserved, but where it can be counted there are seven smaller plates between the large plates, which extrapolates to a total of 32 plates, four large and 28 small, characteristic of Hurdia and Peytoia. By contrast, Anomalocaris mouthparts have three large plates at 120? (Daley and Bergstr?m, 2012). Peytoia mouthparts can be differentiated from Hurdia as Hurdia has numerous tooth rows in the central opening, whereas in Peytoia the central opening lacks tooth rows (Daley and Bergstr?m, 2012). ...
    ... By contrast, Anomalocaris mouthparts have three large plates at 120? (Daley and Bergstr?m, 2012). Peytoia mouthparts can be differentiated from Hurdia as Hurdia has numerous tooth rows in the central opening, whereas in Peytoia the central opening lacks tooth rows (Daley and Bergstr?m, 2012). In the central opening of this specimen, additional tooth rows are visible ('tr' in Fig. 3.3), indicating this specimen is a Hurdia. ...
    Preprint
    Radiodontan body elements, some belonging to Peytoia and Hurdia and some unassigned, have been reported from the Langston Formation (Spence Shale Member), Wheeler Formation, and Marjum Formation of the middle Cambrian (Series 3) of Utah. These identifications are reassessed in light of recent work on the morphology of the radiodontan Hurdia. New specimens of Hurdia are identified from the Spence Shale, representing mouthparts (oral cones), cephalic carapace H-elements, frontal appendages, and a single isolated swimming flap. The shape of the H-elements allows H. victoria Walcott, 1912 to be identified from the Spence Shale for the first time. The flap is larger and more complete than any reported from the Burgess Shale and allows for a better understanding of the morphology of Hurdia swimming flaps. A 3D model of a Hurdia frontal appendage indicates that there is only one morph of Hurdia frontal appendage found in both species, and apparent morphological differences between disarticulated appendages reflect a preservational continuum caused by varying oblique angles relative to the seafloor. Peytoia should no longer be reported from the Spence Shale, but its presence is confirmed in the Wheeler and Marjum formations. New mouthparts (oral cones) of Hurdia from the Spence Shale and Peytoia from the Marjum Formation with surface textures of submillimeter-diameter raised nodes are described. These new features have not been observed in material from the Burgess Shale and suggest slight differences in preservation.
  • ... Many Cambrian members of the iconic euarthro- pod stem-group known as radiodontans (Anomalo- caris and kin) have been viewed as giant apex preda- tors ever since their true body plan was revealed over 30 years ago [1][2][3]. However, more recent find- ings have shown that the body size of some early Palaeozoic radiodontans can range from 4 cm to over 200 cm in length [4][5][6] and that the highly variable frontal appendage morphologies are sugges- tive of a range of feeding modes, from shell-crushing to filter-feeding [6][7][8][9][10][11]. Lyrarapax from the early Cambrian Chengjiang Biota of China represents the smallest radiodontan taxon, with previously re- ported body sizes ranging from 4 to 8 cm in length [4,5]. ...
    ... Of the diverse radiodontan FA morphologies [5,6,8,10], those of amplectobeluids appear the best suited for grasping and manipulating prey, characterized by a proximal hypertrophied en- dite and a series of robust dorsal spines distally [4,5,8,[20][21][22] (Supplementary Fig. 3, available as Supplementary Data at NSR online). Lack of an articulation joint at the base of the hypertrophied endite indicates that it may have functioned as the rigid part of a 'claw', with the more flexible portion of the FA represented by the distal podomeres, thus permitting pincer-like capture of prey [2,8]. ...
    ... The variety of radiodontan feeding structures clearly points to these stem-group euarthropods having played key, often high-tier, trophic roles within early Palaeozoic food webs, including the consumption of zooplankton, as well as nektonic and benthic fauna [6,8,[10][11][12]16,20,37,38]. While certain taxa such as Anomalocaris [27] can still be considered giant apex predators of their time and capable of consuming large prey, the juveniles of some radiodontans like Lyrarapax ( Fig. 4 and Supplementary Fig. 6, available as Supplementary Data at NSR online) demonstrate that predation in the water column was occurring on a variety of scales during the Cambrian [10,37,[39][40][41]. ...
    Article
    Full-text available
    The rapid rise of arthropods during the Cambrian quickly established some clades, such as the euarthropod stem-group called Radiodonta, as the dominant and most diverse predators in marine ecosystems. Recent discoveries have shown that the size and dietary ecology of radiodontans is far more diverse than previously thought, but little is known about the feeding habits of juveniles. Here we document a very small (ca. 18-mm-long), near-complete specimen of the radiodontan Lyrarapax unguispinus from the early Cambrian Chengjiang Biota of China. This specimen is the smallest radiodontan individual known, representing a juvenile instar. Its adult-like morphology—especially the fully developed spinose frontal appendages and tetraradial oral cone—indicates that L. unguispinus was a well-equipped predator at an early developmental stage, similar to modern raptorial euarthropods, such as mantises, mantis shrimps, and arachnids. This evidence, coupled with the basal phylogenetic position of radiodontans, confirms that raptorial feeding habits in juvenile euarthropods appeared early in the evolutionary history of the group.
  • ... Based on these observations, it has been suggested that the head of these radiodontans terminates functionally and anatomically behind the protocerebral segment[5]. The mouth, another key component of the functional head of radiodontans, is located on the ventral side of the head region and consists of a radial oral cone that has been identified in almost all taxa known from articulated specimens, including Anomalocaris canadensis[17,21], Hurdia victoria[19,20]and Peytoia nathorsti[22]. The radial oral cone has thus been considered as a key diagnostic character of Radiodonta[23], distinguishing it from the upper stem group and crown group of Euarthropoda (Deuteropoda sensu Ortega-Hernández 2016[6]). ...
    ... These oral cones consist of four large semirectangular plates arranged perpendicular to one another, with seven smaller plates between them, surrounding a square or rectangular central opening. It was thought that this type of oral cone was consistently present in the then known radiodontan taxa[21,23], but recent research has shown that radiodontan mouthparts are actually highly variable[22]. Hurdia has the typical 32-plate oral cone, but with additional rows of spinose plates within the central opening[19,20]. Anomalocaris (including A. canadensis from the Burgess Shale[17,22], Anomalocaris sp. from the Emu Bay Shale[55], and A. saron from the Chengjiang Biota[27,28]) has been shown to have a flexible oral cone consisting of three large plates with variable numbers of smaller plates between them, all of which bear radially arranged furrows on their outer margins. ...
    ... Hurdia has the typical 32-plate oral cone, but with additional rows of spinose plates within the central opening[19,20]. Anomalocaris (including A. canadensis from the Burgess Shale[17,22], Anomalocaris sp. from the Emu Bay Shale[55], and A. saron from the Chengjiang Biota[27,28]) has been shown to have a flexible oral cone consisting of three large plates with variable numbers of smaller plates between them, all of which bear radially arranged furrows on their outer margins. The Chengjiang taxon Lyrarapax does not have an oral cone with plates, but instead has mouthparts consisting of concentric folds[13,18]. ...
    Article
    Full-text available
    Background: Segmental composition and homologies of the head of stem-group Euarthropoda have been the foci of recent studies on arthropod origins. An emerging hypothesis suggests that upper-stem group euarthropods possessed a three-segmented head/brain, including an ocular segment (protocerebrum) followed by the deutocerebrum with associated antennae/raptorial limbs and the tritocerebrum, while in the lower stem, head structures of Radiodonta are wholly associated with the protocerebrum and its preceding part. However, this hypothesis is incompletely tested because detailed knowledge on the head components of radiodontans is patchy, and informative articulated specimens are lacking for many taxa. Amplectobelua symbrachiata is the most common radiodontan species in the Chengjiang biota (ca. 520 Ma), normally known as isolated frontal appendages. Here we present detailed descriptions of new articulated specimens that elucidate the morphology and function of its head structures, and discuss their implications for hypotheses about euarthropod cephalic organisation. Results: In addition to a central oval head shield, A. symbrachiata also bears a pair of P-elements connected by an elongated rod. The mouth consists of sets of smooth and tuberculate plates, in contrast to the typical radial oral cones of other radiodontans. Previously identified ‘palm-like teeth’ are located external to the mouth in the posterior head region, and are interpreted as segmental gnathobase-like structures (GLSs) associated with at least three reduced transitional flaps in a one (pair)-to-one (pair) pattern, consistent with an appendicular nature. Comparisons with other panarthropods show that GLSs are morphologically similar to the mandibles and other gnathobasic mouthparts of euarthropods, as well as to the jaws of onychophorans, indicating their functional integration into the feeding activities of A. symbrachiata. Conclusions: The functional head of A. symbrachiata must include the reduced transitional segments (and their associated structures), which have been identified in several other radiodontans. This functional view supports the idea that the integration of segments (and associated appendages) into the head region, probably driven by feeding, occurred along the euarthropod stem-lineage. However, the number of reduced transitional segments varies between different groups and it remains uncertain whether GLSs represent proximal or distal parts of appendages. Our study is the first description of appendicular structures other than the frontal appendages in the functional head region of radiodontans, revealing novel feeding structures in the morphological transition from the lower- to the upper- stem-group of Euarthropoda.
  • ... Large and smaller plates can be distinguished in the oral cones, but their exact ar- rangements cannot be determined owing to incompleteness. The oral cones appear to have smooth outer margins that lack the subdivisions seen in the oral cone of Anomalocaris canadensis and the central margin shows no evidence of the extra rows of spiny plates of Hurdia victoria, making their overall configura- tion most similar to the oral cones of Peytoia nathorsti (Daley and Bergstr?m 2012). Indistinct carapace material may be preserved in close association with the disarticulated assemblages ( Fig. 2A). ...
    Preprint
    Full-text available
    As part of a comprehensive examination of all radiodontans from Cambrian localities in the USA, Pates et al. (2017a, b) and Pates and Daley (2017) revised the taxonomic affinities of several described specimens. This included the reinterpretation of two putative lobopodians, one from the Wheeler Formation (Utah, USA) and one from the Valdemiedes Formation (Spain), as frontal appendages of the radiodontan genera Stanleycaris and Caryosyntrips respectively. In their comment, Gámez Vintaned and Zhuravlev (2018) disagree with these conclusions and raise three topics for discussion: (i) anatomical features they suggest support a lobopodian affinity for “Mureropodia”; (ii) the identity of Caryosyntrips as a radiodontan, and the assignment of certain specimens to this genus; and (iii) the nomenclatural status of Stanleycaris hirpex as an invalid taxon. For (i), we dispute that the anatomical features put forward by Gámez Vintaned and Zhuravlev (2018) are biological and conclude that a lobopodian affinity for Mureropodia is untenable. In response to (ii), we provide further evidence supporting a radiodontan affinity for Caryosyntrips, and those specimens ascribed to this genus. Finally, we concur with (iii) Stanleycaris as an invalid taxon according to the International Code on Zoological Nomenclature (ICZN), and have rectified the situation by providing a valid systematic description.
  • ... Large and smaller plates can be distinguished in the oral cones, but their exact ar- rangements cannot be determined owing to incompleteness. The oral cones appear to have smooth outer margins that lack the subdivisions seen in the oral cone of Anomalocaris canadensis and the central margin shows no evidence of the extra rows of spiny plates of Hurdia victoria, making their overall configura- tion most similar to the oral cones of Peytoia nathorsti (Daley and Bergström 2012). Indistinct carapace material may be preserved in close association with the disarticulated assemblages ( Fig. 2A). ...
    Article
    Full-text available
    As part of a comprehensive examination of all radiodontans from Cambrian localities in the USA, Pates et al. (2017a, b) and Pates and Daley (2017) revised the taxonomic affinities of several described specimens. This included the reinterpretation of two putative lobopodians, one from the Wheeler Formation (Utah, USA) and one from the Valdemiedes Formation (Spain), as frontal appendages of the radiodontan genera Stanleycaris and Caryosyntrips respectively. In their comment, Gámez Vintaned and Zhuravlev (2018) disagree with these conclusions and raise three topics for discussion: (i) anatomical features they suggest support a lobopodian affinity for “Mureropodia”; (ii) the identity of Caryosyntrips as a radiodontan, and the assignment of certain specimens to this genus; and (iii) the nomenclatural status of Stanleycaris hirpex as an invalid taxon. For (i), we dispute that the anatomical features put forward by Gámez Vintaned and Zhuravlev (2018) are biological and conclude that a lobopodian affinity for Mureropodia is untenable. In response to (ii), we provide further evidence supporting a radiodontan affinity for Caryosyntrips, and those specimens ascribed to this genus. Finally, we concur with (iii) Stanleycaris as an invalid taxon according to the International Code on Zoological Nomenclature (ICZN), and have rectified the situation by providing a valid systematic description.
  • Article
    Full-text available
    Colour vision is known to have arisen only twice—once in Vertebrata and once within the Ecdysozoa, in Arthropoda. However, the evolutionary history of ecdysozoan vision is unclear. At the molecular level, visual pigments, composed of a chromophore and a protein belonging to the opsin family, have different spectral sensitivities and these mediate colour vision. At the morphological level, ecdysozoan vision is conveyed by eyes of variable levels of complexity; from the simple ocelli observed in the velvet worms (phylum Onychophora) to the marvellously complex eyes of insects, spiders, and crustaceans. Here, we explore the evolution of ecdysozoan vision at both the molecular and morphological level; combining analysis of a large-scale opsin dataset that includes previously unknown ecdysozoan opsins with morphological analyses of key Cambrian fossils with preserved eye structures. We found that while several non-arthropod ecdysozoan lineages have multiple opsins, arthropod multi-opsin vision evolved through a series of gene duplications that were fixed in a period of 35–71 million years (Ma) along the stem arthropod lineage. Our integrative study of the fossil and molecular record of vision indicates that fossils with more complex eyes were likely to have possessed a larger complement of opsin genes.
  • Article
    A recent description of paired gnathobase‐like structures (GLSs) in the head region of the radiodont Amplectobelua symbrachiata raised the question of whether these appendicular structures are more widely spread within Radiodonta, putative lower stem‐group euarthropods. Here we describe a new genus of Radiodonta, Ramskoeldia gen. nov., that also bears GLSs. Its two new species, Ramskoeldia platyacantha sp. nov. and R. consimilis sp. nov., are distinguished based on the morphology of their frontal appendages. The presence of three pairs of GLSs associated with reduced segments posterior to the head and the detailed morphological similarities of the GLSs suggest that Ramskoeldia is closely related to Amplectobelua Hou et al., and they are classified together in the revised Family Amplectobeluidae. Other diagnostic characters of this family include the lack of a radially‐arranged oral cone, instead sharing mouthparts composed of smooth and tuberculate plates, and a frontal appendage with three podomeres in the shaft and prominent larger endites on podomeres 4 and 8. Due to its lack of GLSs and the different morphology of its mouthparts, membership of Lyrarapax Cong et al., in Amplectobeluidae cannot be confirmed. Appraisal of available evidence indicates that the morphology of the feeding structures, including frontal appendages, the mouth apparatus, and GLSs, serves as a fundamental source of characters in the classification of radiodonts.
  • Article
    Full-text available
    Background: Chelicerata represents a vast clade of mostly predatory arthropods united by a distinctive body plan throughout the Phanerozoic. Their origins, however, with respect to both their ancestral morphological features and their related ecologies, are still poorly understood. In particular, it remains unclear whether their major diagnostic characters were acquired early on, and their anatomical organization rapidly constrained, or if they emerged from a stem lineage encompassing an array of structural variations, based on a more labile "panchelicerate" body plan. Results: In this study, we reinvestigated the problematic middle Cambrian arthropod Habelia optata Walcott from the Burgess Shale, and found that it was a close relative of Sanctacaris uncata Briggs and Collins (in Habeliida, ord. nov.), both retrieved in our Bayesian phylogeny as stem chelicerates. Habelia possesses an exoskeleton covered in numerous spines and a bipartite telson as long as the rest of the body. Segments are arranged into three tagmata. The prosoma includes a reduced appendage possibly precursor to the chelicera, raptorial endopods connected to five pairs of outstandingly large and overlapping gnathobasic basipods, antennule-like exopods seemingly dissociated from the main limb axis, and, posteriorly, a pair of appendages morphologically similar to thoracic ones. While the head configuration of habeliidans anchors a seven-segmented prosoma as the chelicerate ground pattern, the peculiar size and arrangement of gnathobases and the presence of sensory/tactile appendages also point to an early convergence with the masticatory head of mandibulates. Conclusions: Although habeliidans illustrate the early appearance of some diagnostic chelicerate features in the evolution of euarthropods, the unique convergence of their cephalons with mandibulate anatomies suggests that these traits retained an unusual variability in these taxa. The common involvement of strong gnathal appendages across non-megacheirans Cambrian taxa also illustrates that the specialization of the head as the dedicated food-processing tagma was critical to the emergence of both lineages of extant euarthropods-Chelicerata and Mandibulata-and implies that this diversification was facilitated by the expansion of durophagous niches.
  • Article
    Full-text available
    The Cambrian Explosion is arguably the most extreme example of a biological radiation preserved in the fossil record, and studies of Cambrian Lagerstätten have facilitated the exploration of many facets of this key evolutionary event. As predation was a major ecological driver behind the Explosion – particularly the radiation of biomineralising metazoans – the evidence for shell crushing (durophagy), drilling and puncturing predation in the Cambrian (and possibly the Ediacaran) is considered. Examples of durophagous predation on biomineralised taxa other than trilobites are apparently rare, reflecting predator preference, taphonomic and sampling biases, or simply lack of documentation. The oldest known example of durophagy is shell damage on the problematic taxon Mobergella holsti from the early Cambrian (possibly Terreneuvian) of Sweden. Using functional morphology to identify (or perhaps misidentify) durophagous predators is discussed, with emphasis on the toolkit used by Cambrian arthropods, specifically the radiodontan oral cone and the frontal and gnathobasic appendages of various taxa. Records of drill holes and possible puncture holes in Cambrian shells are mostly on brachiopods, but the lack of prey diversity may represent either a true biological signal or a result of various biases. The oldest drilled Cambrian shells occur in a variety of Terreneuvian-aged taxa, but specimens of the ubiquitous Ediacaran shelly fossil Cloudina also show putative drilling traces. Knowledge on Cambrian shell drillers is sorely lacking and there is little evidence or consensus concerning the taxonomic groups that made the holes, which often leads to the suggestion of an unknown ‘soft bodied driller’. Useful methodologies for deciphering the identities and capabilities of shell drillers are outlined. Evidence for puncture holes in Cambrian shelly taxa is rare. Such holes are more jagged than drill holes and possibly made by a Cambrian ‘puncher’. The Cambrian arthropod Yohoia may have used its frontal appendages in a jack-knifing manner, similar to Recent stomatopod crustaceans, to strike and puncture shells rapidly. Finally, Cambrian durophagous and shell-drilling predation is considered in the context of escalation – an evolutionary process that, amongst other scenarios, involves predators (and other ‘enemies’) as the predominant agents of natural selection. The rapid increase in diversity and abundance of biomineralised shells during the early Cambrian is often attributed to escalation: enemies placed selective pressure on prey, forcing phenotypic responses in prey and, by extension, in predator groups over time. Unfortunately, few case studies illustrate long-term patterns in shelly fossil morphologies that may reflect the influence of predation throughout the Cambrian. More studies on phenotypic change in hard-shelled lineages are needed to convincingly illustrate escalation and the responses of prey during the Cambrian.
  • Article
    The radiodontans, including anomalocaridids and their allies, are enigmatic stem-group euarthropods and are the most ancient apex giant predators known from the fossil record. Most studies on their feeding behaviors have emphasized their diverse and abundant raptorial frontal appendages, while the oral cone surrounding the mouth opening in these animals has attracted less attention. At present, three oral cone morphotypes are known, from Anomalocaris Whiteaves, 1892, Peytoia Walcott, 1911, and Hurdia Walcott, 1912, respectively. In this paper, we report on a novel form of radiodontan oral cone from the Guanshan Lagerstätte (Cambrian Series 2, Stage 4) in the Wulongqing Formation, eastern Yunnan, South China. This oral cone is unique in combining features seen in Peytoia / Hurdia and Anomalocaris . It possesses a Peytoia / Hurdia -type ‘tetraradial’ configuration comprising a 32-plate outer ring that consists of four perpendicularly arranged large plates and 28 small plates, in addition to furrowed folds and scale-like nodes on plate surfaces otherwise seen only in Anomalocaris . As an intermediate morphotype, the Guanshan oral cone improves our understanding of the occurrence and morphological disparity of radiodontan oral cones, illuminates future investigations on potentially variable radiodontan feeding mechanisms, and reveals possible evolutionary transformations of these peculiar feeding structures. The resolution of current radiodontan phylogeny would be potentially improved by new knowledge on other body parts apart from frontal appendages in future studies.
  • Article
    A new Burgess Shale-type soft-bodied fauna crossing the Lower-Middle Cambrian boundary in the Comet Shale Member of the Pioche Formation in Lincoln County, Nevada, contains common remains of soft-bodied ecdysozoan taxa. These fossils provide important new information about the nature and variety of Cambrian soft-bodied organisms. Arthropod taxa include one species of Canadaspis Novozhilov in Orlov, 1960, one species of ? Perspicaris Briggs, 1977, three species of Tuzoia Walcott, 1912, and at least two species of Anomalocaris Whiteaves, 1892. A priapulid referable to Ottoia Walcott, 1911a, was also recovered. A comprehensive review of Tuzoia is given. Some specimens from Early Cambrian sections are replaced by hematite, resulting in iron staining similar to that in such other Early Cambrian soft-bodied faunas as the Kinzers Formation in Pennsylvania. Some taxa in the Comet Shale, and in other Early and Middle Cambrian soft-bodied faunas, have prodigious geographic ranges that spanned much of Laurentia and even other Cambrian cratons. Moreover, these taxa ranged across the Early-Middle Cambrian boundary relatively unscathed. This is in contrast to many trilobite taxa that had narrow geographic ranges in the Early Cambrian and high levels of extinction at the Early-Middle Cambrian boundary.
  • Article
    The remarkable "evolution" of the reconstructions of Anomalocaris, the extraordinary predator from the 515 million year old Middle Cambrian Burgess Shale of British Columbia, reflects the dramatic changes in our interpretation of early animal life on Earth over the past 100 years. Beginning in 1892 with a claw identified as the abdomen and tail of a phyllocarid crustacean, parts of Anomalocaris have been described variously as a jellyfish, a sea-cucumber, a polychaete worm, a composite of a jellyfish and sponge, or have been attached to other arthropods as appendages. Charles D. Walcott collected complete specimens of Anomalocaris nathorsti between 1911 and 1917, and a Geological Survey of Canada party collected an almost complete specimen of Anomalocaris canadensis in 1966 or 1967, but neither species was adequately described until 1985. At that time they were interpreted by Whittington and Briggs to be representatives of "a hitherto unknown phylum." Here, using recently collected specimens, the two species are newly reconstructed and described in the genera Anomalocaris and Laggania, and interpreted to be members of an extinct arthropod class, Dinocarida, and order Radiodonta, new to science. The long history of inaccurate reconstruction and mistaken identification of Anomalocaris and Laggania exemplifies our great difficulty in visualizing and classifying, from fossil remains, the many Cambrian animals with no apparent living descendants.
  • Article
    Opabinia regalis Walcott is an enigmatic fossil from the Middle Cambrian Burgess Shale of uncertain affinities. Recent suggestions place it in a clade with Anomalacaris Whiteaves from the Burgess Shale and Kerygmachela Budd from the Greenlandic Sirius Passet Fauna; these taxa have been interpreted as 'lobopods'. Consideration of available Opabinia specimens demonstrates that reflective extensions from the axial region, previously thought to be either gut diverticula or musculature, can be accommodated in neither the trunk nor the lateral lobes that arise from it. They must therefore be external structures independent of the lateral lobes. On the basis of their sub-triangular appearance, size and taphonomy, they are considered here to represent lobopod limbs. Some evidence for the existence of terminal claws is also presented. The question of whether Kerygmachela, Opabinia and Anomalocaris constitute a monophyletic or paraphyletic grouping is considered. While they share several characters, most of these are plesiomorphies. Further, Opabinia and Anomalocaris share several arthropod-like characters not possessed by Kerygmachela. It is concluded that these three taxa probably form a paraphyletic grouping at the base of the arthropods. Retention of lobopod-like characters within the group provides important documentation of the lobopod-arthropod transition. A proper understanding of Opabinia and its close relatives, which may include the tardigrades, opens the way for a reconstruction of the arthropod stem-group. This in turn allows the construction of a speculative but satisfying scenario for the evolution of major arthropod features, including the origin of the biramous limb, tergites and arthropod segmentation. 'Arthropodization' may thus be seen not to be a single event but a series of adaptive innovations.
  • Chapter
    Discussion of fossil evidence for the origin and early evolution of the arthropods has been dominated for many years by the evidence from the Middle Cambrian Burgess Shale from British Columbia (Whittington, 1979; Gould, 1989). What these fossils mean, however, both in terms of arthropod classification and the early evolution of the phylum is far from clear: no single opinion has won universal assent. In addition, the Burgess Shale has also yielded some celebrated problematica such as Opabinia (Whittington, 1975), Anomalocaris (Whittington and Briggs, 1985; Collins, 1996) and Hallucigenia (Conway Morris, 1977; Ramsköld and Hou, 1991). No one would dispute that these fossils are problematic, in the sense that they are difficult to understand. However, that methodological difficulty should not be confused with the possibility that these fossils have only remote affinities with all living groups. The sense that these fossils can indeed be understood has strengthened in recent years with the discovery of several more important Cambrian fossil localities.
  • Article
    Full-text available
    The Middle Cambrian Spence Shale Member (Langston Formation) and Wheeler and Marjum Formations of Utah are known to contain a diverse soft-bodied fauna, but important new paleontological material continues to be uncovered from these strata. New specimens of anomalocaridids include the largest and smallest near complete examples yet reported from Utah. New material of stem group arthropods includes two new genera and species of arachnomorphs: Nettapezoura basilika and Dicranocaris guntherorum. Other new arachnomorph material includes a new species of Leanchoilia comparable to L. protogonia Simonetta, 1970; Leanchoilia superlata? Walcott, 1912; Sidneyia Walcott, 1911 a; and Mollisonia symmetrica Walcott, 1912. L. protogonia from the Burgess Shale is confirmed as a separate species and is not a composite fossil. The first example of the trilobite Elrathia kingii preserving traces of the appendages is described. In addition, new material of the bivalved arthropods Canadaspis Novozhilov in Orlov, 1960; Branchiocaris Briggs, 1076; Waptia Walcott, 1912; and Isoxys Walcott, 1890 is described.
  • Article
    A new Burgess Shale-type soft-bodied fauna crossing the Lower-Middle Cambrian boundary in the Comet Shale Member of the Pioche Formation in Lincoln County, Nevada, contains common remains of soft-bodied ecdysozoan taxa. These fossils provide important new information about the nature and variety of Cambrian soft-bodied organisms. Arthropod taxa include one species of Canadaspis Novozhilov in Orlov, 1960, one species of ?Perspicaris Briggs, 1977, three species of Tuzoia Walcott, 1912, and at least two species of Anomalocaris Whiteaves, 1892. A priapulid referable to Ottoia Walcott, 1911a, was also recovered. A comprehensive review of Tuzoia is given. Some specimens from Early Cambrian sections are replaced by hematite, resulting in iron staining similar to that in such other Early Cambrian soft-bodied faunas as the Kinzers Formation in Pennsylvania. Some taxa in the Comet Shale, and in other Early and Middle Cambrian soft-bodied faunas, have prodigious geographic ranges that spanned much of Laurentia and even other Cambrian cratons. Moreover, these taxa ranged across the Early-Middle Cambrian boundary relatively unscathed. This is in contrast to many trilobite taxa that had narrow geographic ranges in the Early Cambrian and high levels of extinction at the Early-Middle Cambrian boundary.
  • Article
    The giant Cambrian form Anomalocaris is considered to have been a raptoral predator of trilobites. However, doubt has been raised about its ability to successfully predate on strongly biomineralized forms (durophagy). A specimen of the trilobite Naraoia from the Early Cambrian Emu Bay Shale of South Australia represents the earliest direct body fossil evidence of predation on nonbiomineralized individuals. Analysis of arthropod cuticle rheology and examination of the injuries inflicted on this specimen suggest that Anomalocaris was the predator. It appears that some anomalocaridids actively utilized their large frontal appendages to rapidly flex trilobites during predation. Comparison with predation damage from mineralized trilobites and coprolites suggests that this method of flexing allowed durophagous predation. The presence in the Early Cambrian of durophagous, nonbiomineralized predators may have important implications for the role of predation pressure in the acquisition of mineralized cuticles and the rise of enrollment in trilobites. Variation in the frontal appendages of anomalocaridids indicates that niche partitioning within the genus was well established by the late Early Cambrian.