The oral cone of Anomalocaris is not a classic ‘‘peytoia’’
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- Daley, A.C. & Bergström, J. Naturwissenschaften (2012) 99: 501. doi:10.1007/s00114-012-0910-8
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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.
KeywordsAnomalocaridids Cambrian Oral cone Peytoia Predation Burgess Shale
Anomalocaridids are some of the more controversial taxa described from Cambrian fossil Lagerstätten, being characterized 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 arthropods (see Edgecombe (2010) for review).
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.
Materials and methods
A total of 44 specimens from the Royal Ontario Museum (ROM 51213, 51215–51216 and 61642–61680), Geological Survey of Canada (GSC 75535) and Smithsonian National Museum of Natural History (USNM 189024) were examined. 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 photographed 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
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. 2g–i) 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. canadensis 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. 3–6, 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. 5.1 of Collins 1996). Collins (1996, Fig. 5.1) illustrated ROM 51215 as a mouth cone belonging to A. canadensis but neither noted its triradial symmetry (Fig. 2b–d) nor showed the accompanying appendages (Fig. 2a) and partial body. Additionally, 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 centimeters (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 (Daley and Budd 2010). Three isolated specimens of Anomalocaris-type mouthparts have also been recognized, one of which is well-preserved and complete (Fig. 2j).
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; Chen et al. 1994), and this second taxon has been called L. cambria (Collins 1996; Daley et al. 2009; Daley and Budd 2010), P. nathorsti (Chen et al. 1994; Hou et al. 2006) and Laggania nathorsti (Briggs et al. 2008). As the specimen used to identify P. nathorsti 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 Anomalocaris from Peytoia (Collins 1996). It is now unclear if differences 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 20–24 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 Anomalocaris saron (Fig. 6 of Hou et al. 1995). The only other published specimen of an A. saron oral cone (Figs. 8.1 and 9 of Lieberman 2003) 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. canadensis, is actually poorly known. A clearer picture of anomalocaridid 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; Ma et al. 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 Anomalocaris suggests that Cambrian anomalocaridid taxa were employing a variety of different feeding strategies, corroborating what has also been shown from frontal appendages (Daley and Budd 2010). Anomalocaris was previously considered as the highly specialized predator responsible for W-shaped “bite marks” in 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 unsuitable 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 predator–prey relationship between Anomalocaris and trilobites was formerly the best example of apex predation in the Cambrian, and its removal suggests that ecological dynamics in the Cambrian had not yet achieved a level of complexity where highly specific prey exploitation was possible.
We thank G. Budd and J-B. Caron for discussions. Comments from G. Edgecombe, J. Esteve, B. Lieberman and an anonymous 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.