Nature | Letter

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A giant Ordovician anomalocaridid

Journal name:
Nature
Volume:
473,
Pages:
510–513
Date published:
(26 May 2011)
DOI:
doi:10.1038/nature09920
Received
Accepted
Published online

Anomalocaridids, giant lightly sclerotized invertebrate predators, occur in a number of exceptionally preserved early and middle Cambrian (542–501 million years ago) biotas and have come to symbolize the unfamiliar morphologies displayed by stem organisms in faunas of the Burgess Shale type. They are characterized by a pair of anterior, segmented appendages, a circlet of plates around the mouth, and an elongate segmented trunk lacking true tergites with a pair of flexible lateral lobes per segment1, 2. Disarticulated body parts, such as the anterior appendages and oral circlet, had been assigned to a range of taxonomic groups—but the discovery of complete specimens from the middle Cambrian Burgess Shale showed that these disparate elements all belong to a single kind of animal3. Phylogenetic analyses support a position of anomalocaridids in the arthropod stem, as a sister group to the euarthropods4, 5, 6. The anomalocaridids were the largest animals in Cambrian communities. The youngest unequivocal examples occur in the middle Cambrian Marjum Formation of Utah7 but an arthropod retaining some anomalocaridid characteristics is present in the Devonian of Germany5. Here we report the post-Cambrian occurrence of anomalocaridids, from the Early Ordovician (488–472 million years ago) Fezouata Biota8 in southeastern Morocco, including specimens larger than any in Cambrian biotas. These giant animals were an important element of some marine communities for about 30 million years longer than previously realized. The Moroccan specimens confirm the presence of a dorsal array of flexible blades attached to a transverse rachis on the trunk segments; these blades probably functioned as gills.

Subject terms:

Main

Anomalocaridids were first described from the middle Cambrian of Mount Stephen in British Columbia, Canada9. The specimens, which consisted of isolated raptorial appendages, were interpreted as the body of a shrimp9. A different raptorial appendage from the middle Cambrian Burgess Shale was subsequently misinterpreted by Walcott as that of the arthropod Sidneyia3, 10. Walcott interpreted the oral circlet as a medusoid and also described an incomplete specimen of the body as a holothurian11. The carapace elements of the anomalocaridid Hurdia also were misidentified originally—as two different arthropods6, 12, 13. The first reconstruction of an anomalocaridid based on complete specimens dates from the 1980s2, 3. As a result of discoveries from other Cambrian localities worldwide, it was largely accepted by the mid-1990s that anomalocaridids are arthropods1. Some authors, however, continued to argue for non-arthropodan affinities14 and the exact systematic placement of the group remained uncertain. Although inclusion of anomalocaridids in the arthropod crown has been favoured by some15, they are generally regarded as belonging in the euarthropod stem4, 5, 6, 16.

Anomalocaridids are known from early and middle Cambrian sites in Canada, the United States, Poland, Russia, China, Australia and, possibly, Greenland and the Czech Republic6, 7, 16, 17, 18, 19, 20. The oldest known example is Cassubia infercambriensis from the early Cambrian of Poland16, while the youngest are from the middle Cambrian of the United States7; a single specimen from the late Cambrian of the Holy Cross Mountains in Poland may represent an oral circlet21. It has been suggested that the Early Ordovician Pseudoangustidontus duplospineus might represent an anomalocaridid spine22 or a complete grasping appendage20. Its morphology, however, differs from an anomalocaridid spine20, and its unsegmented, sclerotized nature is inconsistent with an anterior appendage22. Schinderhannes bartelsi from the Lower Devonian Hunsrück Slate retains some anomalocaridid characters, including a circular mouth and anterior raptorial appendages, but clearly lies crownward as a sister taxon to the euarthropods5.

The Fezouata Biota preserves a fully marine Burgess Shale fauna in combination with more advanced taxa8, 23. The anomalocaridid specimens are associated with a diverse fauna8 and were recovered from five excavations north of Zagora, in southeastern Morocco. Excavations 1 and 2 are approximately coeval, and sit just below the boundary between the Lower and Upper Fezouata Formations; they are latest Tremadocian in age. The remaining excavations are slightly younger, but all three occupy approximately the same stratigraphic level: they sit at the base of the Upper Fezouata Formation, dating them to the earliest Floian (Supplementary Fig. 1).

The Fezouata anomalocaridids occur in two distinct preservational styles. Smaller specimens, like the majority of Fezouata fossils8, 23, are flattened in the mudstones and preserved in pyrite weathered to iron oxides. Larger specimens occur in massive concretions, dominated by authigenic silica, in close proximity to each other within the mudstones. The composition of the fossils indicates weathered pyrite, but a significant proportion of manganese is present. Concretion formation was probably the result of the rapid decay of a large amount of organic material (large trilobites are also preserved in this way24). The concretions provided a degree of protection from compaction, so that the trunk retains some convexity and the lateral lobes project at a high angle.

The large anomalocaridid specimens were collected at Excavation 1. They comprise articulated bodies but they lack most or all of the head region. The most complete specimen (Fig. 1a–c, Supplementary Fig. 2) preserves the posterior margin of the head and a trunk of 11 segments; there is no evidence of tergites. The maximum preserved length and width (excluding lateral lobes) of this fossil (Fig. 1a) are respectively ~915 mm and ~295 mm. Specimens YPM 226438 and YPM 226439 (Supplementary Fig. 3a, b) are less complete, but their trunks attain a comparable width, indicating that they were of similar size. The segments are approximately equal in length except for the posteriormost 3 or 4, which become progressively shorter where the trunk tapers to a blunt end. They are covered by long, flexible blade-like structures, more than 100 in the widest segments, oriented parallel or slightly oblique to the axis of the trunk (Fig. 1a, b, Supplementary Figs 2, 3a). They are interpreted as covering the dorsal surface of the segments, based on the position of similar structures in Laggania14, 25, 26. Their attitude may be straight to gently curved or even sinuous; they run parallel to each other with limited overlap, except where they are folded and distorted in the incomplete terminal body segment of YPM 226437 (Supplementary Fig. 2c, d). There is no evidence that the blades continue laterally across the small triangular, flexible lobes that project from the ventro-lateral margin of the trunk (Fig. 1a–c; Supplementary Figs 2a, b, 3a, b); their exact relationship to the base of the lobes is unclear. Only the most proximal part of the lobes is clearly preserved; narrow closely spaced rays run parallel to the axis (Fig. 1c, Supplementary Fig. 3b).

Figure 1: Anomalocaridid specimens from the Lower Ordovician Fezouata formations.
Anomalocaridid specimens from the Lower Ordovician Fezouata formations.

Drawings by camera lucida of the specimens are provided in Supplementary Fig. 4. a–c, Giant, near-complete specimen preserved in a concretion, dorsal side exposed, Excavation 1 (YPM 226437). a, Entire specimen. b, Segments 5 and 6 showing blades. c, Right lobes 5 and 6 showing rays. d, Left lateral ‘P-element’ of carapace, part, Excavation 2 (YPM 227518). e–i, Central ‘H-element’ of carapace, Excavation 2 (YPM 227517). e, Part showing evidence of a healed injury, posterior right. f, Counterpart. g, Reticulate structure on the anterior right of the part. h, Coarse tubercles on the mid-posterior of the part. i, Fine tubercles on the counterpart. j, Fragment of gill, part, Excavation 2 (YPM 227934). k, Incomplete oral circlet, part, Excavation 3 (YPM 227643). l, Great appendage, part, Excavation 5 (YPM 227644).

Smaller individuals were represented in the Fezouata Formation at other excavations (Supplementary Fig. 1). Excavation 2 yielded an elongate valve-like sclerite (41 mm long including spines), with a robust triangular projection at one end and a long slender pointed projection at the other (Fig. 1d, Supplementary Fig. 4c). A sub-triangular sclerite (Fig. 1e–i, Supplementary Fig. 4b, c), 32 mm long, was found at the same excavation. It preserves a reticulate structure on the part (Fig. 1e, g) but not on the counterpart (Fig. 1f): this may be an internal feature of the cuticle revealed by exfoliation. Coarse tubercles are scattered in the posterior half (Fig. 1e, h) and fine tubercles are closely spaced elsewhere (Fig. 1i).

Excavation 2 also yielded a relatively broad jointed rachis about 15 mm long, to which long, flat, blunt-tipped, overlapping flexible blades are attached, one on each podomere (Fig. 1j, Supplementary Fig. 4d). These structures are similar to those on the segments of the largest specimens (Fig. 1a, b; Supplementary Figs 2, 3a). Two less well-preserved fragments of similar morphology were also recovered from the slightly younger Excavation 4.

An incomplete oral circlet consisting of one major and two minor plates (Fig. 1k, Supplementary Fig. 4e) was found at Excavation 3. The major plate (preserved length ~13 mm) shows two narrow radial strengthening ridges; only one wider ridge is present on the minor plates. The teeth were broken away as the shale was split to reveal the fossil. Extrapolation suggests a diameter of the complete circlet of slightly more than 30 mm.

Two specimens of a great appendage were also recovered. The number of podomeres and the morphology of the spines indicates that they belong to an anomalocaridid. The larger specimen from Excavation 5 (preserved length ~34 mm along the curve) is incomplete at both ends, but preserves evidence of 9 podomeres (Fig. 1l, Supplementary Fig. 4f). A distal spine on the dorsal side is small and more dorsally directed on the more proximal podomeres; these spines become more robust and near parallel to the appendage on successively distal podomeres. A very robust, slightly recurving, long spine projects ventrally from the mid-length of the more proximal podomeres but may have been absent from the distalmost four. This ventral spine terminates in a curved point, and bears five or six secondary spines along its proximal length. A fine bundle of spines or setae is associated with the proximal part of this larger specimen but it is not known whether this is simply a chance association. A smaller specimen from Excavation 3 (preserved length ~16 mm along the curve) comprises 10 or 11 podomeres (Supplementary Fig. 3c, d); ventral spines appear to be present only on the median 4 podomeres.

In summary, the large articulated bodies all derive from Excavation 1, whereas the small carapace elements were found at an adjacent site of similar age (Excavation 2) together with a fragment of rachis with blades. Blade-like structures were collected from the younger Excavation 4 whereas the similar aged Excavations 3 and 5 yielded raptorial appendages, associated with a partial oral circlet at Excavation 3. It is unclear whether the Moroccan specimens represent more than one type of anomalocaridid: a formal description awaits the discovery of more material.

The blade-like structures on the surface of the segments and in the fragmentary specimens are similar to those in Hurdia and Laggania6, and may be comparable to the blades in Opabinia27. A transverse arrangement of blades across the trunk similar to that in the large Moroccan specimens has been described and reconstructed on the dorsal surface of Laggania14, 25, 26. The attachment of the blades to a rachis is similar to the arrangement in Hurdia, and the transverse mineralized structures in Laggania may be homologous. The lateral lobes show rays, as observed in Laggania. The carapace elements are strikingly similar to the central ‘H-element’ and lateral ‘P-element’ that make up the tripartite Hurdia headshield6. Although they differ in outline from those typical of Hurdia victoria from the Burgess Shale, the H-element preserves an internal reticulate structure similar to that in Hurdia sclerites6. The great appendages resemble morph B in Hurdia6 although they differ in detail.

The specimens from Excavation 1 represent the largest articulated anomalocaridid specimens known, and even though the size of the head is unknown, it is likely that the largest Moroccan individual was significantly larger than its Burgess Shale counterparts3. These anomalocaridids are rivalled in size among arthropods only by pterygotid eurypterids28 and the terrestrial arthropleurids29 (although extrapolation based on remains of the oral circlet from the early Cambrian Chengjiang biota of China1 has been used to infer an even larger anomalocaridid, these estimates are uncertain14). They dwarf the other organisms known from the Fezouata Biota: the largest trilobites are nileids, asaphids and dikelokephalinids, which reach a maximum of ~30 cm (ref. 24), less than 30% of the length of the anomalocaridids.

Like other anomalocaridids, the Moroccan examples are assumed to have been swimming predators. The great appendages seem to be adapted to entrap prey and to help to transfer it to the mouth. No biomineralized organisms with injuries compatible with the anomalocaridid oral circlet have been recovered from the Fezouata formations, but it is likely that the Moroccan anomalocaridids, like their Cambrian predecessors, fed mostly on unmineralized organisms3. The size and associated food requirements of the largest Fezouata individuals might imply low population densities. The association of at least five individuals in close proximity at Excavation 1 may indicate an abundant food source, or congregation for some other purpose, such as moulting or mating.

The most striking feature of the Moroccan specimens, apart from their size, are the series of dorsal blades. These specimens provide the most compelling evidence yet that such structures traversed the entire trunk of some anomalocaridid taxa19, 25, 26. They do not resemble scales25 and their interpretation as gills is more plausible, even if their unprotected position is anomalous. There is no sign of any separation of the left and right halves as in Hurdia6. While the blades may originate as exites6, the rachis to which they connect appears to be attached across the dorsal width of the trunk in the middle of the intersegment areas in a manner unknown in euarthropods; it is unclear whether the rachis also attached to the base of the lobes. If the function of the blades was respiratory, they may reflect low oxygen conditions or the high oxygen requirement of a large active swimmer; their dorsal position would have assured continued oxygenation when in close proximity to anoxic bottom conditions.

The Fezouata discoveries extend the range of unequivocal anomalocaridids by about 30 million years ago, from the middle Cambrian to the Early Ordovician, and provide the only temporal link between the Cambrian occurrences and the Early Devonian great appendage arthropod Schinderhannes, which retains some anomalocaridid characters5. The Moroccan occurrences show that anomalocaridids were the largest organisms in some ecosystems even in the Ordovician, and were presumably at the top of the food chain. With the exception of the singular Polish and possible Czech occurrences, which are from intermediate and polar palaeolatitudes respectively, all Cambrian anomalocaridid localities are situated in the palaeotropics. The Fezouata formations, in contrast, were deposited at a high polar southern palaeolatitude, confirming a global distribution of anomalocaridids, at least latitudinally, during the early Palaeozoic, as observed for many other taxa of Burgess Shale type8. The demise of anomalocaridids may have been associated with the diversification of large predatory eurypterids and stem cephalopods during the Great Ordovician Biodiversification Event30.

Methods

All figured specimens are housed in the collections of the Yale Peabody Museum of Natural History. Locality details are kept at the Museum, and can be provided on request. Small specimens were prepared with scalpels and fine needles under high magnification using Leica MZ6 and MZ16 stereomicroscopes and, when necessary, repaired using cyanoacrylate glue. The large specimens were prepared with the aid of fine chisels and electric engravers, and assembled using cyanoacrylate glue and epoxy. Interpretative drawings were made with a camera lucida attached to a Leica MZ6 stereomicroscope. Photographs of the large specimens were made with a Canon EOS 300D digital reflex camera with a Sigma EX 50 mm f 2.8 DG macro lens stopped down to f5 for maximum sharpness, while smaller specimens were imaged using a Leica MZ16 stereomicroscope with Leica DFC 425 digital camera. All photographs were taken with crossed polarizers, and, in addition, the specimen in Supplementary Fig. 3c was photographed under ethanol. Digital photographs were processed in Adobe Photoshop CS2 and CS3. To maximize depth of field, between 10 and 30 images were stacked using CombineZP and Helicon Focus Pro software. Figures 1a, b, d, e, f, j, l and Supplementary Figs 2a, c, and 3a are composite images, stitched together using Adobe Photoshop CS3 and Microsoft ICE. Elemental composition was analysed in a Philips XL 30 environmental scanning electron microscope (ESEM) equipped with an energy dispersive X-ray analyser (EDX).

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Acknowledgements

S. Butts (Yale Peabody Museum of Natural History) provided access to specimens. M. Ben Said Ben Moula originally discovered the specimens and made them available for study; he, together with J. P. Botting-Muir and L. A. Botting-Muir, P. J. Orr, C. Upton and J. Vinther also assisted with fieldwork, and B. Tahiri arranged logistical support. J. W. Hagadorn shared information on anomalocaridid size and R. R. Gaines discussed aspects of the taphonomy. E. Champion helped with the preparation of figures. This research was supported by a National Geographic Society Research and Exploration grant and by Yale University.

Author information

Affiliations

  1. Department of Geology and Geophysics, Yale University, PO Box 208109, New Haven, Connecticut 06520, USA

    • Peter Van Roy &
    • Derek E. G. Briggs

  2. Research Unit Palaeontology, Department of Geology and Soil Science, Ghent University, Krijgslaan 281/S8, B-9000 Ghent, Belgium

    • Peter Van Roy

  3. Yale Peabody Museum of Natural History, Yale University, New Haven, Connecticut 06520, USA

    • Derek E. G. Briggs

Contributions

The authors contributed equally to interpreting the fossils and writing the paper. P.V.R. played the primary role in field work, and prepared, photographed and drew the specimens.

Competing financial interests

The authors declare no competing financial interests.

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