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The Burgess Shale Anomalocaridid Hurdia and Its Significance for Early Euarthropod Evolution

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Science  20 Mar 2009:
Vol. 323, Issue 5921, pp. 1597-1600
DOI: 10.1126/science.1169514

Abstract

As the largest predators of the Cambrian seas, the anomalocaridids had an important impact in structuring the first complex marine animal communities, but many aspects of anomalocaridid morphology, diversity, ecology, and affinity remain unclear owing to a paucity of specimens. Here we describe the anomalocaridid Hurdia, based on several hundred specimens from the Burgess Shale in Canada. Hurdia possesses a general body architecture similar to those of Anomalocaris and Laggania, including the presence of exceptionally well-preserved gills, but differs from those anomalocaridids by possessing a prominent anterior carapace structure. These features amplify and clarify the diversity of known anomalocaridid morphology and provide insight into the origins of important arthropod features, such as the head shield and respiratory exites.

Like other anomalocaridids (1), Hurdia has a complex history. The mouthparts (2), frontal appendages (35), body (6), and frontal carapaces (7, 8) were all first described in isolation as separate animals with disparate affinities, including medusoids, holothurians, and various arthropods (1). When research in the 1980s revealed that many of these taxa were in fact different parts of the same animal, two anomalocaridid genera were defined (9), and several specimens here identified as Hurdia were assigned to either Anomalocaris or Laggania. These genera possess stalked eyes, frontal appendages, a circular toothed mouth structure, and a body bearing gills in association with lateral flaps. Later, Collins (10, 11) informally recognized that a third undescribed anomalocaridid exhibits all these features, as well as a prominent anterior carapace composed of a triangular element, the Hurdia carapace (7), together with the purported phyllopod carapace Proboscicaris (8).

Access to important new material at the Royal Ontario Museum and restudy of older collections (12) identified parts of the Hurdia animal scattered through at least eight Cambrian taxa. This realization clarifies the systematics and complex morphology of Burgess Shale anomalocaridids, revealing that previous reconstructions of Anomalocaris and Laggania have been partially misled by the inclusion of Hurdia material. For clarity, generic names previously applied to anomalocaridid body parts are referred to as follows: “Hurdia” (7) is referred to as the H-element, “Proboscicaris” (8) as the P-element (with both together as the frontal carapace), “Peytoia” (2) as the mouthpart, and “appendage F” (35) as frontal appendage.

Systemic paleontology. Stem Euarthropoda, Class Dinocarida, Order Radiodonta, Genus Hurdia Walcott, 1912. Synonymy and taphonomy. See supporting online material (SOM) text. Type species. Hurdia victoria Walcott, 1912. Revised diagnosis. Anomalocaridid with body divided into two components of subequal length: anterior with a nonmineralized reticulated frontal carapace and posterior consisting of a trunk with seven to nine lightly cuticularized segments. The frontal carapace includes a triangular H-element attached dorsally and a pair of lateral P-elements. Posterior to the frontal carapace is a pair of dorsolateral oval eyes on short annulated stalks. The anteroventral mouthparts consist of an outer radial arrangement of 32 broadly elliptical plates (similar to Laggania and Anomalocaris) forming a domed structure, within which is found a maximum of five inner rows of teeth (lacking in Laggania and Anomalocaris). A pair of appendages is located on either side of the mouthparts, consisting of 9 or 11 podomeres each, bearing short dorsal spines and long spiniferous ventral spines. The posterior half of the body consists of seven to nine reversely imbricated lateral flaps bearing a series of wide lanceolate gill-like blades. The body lacks a posterior tapering outline and tail fan (in contrast to Laggania and Anomalocaris), and the terminal body segment has two small lobe-shaped outgrowths. Holotype of the type species. U.S. National Museum of Natural History (USNM) specimen no. 57718, Washington, DC, USA. Paratypes. USNM 274159 and counterpart in two pieces (274155 and 274158). Royal Ontario Museum (ROM) 59252, 49930, 59254, and 59255, Toronto, Canada. Other material. At least 732 Hurdia specimens (12) from the ROM; National Museum of Natural History (NMNH); Geological Survey of Canada (GSC), Ottawa; and Museum of Comparative Zoology (MCZ), Harvard University (table S1). Horizons and localities. Middle Cambrian Burgess Shale Formation (13) (Fossil Ridge, Mount Field, and Mount Stephen); Yoho National Park; and Middle Cambrian Stephen Shale Formation (Stanley Glacier), Kootenay National Park, British Columbia, Canada.

Description. Specimens are up to 200 mm in length (table S2), with the frontal carapace making up approximately half of the total body length (Fig. 1). The P-elements (Fig. 2F) lie beneath the lateral margins of the dorsal H-element (Fig. 2G) and were attached at their anteriorly pointing narrow protrusions beneath the H-element's rostral point (Fig. 3). H- and P-elements have a polygonal pattern (fig. S1D) formed by thin walls between outer cuticle layers (SOM text). Short annulated stalks bearing oval eyes protruded through posterior notches in the frontal carapace (Figs. 1, A and B, and 3).

Fig. 1.

H. victoria from the Burgess Shale, paratype specimens. (A) USNM 274159, dorsolateral specimen previously described as Emeraldella brocki (6) and Anomalocaris nathorsti (9). (B) Camera lucida drawing of USNM 274159. (C) ROM 59252, specimen is in dorsal view. (D) Camera lucida drawing of ROM 59252. Scale bars, 1 cm. ag, anterior gills; b, burrow; m, mouthparts; Ey, eye; F, frontal appendage; g, gill; H, H-element; l, left; L, lateral flap and associated gill; r, right; Re, reticulated structure; P, P-element; S, eye stalk; T, tail lobe; V, mineral vein.

Fig. 2.

Paratype specimen and isolated components of H. victoria. (A) ROM 49930, paratype, lateral view showing lateral flaps. (B) ROM 59258, frontal appendage morph A. (C) ROM 59259, frontal appendage morph B. (D) ROM 59260, mouthpart with extra teeth rows. (E) ROM 59261, lanceolate gill blades showing attachment at one end (arrow). (F) ROM 59262, paired P-elements. (G) USNM 57718, holotype of H. victoria. Scale bars, 1 cm. Abbreviations are as in Fig. 1. B, Banffia; ex, extra teeth rows.

Fig. 3.

Reconstruction of H. victoria. [Drawing by M. Collins, 2008 © ROM/J. B. Caron]

Mouthparts consist of a circlet of 32 plates, each bearing two or three small teeth, with four larger plates arranged perpendicularly and separated by seven smaller plates (Fig. 2D and fig. S1, D and E). The outer margins of these plates curve downward, conferring a domed shape to the structure best seen in lateral view (fig. S1A). Within the square central opening are situated five imbricated rows of teeth bearing as many as 11 sharp spines (Fig. 2D and fig. S2, D and E). All domed mouth parts with inner teeth belong to Hurdia (SOM text).

The frontal appendages of Hurdia specimens consist either of 11 robust podomeres with one dorsal spine, three lateral spines, and five elongated ventral spines (Fig. 2B and fig. S2E), or they have nine thinner podomeres with single dorsal spines, no lateral spines, and seven elongated ventral spines (Fig. 2C and fig. S2C). Both appendage types are unquestionably associated with definite Hurdia elements, suggesting the existence of two morphs or species.

The trunk of the Hurdia body consists of seven to nine poorly delimited segments of roughly equal width (Figs. 1 and 2). Each segment bore a pair of lateral flaps covered by smooth cuticle (Fig. 3), which were overlain by thin lanceolate structures arranged in series (Fig. 2E and fig. S2, C and H), interpreted to be gills. The lanceolate structures were attached to the anterior margins of the lateral flaps and were free-hanging posteriorly (fig. S2, C and H). Lateral flaps and gills are arranged in reverse imbrication. Four pairs of smaller lanceolate structures surround the mouthparts and frontal appendages (Figs. 1, A and B, and 3).

Discussion. Hurdia is the most common anomalocaridid in at least the Walcott Quarry. It occurs in six Burgess Shale localities in the Canadian Rockies, representing six members and two formations (table S1), as well as in Utah (14), Bohemia (15), and possibly Nevada (16) and China (17), suggesting that Hurdia was a generalist adapted to a range of environmental conditions (18). Its cephalic carapace structure is unique in its composition and anterior position relative to the rest of the body. Such a complex anterior structure finds no convincing analogs in any living or fossil arthropod. This position of the frontal carapace is probably original and not the product of postmortem displacement or moult configurations (SOM text). Like other anomalocaridids (9), Hurdia was likely an active nektobenthic animal, probably a predator or scavenger. The less robust morphology of the frontal appendages of Hurdia suggests that it may have been exploiting different prey sources than Anomalocaris.

Anomalocaridids have been variously regarded as stem- (19, 20) or crown- (21, 22) group euarthropods, as a sister group to arthropods in the broad sense (23, 24), or within the cycloneuralian worms (25). The phylogenetic analysis (12) we conducted places Hurdia as sister to a group composed of Anomalocaris and Laggania, with these three taxa forming a clade in the stem group of the euarthropods (Fig. 4). Although Anomalocaris and Laggania have similar trunk morphology and number of cephalic segments, the latter taxon also shares traits with Hurdia, notably similar frontal appendages, weakly sclerotized anterior carapace elements, and the position of the stalked eyes directly posterior to the frontal carapace (9) (fig. S2, A and B). The frontal appendage of Hurdia was previously assigned to Laggania (9) [appendage F of A. nathorsti (9)], and although Laggania's frontal appendages are similar in general morphology to the more robust of the two Hurdia appendage types [compare figure 7.2 of (1) to Fig. 2B], inadequate preservation of Laggania specimens prevents a more detailed comparison. The phylogenetic analysis suggests that the frontal appendages and anterior carapaces of Hurdia and Laggania are plesiomorphic for the anomalocaridids, making Anomalocaris the most derived member of the clade, because it secondarily lost or modified these structures. If the carapace is homologous with the euarthropod cephalic shield, this head covering may have originated before the last common ancestor of the anomalocaridids and higher euarthropods.

Fig. 4.

Cladistic analysis (12) of selected stem- and crown-group arthropods (SOM text, fig. S3, and table S3). This is a strict consensus of three trees found using branch and bound search under implied weights [concavity constant (k) = 2]. Tree length, 53.89; rescaled consistency index, 0.76. Jackknife supports are shown at the nodes when over 50%.

We regard the lanceolate structures reported here from Hurdia as being respiratory in function, based on their morphology and arrangement. They closely resemble and clarify the structure of those identified as present in Anomalocaris, Laggania (fig. S2I), and in some (26, 27) but not all (28) interpretations of Opabinia (fig. S2G). In Hurdia, the insertion points of the gills (Fig. 2E and fig. S2, C and H) bear some resemblance to the “transverse rods” (9, 27) of Laggania (fig. S2, A and B, and D to F), with both having a regularly spaced, beaded morphology and darkening associated with sclerotization. If these structures are homologous, this adds evidence to the theory that the annuli of the transverse rods are the points of origin for the blades (27). The morphology of the gills of Hurdia reveals more clearly than before that presumed anomalocaridid respiratory structures, like those of Opabinia (28), closely resemble the setae commonly associated with outer branches of Cambrian arthropod limbs (29). Both structures consist of a series of free-hanging filamentous gills attached to a supporting structure (the lateral lobe in anomalocaridids and the outer branch of Cambrian arthropod limbs). This homology is in accordance with the suggestion that such branches are homologous to respiratory exites of extant crustaceans and chelicerates, and not to the outer branch of the modern biramous limb (30). The modern biramous limb forms by division of the main limb axis (30), in contrast to the Cambrian limb, which may be formed by the fusion of a uniramous limb with a respiratory exite. The presence of the respiratory exite in Hurdia pushes the origin of this structure deep into the euarthropod stem group.

Note added in proof: The recently described Schinderhannes bartelsi (31) has been placed between Anomalocaris and the upper stem group arthropods in a cladogram consistent with the analysis here. It has biramous trunk limbs with filamentous exites, an anomalocaridid-like radial mouthpart, and frontal appendages remarkably similar to those of Hurdia morph B. Presence of these features in an animal that lacks lateral lobes and gills adds evidence to the theory that Cambrian biramous limbs formed by fusion of these structures.

Supporting Online Material

www.sciencemag.org/cgi/content/full/323/5921/1597/DC1

Materials and Methods

SOM Text

Figs. S1 to S3

Tables S1 to S3

References

References and Notes

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