HEAD STRUCTURE IN UPPER STEM-GROUP EUARTHROPODS

[Palaeontology, Vol. 51, Part 3, 2008, pp. 561 573] HEAD STRUCTURE IN UPPER STEM-GROUP EUARTHROPODS by GRAHAM E. BUDD Department of Earth Sciences, Palaeobiology, Uppsala University, Norbyvägen 22, Uppsala, SE-752 36, Sweden; e-mail: graham.budd@pal.uu.se Typescript received 7 November 2006; accepted in revised form 4 April 2007 Abstract: Continuing debate over the evolution and morphology of the arthropod head has led to considerable interest in the relevance of the evidence from the fossil record. However, dispute over homology and even presence of appendages and sclerites in Cambrian arthropods has resulted in widely differing views of their significance. The head structures of several important taxa, Fuxianhuia, Canadaspis, Odaraia, Chengjiangocaris and Branchiocaris are redescribed, revealing the essential similarity between them. In particular, all possessed an anterior sclerite, probably followed by a large posterior, ventral sclerite that is likely to be homologous to the hypostome of trilobites. The presence of a similar feature in Sanctacaris is also possible, but less well-supported. An anterior sclerite, usually bearing eyes, as in Fuxianhuia, appears to be a widespread feature of basal arthropods. Whether or not this sclerite represents an original articulating protocerebral segment on its own is, however, open to debate. Key words: Burgess Shale, Chengjiang, Cambrian, head segments, arthropods. The exceptionally preserved arthropods from the Cambrian fauna have exerted a great influence on both general understanding of the Cambrian explosion (e.g. Gould 1991; Wills et al. 1995) and on specific understanding of arthropod evolution. In particular, a great deal of attention has been paid to understanding how the arthropod head evolved, and several distinct palaeontological contributions to this topic have recently been published (e.g. Chen et al. 1995; Dewel et al. 1999; Budd 2002; Chen et al. 2004; Cotton and Braddy 2004; Scholtz and Edgecombe 2005, 2006; Waloszek et al. 2005). Nevertheless, each of these proposals has been controversial because of continued dispute over the presence and interpretation of various features in the key taxa. Central to this has been the putative great appendage -like structure in the Chengjiang fauna taxon Fuxianhuia. This paper deals with a group of taxa, probably not monophyletic, that has been reported to lie close to, but below, the base of the crowngroup euarthropods, i.e. the clade consisting of the last common ancestor of the myriapods, crustaceans, insects and chelicerates plus all of its descendants (Budd 2002). Here, I re-illustrate some of the features of their heads to demonstrate some of their hitherto overlooked features, and to offer a reinterpretation of structures already illustrated. Abbreviations. CN, Catalogue number, Nanjing Institute of Geology and Palaeontology, Academia Sinica; ELRC, Early Life Research Centre, Chengjiang, China; NIGPAS, Nanjing Institute of Geology and Palaeontology, Academica Sinica; RCCBYU, Research Centre for the Chengjiang Biota, Yunnan University, China; ROM, Royal Ontario Museum, Toronto, Canada; SK, Shankou (village) collection in Early Life Research Centre, China; USNM, United States National Museum, Smithsonian Institution, Washington, DC. SYSTEMATIC PALAEONTOLOGY Branchiocaris pretiosa (Resser, 1929) Text-figures 1 2 Material. USNM 189028, counterpart, figured by Briggs (1976, pl. 3, text-fig. 5). Description of cephalic region. Specimen USNM 189028 shows that Branchiocaris possessed a semicircular sclerite that lay medially between the pair of valves, approximately a third of which projected anterior to the valves (Text-figs 1 2). No definite details are visible on the surface, but the anterior boundary is distinct. Behind the posterior boundary lies a more poorly defined, broader, central arcuate structure that is here interpreted as the anterior edge of a ventral sclerite. This sclerite oversteps the first appendage, and perhaps also the second appendage (see below). Its central longitudinal axis, slightly displaced in this specimen, is marked by a narrow, parallel-sided ridge, and faint also parallel grooves lie either side of this ridge. This sclerite appears to be at least twice as long as the anterior one, but it is incomplete in this specimen and the posterior margin is indistinct. ª The Palaeontological Association doi: 10.1111/j.1475-4983.2008.00752.x 561

562 PALAEONTOLOGY, VOLUME 51 TEXT-FIG. 1. Branchiocaris pretiosa (Resser, 1929). USNM 189028B, showing central anterior sclerite, insertion of the pairs of appendages, and probably a large hypostome lying behind the anterior sclerite; 6.5. TEXT-FIG. 2. Branchiocaris pretiosa (Resser, 1929). Interpretative drawing of USNM 189028B (see Text-fig. 1). Scale bar represents 5 mm. As described by Briggs (1976), the cephalic region is equipped with two pairs of appendages. The first of these is a stout, antenna-like structure with some 20 articles. This appendage appears to insert on the anterior-lateral edge of the posterior sclerite, and just behind the posterior edge of the anterior one. The second appendage is more poorly defined. It possessed perhaps six or seven articles including a terminal one, which appears to consist of a spike with a prominent central furrow (Briggs 1976). In both specimens that show the appendage clearly (USNM 189028, Text-fig. 1 herein and USNM 189030, pl. 5, fig. 2 of Briggs 1976) there is some evidence of a definite geniculation behind the most anterior two articles. The appendage inserts rather closely posterior to the antenna-like appendage, also under the broad posterior ventral sclerite.

BUDD: HEAD STRUCTURE IN UPPER STEM-GROUP EUARTHROPODS 563 Fuxianhuia protensa Hou, 1987 Text-figures 3 4 Material. ELRC 19255b, Chen et al. (1995, fig 1); 19245. Description of cephalic region. The head of Fuxianhuia possessed an oval anterior sclerite from which emerge a pair of stalked structures normally interpreted as eyes (e.g. Chen et al. 1995). A pair of stout, antenna-like appendages also insert close to or under this sclerite, although the exact position remains unclear: the best specimens, however, seem to show it inserting posterior to the sclerite (e.g. ELRC 19258: Chen et al. 1995, fig. 2D; Waloszek et al. 2005, fig. 2E, NIGPAS100127). Behind the anterior sclerite lies a broader ventral sclerite. The size of this structure is unclear, because in one of the betterknown specimens that shows it well (ELRC 19255b; Chen et al. 1995, fig. 1; Text-figs 3A, 4 herein) the posterior margin is clearly broken. The presence of a second pair of appendages in the cephalic region has proved to be highly controversial. Geniculate structures are clearly present (Text-figs 3A B, 4) but their significance is unclear (see discussion). However, Chen et al. (1995) figured a drawing of a supposed isolated subchelate appendage that is photographically figured here for the first time (ELRC 19245; Text-fig. 3C) together with an enlargement of one of the geniculate structures of ELRC 19255b, at the same scale and orientation (Text-fig. 3B). The similarity between these structures is striking, including a prominent longitudinal ridge along the most proximal portions of both. A B C TEXT-FIG. 3. A C, Fuxianhuia protensa Hou, 1987. A, ELRC 19255b, ventral view of head region showing eyes, anterior sclerite, broken hypostome and the two putative subchelate appendages ; 8. B, same, close-up of left appendage, orientated horizontally; 20. C, ELRC 19245, isolated putative subchelate appendage at same magnification and orientation as structure in Text-figure 2; 20.

564 PALAEONTOLOGY, VOLUME 51 medial crease right antenna anterior sclerite hypostome TEXT-FIG. 4. Fuxianhuia protensa Hou, 1987. Explanatory drawing of ELRC 19255b (cf. Text-fig. 3A). Scale bar represents 5 mm. broken rear of hypostome right great appendage left great appendage Chengjiangocaris longiformis Hou and Bergström, 1991 Plate 1, figure 4; Text-figures 5 6 Material. RCCBYU 10256. Hou et al. (2004, p. 106, fig. 16.5b). Description of cephalic region. Chengjiangocaris possessed, like Fuxianhuia, an anterior, rounded sclerite associated with a pair of putative stalked eyes. In addition, a pair of antennae appears to be present (Hou and Bergström 1997). Behind the anterior sclerite lies a larger sclerite. The sclerite is large, and, when studied closely, it can be seen that the structure interpreted as the posterior, concave margin (Waloszek et al. 2005) is an asymmetric fold. Dark staining slightly anterior and slightly posterior to the true posterior margin of the sclerite may indicate the position of the mouth (Waloszek et al. 2005) and the anterior gut, presumably curving back towards the mouth. Behind the posterior margin of the sclerite lies a series of lobed dark stains (Textfigs 5 6) which, by analogy with other arthropods, is likely to represent gut diverticula. Canadaspis perfecta (Walcott, 1912) Text-figures 7A B, D, 8 Material. USNM 189019B, Briggs (1978, figs 81, 84); Simonetta and Delle Cave (1975, pl. 39, fig. 1); 207298. See discussion in Briggs 1978, p. 454. TEXT-FIG. 5. Chengjiangocaris longiformis Hou and Bergström, 1991. Close-up of head region of RCCBYU 10256; 11.

BUDD: HEAD STRUCTURE IN UPPER STEM-GROUP EUARTHROPODS 565 TEXT-FIG. 6. Chengjiangocaris longiformis Hou and Bergström, 1991. Interpretative drawing of RCCBYU 10256. Scale bar represents 1 mm. A B C D TEXT-FIG. 7. A B, D, Canadaspis perfecta (Walcott, 1912). A, USNM 189019B, showing anterior sclerite with faint traces of compressional wrinkling at top right; the arcuate anterior margin of the probable hypostome is also visible; 6. B, same, close-up of anterior sclerite; 11. D, USNM 20729, anterior sclerite, again showing antennae inserting apparently just behind it; 8. See Textfigure 8 for explanatory drawings. C, Odaraia alata Walcott, 1911, USNM 213807, close-up of head region showing anterior, articulating sclerite with large lateral eyes; 6. Description of cephalic region. Canadaspis, too, appears to have possessed a rather clearly-defined anterior sclerite, although the structure is not as well preserved as in Branchiocaris. In USNM 198019B it appears as a structure lying in the same place as the anterior sclerite in Branchiocaris, with one-third to one-half of the sclerite protruding in front of the valves. Faint marginal

566 PALAEONTOLOGY, VOLUME 51 A anterior sclerite B antenna antennae hypostome? anterior sclerite folds may be seen in the structure of USNM 189019B, suggesting that it had some relief and resistance. The larger pair of antennae of Canadaspis appear to insert just behind this sclerite (Text-fig. 7D). Behind the anterior sclerite is a faint arcuate structure, as in Branchiocaris, that may represent the anterior margin of a larger posterior sclerite (Text-fig. 7A B). Briggs (1978) figured several instances of this anterior structure (e.g. USNM 189019), but interpreted it as the anterior portion of a rather elongate labrum, with a somewhat complex posterior portion that was difficult to delimit because of poor exposure in known specimens (e.g. USNM 213853; his pl. 4, figs 52, 59). The best exposure is probably in USNM 207290 (Briggs 1978, fig. 32; pl. 3, fig. 42). This specimen shows a rather broad anterior sclerite, with two longitudinal structures behind delimiting either another structure (the interpretation favoured here) or the posterior portion of a labrum hypostome (the interpretation of Briggs 1978), in which case the two regions of the structure were rather different. Such an interpretation cannot be ruled out with the current data; however, several lines of evidence point towards the anterior structure being homologous to that of Fuxianhuia. First, the structure is extremely anterior; indeed, it forms the anterior margin of the entire axis of the animal. Furthermore, rather than being part of a smooth anterior margin of the animal (as in Briggs 1978, fig. 62), it appears to form a distinct cephalic sub-unit of its own (particularly in USNM 189019; see Briggs 1978, figs 81, 84; Text-fig. 7A B herein). Second, the limited evidence from 198019B is that a second structure, the posterior sclerite, lies behind it, which is here interpreted as the true hypostome, and that the anterior structure is not part of it (Text-fig. 7B). Third, the marginal wrinkling suggests that it had a considerable degree of convexity. Fourth, since the description of Canadaspis in 1978, several taxa have been described (some of which are considered here) that allow the morphology of Canadaspis to be considered in a context that was not available in 1978. The relationship of the eyes and antennae to this structure are the same in all cases, i.e. with the eyes emerging from under this structure, and the antennae from just behind it; a similar situation (without eyes being preserved) is seen in Branchiocaris in which the evidence for a large posterior sclerite behind an anterior sclerite is slightly clearer. In the rather Canadaspis-like taxon Perspicaris (Briggs 1977), the anterior sclerite as a separate, non-labral structure is considerably clearer (see discussion below), again with the same relationship to the eyes and antennae, and this can be considered to be additional evidence that the structure in Canadaspis is a true anterior sclerite and not a hypostome labrum. Odaraia alata Walcott, 1912 Text-figures 7C, 9 Material. USNM 213807, Briggs (1981, pl. 4, figs 33 35). TEXT-FIG. 8. Canadaspis perfecta (Walcott, 1912), interpretative drawings. A, USNM 189019B; B, USNM 207298. Scale bars represent 5 and 10 mm respectively. Description of cephalic region. Odaraia bears a very large pair of eyes on an anterior region of the head. The nature of this structure is not entirely clear. Some specimens, such as USNM 189232 (Briggs 1981, fig. 61; pl. 7, figs 66 67), seem to show that this region is continuous with the rest of the trunk. However, other specimens, such as USNM 213807 (Text-figs 7C, 9), suggest that this region is a definite region of the body that is well-sclerotised and narrows posteriorly before connecting to the rest of the trunk. USNM 213807 is difficult to interpret, but seems to indicate an overlap between an anterior sclerite, the posterior shield, and perhaps another ventral posterior sclerite (Text-fig. 9), although the obscure overlap region cannot be easily resolved. A more or less clear posterior margin to an anterior sclerite is seen in other specimens such as USNM 189234 (Briggs 1981, fig. 29; pl. 1, fig. 4) and USNM 189231 (Briggs 1981, pl. 2, figs 12, 14). In ROM 383938 (Briggs 1981, figs 48 50; pl. 6, fig. 57) the posterior margin may simply be formed by the two valves meeting at the hinge; if so, though, the smooth curve with which they meet is not in accord with the sharp angle in the eyes overlap region eye stalk anterior sclerite? underlying sclerite? TEXT-FIG. 9. Odaraia alata Walcott, 1911. Explanatory drawing of USNM 213807 (cf. Text-fig. 7C). Scale bar represents 5 mm.

BUDD: HEAD STRUCTURE IN UPPER STEM-GROUP EUARTHROPODS 567 reconstruction (Briggs 1981, fig. 103a). Furthermore, this specimen in particular shows that the anterior sclerite lies on a distinct body region that narrows posteriorly, rather as it is in Perspicaris. As noted by Briggs (1981), the region interpreted as the anterior sclerite here bears three small reflective spots that he reasonably interprets as median eyes (USNM 189232, Briggs 1981, fig. 61, pl. 7, figs 66 68). extent forward into a rounded point. Either this extension is in fact the anterior sclerite or, perhaps more likely, the sclerite lies beneath it. Nevertheless, the eyes of Sanctacaris seem to lie well behind the putative frontal sclerite, and not to insert into it (Pl. 1, fig. 1; Briggs and Collins 1988), and thus show substantial differences from the arrangement in the other taxa discussed here. Sanctacaris uncata Briggs and Collins, 1988 Plate 1, figures 1 3; Text-figure 10 Material. ROM 43502 (holotype) Briggs and Collins (1988, pl. 71; text-fig. 1), 43504 (Briggs and Collins 1988, pl. 72; textfig. 2). See discussion in Briggs and Collins (1988, pp. 781 786). Description of cephalic region. The head shield of Sanctacaris consists of a circular central structure with flanking wings (Pl. 1, fig. 1), which is closely comparable to that of Fuxianhuia (Text-fig. 3A). Anteriorly lies a complex array of frontal appendages with both spined and limb-like rami. These structures may, however, be partly or fully branches of a single structure (see e.g. Briggs and Collins 1988, text-figs 1B, 2A). In particular, the holotype demonstrates that the branches seem to insert in almost the same place (Pl. 1, figs 1 2), suggesting that they attach to a single structure that then inserts into the body. Although this might be explicable by taphonomic distortion, the rest of the specimen does not appear so distorted. As discussed by Briggs and Collins (1988), the array of armoured appendages or rami is followed by an apparently separate, more antenniform structure (Pl. 1, figs 1 2). Specimen ROM 43504 also appears to show some sign of an anterior, subrectangular sclerite (Pl. 1, fig. 3; Text-fig. 10), lying just in front of the frontal appendage(s). It is partly cut by a crack in the rock. This structure is also visible in the original illustration of Briggs and Collins (1988), which shows that the putative sclerite extends just beyond the crack (not visible in Pl. 1, fig. 3). Although this sclerite is not visible in the holotype, ROM 43502, the front of the head shield does apparently DISCUSSION The new data and interpretations above significantly amend our understanding of basal euarthropod cephalic morphology. In particular, the presence of an anterior sclerite that projects in front of the rest of the body appears to be widespread. Previous descriptions of these taxa, such as of Branchiocaris and Canadaspis, interpreted these extensions as simply the anterior margin of the body or as the anterior portion of a labrum. However, the data presented above, especially for Branchiocaris, suggest that this extension is, rather, a discrete and well-sclerotised structure. The anterior sclerite seems also to be present in several other taxa not figured here including Protocaris marshi Walcott, 1884 (Briggs 1976, pl. 1, fig. 3; text-fig. 3); Shankouia Chen et al., in Waloszek et al. (2005; SK10065A, see their fig. 1B); and Perspicaris dictynna (Simonetta and Delle Cave, 1975) (Briggs 1977, his pl. 68, figs 4, 6). In the last of these, the structure is separated from the rest of the body, including the mouth, by a distinct narrow neck, and thus cannot be a labrum. An intermediate morphology between Perspicaris dictynna and Canadaspis is seen in Perspicaris recondita Briggs, 1977 (e.g. USNM 114255; see his pl. 69, fig. 5 and textfig. 12), although the head region is not well preserved in this taxon. All of the taxa discussed above have had a long history of controversial taxonomic assignment. Two, Canadaspis TEXT-FIG. 10. Sanctacaris uncata Briggs and Collins, 1988, interpretative drawing of 43504 (part). The part of the putative anterior sclerite to the left of the prominent crack is not readily visible in this image, but is evident in Briggs and Collins (1988, pl. 72, fig. 1). Scale bar represents 2 mm. cracks in rock anterior sclerite? posterior margin of sclerite? mass of anterior appendage rami

568 PALAEONTOLOGY, VOLUME 51 (Briggs 1978) and Sanctacaris (Briggs and Collins 1988), were assigned to the (by implication) crown-group crustaceans and stem-group chelicerates, respectively. However, advances in systematic methodology (e.g. the introduction of the stem- and crown-group concepts) and description of new material has provided a new context in which to consider these taxa. Budd (2002) recovered a monophyletic clade including Perspicaris, Odaraia, Branchiocaris, Fuxianhuia and Canadaspis, and by implication Chengjiangocaris and Protocaris (Sanctacaris resolved as the sister group to this clade plus the crowngroup euarthropods), even without the new data presented here. Given the apparent apomorphies shared by these taxa then, it seems reasonable to look for further potential homologies, including the characters presented herein. Thus, although the evidence for the anterior sclerite plus eyes, followed by antennal insertion and posterior sclerite arrangement, cannot on its own be considered to be completely compelling for all the taxa considered here, their phylogenetic context is one reason (among several) to interpret their suggestive morphology as such. Cephalic structure in Fuxianhuia. The presence of a large posterior sclerite is harder to document in the taxa described above, although traces of it are apparently present in Branchiocaris and Canadaspis, and it is certainly present in Chengjiangocaris and Fuxianhuia. The posterior sclerite appears to be rather large in Chengjiangocaris, and perhaps can be inferred to have been in Fuxianhuia. The large size of this sclerite suggests that it was not possible for the valves (see below) of these taxa to close fully. Given its position in front of the mouth, it seems likely that this sclerite is homologous to the hypostome that is found in many other Cambrian arthropods such as the trilobites. The presence of the posterior sclerite, combined with the appendage and sclerite data from Branchiocaris, adds a new twist to the debate about the presence of the subchelate appendage in Fuxianhuia (Chen et al. 1995; Hou and Bergström 1997; Budd 2002; Waloszek et al. 2005; Scholtz and Edgecombe 2006). Fuxianhuia was first described in 1987, and its primitive characteristics (multi-articulated limbs and head apparently comprising few segments) were soon recognized (although see Wills 1996 for a counter-view). Nevertheless, its morphology has generated considerable controversy, from the relationship between the number of limbs and tergites to its head structures. In particular, based on new material, the peculiar putative second appendage was suggested to be a gut diverticulum by Waloszek et al. (2005). The purported appendage is difficult to assess because it is invariably preserved with both of the pair curved backwards and superimposed over the body. Any podomeres are difficult to see distinctly, and the whole structure appears to have a somewhat bag-like appearance. Furthermore, the mineralized tip to the structures is compatible with the mineralization seen at the ends of some arthropod gut diverticula in the Cambrian record (Butterfield 2002). Waloszek et al. (2005) dissected down through the dorsal surface of a Fuxianhuia specimen and found cuticle both above and below the disputed structures, with the implication that the structures were internal (Waloszek et al. 2005, fig. 2A D, p. 197). The comments of Waloszek et al. (2005) are reasonable objections to the appendiculate nature of the disputed structures. Nevertheless, in the light of the new data presented here, they are not completely compelling. First, the presence of the cuticle beneath the appendages may simply reflect the presence of a large posterior sclerite, as seems to be the case for Chengjiangocaris (see also Hou and Bergström 1997, fig. 9C of CN 115354). Second, the presence of the anterior sclerite in Branchiocaris, together with its other apparent similarities to Fuxianhuia (Budd 2002), suggests that its morphology may be of particular relevance in interpreting that of Fuxianhuia. Branchiocaris shows more clearly than any other Cambrian taxon the presence of a stout antenniform and a great appendage. The morphology of the second appendage in Branchiocaris is also of note; rather poorly defined with few welldeveloped articulations and the hint of a pronounced geniculation before the terminal subchelate structure, all of which are compatible with a description of the structure in Fuxianhuia. Although the structure in Fuxianhuia appears to be particularly bag-like, it does appear to have a cuticular composition that is comparable to that of the rest of the external morphology. Finally, the illustration of an isolated structure (Chen et al. 1995, fig. 3D; Text-fig. 3B C herein) is also hard to reconcile with this structure being an internal gut diverticulum. The evidence from Chengjiangocaris also suggests that the gut does not pass anterior enough to allow connection with these structures. Whilst not absolutely convincing then, the EXPLANATION OF PLATE 1 Figs 1 3. Sanctacaris uncata Briggs and Collins, 1988. 1, ROM 43502 (holotype part), complete specimen; 1.75. 2, same, close-up of head appendages showing cluster of frontal rami and antenniform appendage behind; 5.5. 3, ROM 43504 (part) showing putative anterior sclerite; 3. Fig. 4. Chengjiangocaris longiformis Hou and Bergström, 1991, complete specimen RCCBYU 10256; 2.7.

PLATE 1 1 2 4 3 BUDD, Chengjiangocaris, Sanctacaris

570 PALAEONTOLOGY, VOLUME 51 data here suggest that, although it has some peculiar features, the large geniculate structure in the head of Fuxianhuia is an appendage (see also comments in Scholtz and Edgecombe 2006 that come to similar conclusions). Its stereotypical position and appearance may reflect the fact that it was constrained to lie beneath the posterior sclerite. Its preservational pecularities may be analogous to the known case of limbs being preserved differently under cuticle in Burgess Shale-type fossils. Budd (2002) suggested, rather enigmatically, that the head shield of Fuxianhuia was effectively bivalved. There are two lines of evidence to suggest that the headshield was not a simple domed structure. The first is the consistent presence of a central crease evident in both dorsal and ventral aspect, perhaps representing a composite mould in the latter case (e.g. RCCBYU 10255, Hou et al. 2004, fig. 16.3b; CN 115353, Hou and Bergström 1997, fig. 8B; Text-fig. 4 herein). Such creases are common artefacts during compression (e.g. Fortey and Theron 1994; Jell and Hughes 1997; Budd 1999; Ritchie and Edgecombe 2001). Nevertheless, in ELRC 19254a (Chen et al. 1995, figs 2A, 3C) the crease is associated with a highly creased indentation of the anterior margin of the shield; this would not be expected if it was simply a compressional artefact. Second, both Fuxianhuia and Chengjiangocaris are known from lateral compressions that show a more or less straight dorsal margin to the shield (CN 115355, Hou and Bergström 1997, fig. 9D, and CN 115359, Hou and Bergström 1997, figs 12B C, 14A: the dorsal margin is clearer in the photographs than in the drawing), indeed not dissimilar to lateral compressions of Canadaspis (Briggs 1978). Conversely, many dorsoventral compressions show no signs of the feature. However, effacement of such features is common in other taxa such as Canadaspis and Waptia (e.g. Briggs et al. 1994, fig. 112). The nature of the hinge in such taxa is unclear. There is no suggestion that the shield in Fuxianhuia or Chengjianocaris is physically divided into two separate valves. On the other hand, an arrangement similar to that claimed for Waptia, where a central fold perhaps allows a certain amount of flexibility (Briggs et al. 1994, p. 157) might be possible. Hinges in the taxa described herein may indeed fall along a spectrum of virtual non-existence (Odaraia?) through to a more obvious division into two components such as in Canadaspis, where isolated valves are common; it should be noted, too, that probable adductor muscle scars are known from Canadaspis, Odaraia and Branchiocaris, but have not been reported from Chengjiangocaris or Fuxianhuia. In any case, it is clear from their style of preservation that Fuxianhuia and Chengjiangocaris possessed highly domed cephalic shields that allowed lateral preservation of the animals, and that they may have had some sort of central fold acting as an effective hinge. Distribution of the anterior sclerite. An anterior sclerite has been reported in other Cambrian taxa apart from those figured here, i.e. the helmetiid lamellipedians Helmetia Walcott, 1918, Kuamaia Hou, 1987, Rhombicalvaria Hou, 1987 (possibly a synonym of Kuamaia; Hou and Bergström 1997), Saperion Hou et al., 1991, Skioldia Hou and Bergström, 1997 and probably Tegopelte Whittington, 1985 (see discussion of character 10 in Edgecombe and Ramsköld 1999) where it occupies a similar position, in front of a hypostome. These taxa have been considered to lie together in a clade (Edgecombe and Ramsköld 1999). One group of taxa that does not clearly show such a feature, however, is that composed of the great appendage arthropods such as Leanchoilia and Yohoia; the possible exception, if it belongs broadly here, is Sanctacaris (see above). Nevertheless, the evidence for the sclerite in Sanctacaris is equivocal, and other details of its morphology (e.g. the position of the eyes) makes direct comparison with the other taxa here problematic. Some of the taxa identified to lie in a clade with Branchiocaris, Canadaspis and other genera by Budd (2002) have not been considered here. These are Fortiforceps, Occacaris (and presumably the similar Forfexicaris, see Hou 1999), Pectocaris and Clypecaris. With the exception of Fortiforceps, these are bivalved taxa whose head structures are generally obscured by the valves. As a result, the presence or absence of head sclerites in these taxa must be considered an open question. The head region of Fortiforceps is poorly known, but at least one specimen hints at the presence of an anterior, circular sclerite being present (i.e. CN 115373; see Hou and Bergström 1997, figs 31C D, 33E). In addition, the poorly known Combinivalvula Hou, 1987 shows some indications of a similar arrangement (Hou et al. 2004, fig. 16.32). The question of whether or not the helmetiid sclerites are homologous to those identified in the taxa described above is a matter for phylogenetic analysis, together with appropriate outgroups such as the anomalocaridids (Budd, unpublished data). In particular, the relationship of the eyes to the anterior sclerite in these taxa is not quite clear. Nevertheless, Edgecombe and Ramsköld (1999) figured several suggestive specimens that imply the eyes in these taxa are ventral, stalked, and originate from the anterior sclerite body region (for Kuamaia, see their figs 5 6; for Saperion, figs 3 4; see their discussion, pp. 267 273, for anterior structures in these taxa). The best specimen of Helmetia (USNM 83952, Briggs et al. 1994, fig. 141) also suggests that the eyes are connected to the anterior sclerites by stalks. If the eyes do originate from the anterior sclerite, then this should be regarded as reasonable a priori evidence for homology. A further similarity is the presence of paired frontal organs on the anterior sclerite of at least Helmetia (see discussion in Edgecombe and Ramsköld 1999, and USNM 83952, Briggs et al. 1994, fig. 141) that

BUDD: HEAD STRUCTURE IN UPPER STEM-GROUP EUARTHROPODS 571 are interpreted to be median eyes. A cluster of three small, reflective spots is also seen on the frontal sclerite of Odaraia (e.g. Briggs 1981, fig. 61, pl. 7, figs 66 68), and again, this may be taken as an indicator of homology. It is generally agreed that Fuxianhuia and its allies lie outside the euarthropod crown group (Hou and Bergström 1997; Budd 2002; Waloszek et al. 2005 and references therein; but see also Wills 1996). Identification of a homologous sclerite in taxa generally considered to lie more crownward would, therefore, polarize upper stem group and crown group arthropods so as to place Helmetia and its lamellipedian allies basally in a potentially paraphyletic assemblage. This in turn would have important implications for the rooting of the crown group euarthropods generally, and such vexed questions as the position of the trilobites. The information presented here would thus have the effect of making the anterior sclerite and the associated head structure plesiomorphic for a large clade of arthropods including the crown-group euarthropods. A formal cladistic analysis of this proposition must, however, await description of the state in other relevant taxa such as the anomalocaridids. What does the anterior sclerite represent? Early work suggested that it was the tergite of a true articulating segment bearing the eyes, corresponding to the protocerebrum of the arthropod brain (Chen et al. 1995), a view that has been supported more recently (Waloszek et al. 2005). Work on putatively even more basal taxa, such as the anomalocaridids (Budd, unpublished data) does not support this assertion, but rather suggests that this sclerite is an innovation that occurred deep in the euarthropod stem lineage. Nevertheless, the suggestion from the new data presented here is that such a protocerebral segment, whether or not absolutely basal, does characterize most of the euarthropods, and has been modified in the living crown groups (thus agreeing with the main point of Chen et al. 1995 and Waloszek et al. 2005). Its subsequent history may perhaps be traced into taxa such as the naraoiids, where a boomerang -shaped sclerite, with frontal organs, lies in front of the hypostome in at least Misszhouia (Chen et al. 1997, figs 2 3, 7a; see character 11 of Edgecombe and Ramsköld 1999). Although the rostral plate in trilobites is another possible homologue (an arcuate rostral plate characterizes many putatively basal taxa such as the olenellids), Edgecombe and Ramsköld (1999) argued that this is probably not homologous with the anterior sclerite, with the implication that, as in Misszhouia, the structure has already been merged with the front of the hypostome. This view is perhaps supported by the presence of the paired maculae in trilobite hypostomes, although as Chen et al. (1997) pointed out, the more posterior maculae are not positioned in the same place as the frontal organs. Potentially homologous organs are also found in Agnostus pisiformis (Müller and Walossek 1987, pl. 13); indeed, the frontal organs of crustaceans and the ventral eyes of the chelicerates may all potentially be homologous (see e.g. discussion in Chen et al. 1997, p. 3). Finally, the attractive suggestion that the problematic cephalon of Sidneyia may be simply an anterior sclerite of the sort discussed here (Hou and Bergström 1997, p. 99) requires investigation, in particular to determine whether it truly bears the antennae or simply the eyes as would be expected. Head appendages in stem-group euarthropods. The presence and nature of head appendages in stem-group euarthropods continues to be controversial. If the conclusions presented here are correct, namely that a large array of rather disparate taxa can be united on the presence of the anterior sclerite, probably followed by a broad posterior sclerite, then the nature of the appendages becomes a little clearer by analogy to other members of the group. At least some taxa (especially Branchiocaris) possessed two pairs: a stout, antenna-like anterior pair inserting close to, but not quite on, the anterior margin of the posterior sclerite; and a larger, subchelate pair inserting more laterally on the posterior sclerite. While the presence of the two pairs in Branchiocaris is, of course, widely accepted, their significance is less clear, with Waloszek et al. (2005) suggesting, along with Briggs (1976), that the second pair are post-oral and thus, by implication, of no importance in understanding the evolution of the most anterior region of the head. However, it is not clear that this is the case. A mineralized and reflective central region appears to indicate the position of the gut (Briggs 1976, pl. 3, fig 3; pl. 4, figs 2 3; pl. 5, fig. 2), and the anterior portion is preserved in relief (see Branchiocaris, above). Briggs (1976) suggested that the most anterior extent of this portion in relief represented the position of the mouth. However, if so, then the mouth would be extremely far forward, not only anterior to the large second appendage but level with, and possibly anterior to, the antenniform appendages as well. The probable presence of a large posterior sclerite, however, rules out the mouth being this far forward, and in any case the gut typically curves ventrally and posteriorly before opening out into the mouth (see comments in Waloszek et al. 2005). If so, there is no particular reason to think that the mouth is as far forward as has been assumed for Branchiocaris. Rather, it would be placed in a relatively posterior position, and both pairs of appendages would be pre-oral. CONCLUSIONS The anterior sclerite known from the problematic Fuxianhuia is a widespread feature of putative stem-group euarthropods, and its presence helps to clarify several

572 PALAEONTOLOGY, VOLUME 51 problematic issues surrounding these taxa. It appears also to be present in Branchiocaris, Canadaspis, Perspicaris, Odaraia and Chengjiangocaris; it is doubtfully present in Sanctacaris. In addition, a similar structure is found in the helmetiid lamellipedians. At least some relatives of Fuxianhuia possessed two cephalic appendages, and the evidence presented here confirms that Fuxianhuia did too. A large posterior sclerite normally lies behind the anterior sclerite, although it is typically less clearly preserved than the anterior sclerite itself; and the second, larger pair of appendages in at least Branchiocaris inserts lateral to it. The overall unity of these taxa suggests that they form a paraphyletic or perhaps monophyletic assemblage in the stem-group, and thus provide important clues to basal euarthropod evolution. Despite the description of some of these taxa, in particular Canadaspis (Briggs 1978), as crustaceans, the new evidence here reinforces their similarities with other stem-group euarthropods, many of which bore a large, and sometimes bivalved carapace (Budd 2002). The presence of this sclerite as an early feature in the upper euarthropod stem group suggests, in the absence of evidence to the contrary, that some of the lamellipedians such as Helmetia have retained the anterior sclerite. This in turn may indicate that the lamellipedians are paraphyletic and may have given rise to the crown group euarthropods, that is, the lineages leading to the extant mandibulates and chelicerates. Acknowledgements. Doug Erwin and Jann Thompson, and Jean- Bernard Caron and Janet Waddington, are thanked for enabling access to the Smithsonian and ROM collections of Burgess Shale material, respectively. 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