Beyond the Burgess Shale: Cambrian Microfossils Track the Rise and Fall of Hallucigeniid Lobopodians Rspb.Royalsocietypublishing.Org Jean-Bernard Caron1,2, Martin R

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Beyond the Burgess Shale: Cambrian microfossils track the rise and fall of hallucigeniid lobopodians rspb.royalsocietypublishing.org Jean-Bernard Caron1,2, Martin R. Smith3 and Thomas H. P. Harvey3 1Department of Natural History (Palaeobiology Section), Royal Ontario Museum, Toronto, Ontario, Canada 2Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada 3Department of Earth Sciences, University of Cambridge, Cambridge, UK

Research Burgess Shale-type deposits are renowned for their exquisite preservation of soft-bodied organisms, representing a range of animal body plans that evolved Cite this article: Caron J-B, Smith MR, Harvey during the Cambrian ‘explosion’. However, the rarity of these fossil deposits THP. 2013 Beyond the Burgess Shale: Cambrian makes it difficult to reconstruct the broader-scale distributions of their constitu- microfossils track the rise and fall of halluci- ent organisms. By contrast, microscopic skeletal elements represent an extensive chronicle of early animal evolution—but are difficult to interpret in the absence geniid lobopodians. Proc R Soc B 280: of corresponding whole-body fossils. Here, we provide new observations on the 20131613. dorsal spines of the Cambrian lobopodian (panarthropod) worm Hallucigenia http://dx.doi.org/10.1098/rspb.2013.1613 sparsa from the Burgess Shale (Cambrian Series 3, Stage 5). These exhibit a distinctive scaly microstructure and layered (cone-in-cone) construction that together identify a hitherto enigmatic suite of carbonaceous and phosphatic Cambrian microfossils—including material attributed to Mongolitubulus, Received: 21 June 2013 Rushtonites and Rhombocorniculum—as spines of Hallucigenia-type lobopodians. Accepted: 9 July 2013 Hallucigeniids are thus revealed as an important and widespread component of disparate Cambrian communities from late in the Terreneuvian (Cambrian Stage 2) through the ‘middle’ Cambrian (Series 3); their apparent decline in the latest Cambrian may be partly taphonomic. The cone-in-cone construction of hallucigeniid sclerites is shared with the sclerotized cuticular structures ( jaws Subject Areas: and claws) in modern onychophorans. More generally, our results emphasize palaeontology, evolution the reciprocal importance and complementary roles of Burgess Shale-type fossils and isolated microfossils in documenting early animal evolution. Keywords: small carbonaceous fossils, small shelly fossils, Lagersta¨tten, biostratigraphy, Cambrian 1. Introduction evolutionary radiation Cambrian lobopodian worms are pivotal to understanding the emergence of panarthropods (Arthropoda, Tardigrada and Onychophora) [1]. Although the fossil record reveals a diversity of extinct marine lobopodians, these are largely restricted to a small number of Cambrian Burgess Shale-type deposits with Author for correspondence: exceptional whole-body preservation—in particular, the Chengjiang and Jean-Bernard Caron Burgess Shale biotas [2]. Burgess Shale-type preservation is rare after the e-mail: [email protected] middle-Cambrian [3], which limits our understanding of longer-term trends in lobopodian diversity, abundance and geographical distribution. However, various early lobopodians possessed recalcitrant sclerites that have the potential to be recognized as small shelly fossils (SSFs) and/or small carbonaceous fossils (SCFs), which in general tend to be more abundant, more diverse and more widely distributed in space and time than corresponding macrofossils [4]. To date, secure identifications of lobopodian microfossils have been limited to the dorsal sclerites of Microdictyon and Onychodictyon, which occur among SSF assemblages as well as in situ on body fossils in the Chengjiang Lagersta¨tte [5]. Surface texture has been documented on the spines of Hallucigenia from Chengjiang [5], although details are obscured by extensive weathering. Here, we describe unweathered Hallucigenia sparsa spines from whole-bodied Burgess Electronic supplementary material is available Shale macrofossils (Cambrian Series 3, Stage 5; British Columbia, Canada) [6,7]. at http://dx.doi.org/10.1098/rspb.2013.1613 or Our new observations allow previously enigmatic SCFs and SSFs to be recognized via http://rspb.royalsocietypublishing.org. as hallucigeniid spines. We discuss the implications for the taphonomy, mode of growth and broad-scale distributions of armoured marine lobopodians.

2. Spines of Hallucigenia sparsa from the distinguished by having ornamenting scales with finely fringed 2 tips (figure 2k). This form resembles certain isolated spines sbryloitpbihn.r rcRScB20 20131613 280: B Soc R Proc rspb.royalsocietypublishing.org Burgess Shale attributed to Hallucigenia hongmeia (fig. 7f of [5]). Hallucigenia sparsa bears seven pairs of slender, slightly curved dorsal spines that measure up to 12 mm in length. Each is elliptical in cross-section (based on bedding-perpendicular specimens) and tapers uniformly from its non-flaring base to its 4. ‘Small shelly’ hallucigeniid spines pointed apex, with an apical angle of ca 68 (figure 1a–g,j–k). A Hallucigenia-like surface ornament also characterizes various The spines comprise thick carbon films (figure 1l), indicating isolated spines that occur as phosphatic, three-dimensionally that the original carbonaceous component was notably robust preserved SSFs. The best studied of these is Mongolitubulus,a [8]. Phosphate is also present (figure 1m), although in much demonstrably polyphyletic form-taxon that includes com- lower concentrations than in organophosphatic Burgess Shale ponents of bradoriid and trilobite carapaces [14,15] and has shells [9], indicating that these spines were at most lightly speculatively been linked to lobopodians [16]. Most specimens phosphatized in life. assigned to Mongolitubulus are readily distinghuished from The spines bear a distinctive external ornamentation com- hallucigeniid spines, including the type material of the type prising a repeated motif of distally directed and inclined species, Mongolitubulus squamifer; this has rhomboidal rather triangular scales that are raised above the smooth surface of than triangular scales that form an uninterrupted spiral from the spines (figure 1h,i,n–p). These reach 10 mminlength, the spine base to tip. The spines of other Mongolitubulus species have a 308 apical angle and are most pronounced in the central have wide flaring bases and lack internal lineations, in clear region of each spine (figure 1n), disappearing towards each contrast to Hallucigenia. However, a subset of specimens spine’s tip (figure 1f,g). The scales are arranged in intersecting ascribed to M. squamifer do exhibit non-flaring bases, locally diagonal series; towards the base, the number and density of interrupted ornamentation and internal longitudinal linea- scales increases, with individual scales becoming smaller, tions [17–20]; we re-interpret these as hallucigeniid spines less regularly arranged and less prominent (figure 1o). The (see the electronic supplementary material, table S1). In sum- spines also contain a series of edge-parallel lineations that mary, hallucigeniid spines can be recognized on the basis of are most prominent near the spine apex (figure 1f,g). their shape (gently curving, without a flared base), ornament The spines comprise a series of nested internal structures (a locally perturbed diagonal arrangement of rounded triangu- with a consistent outline (figure 1e–i). In the smallest whole- lar scales, diminishing near the tip and base) and structure body specimens (presumably representing juveniles), a single (a cone-in-cone construction and an internal layer with longi- internal cone is present within the spines, which are typically tudinal lineations). This diagnostic suite also characterizes the less than 2 mm long (figure 1k,l ). The number of cones type material of a second SSF taxon, Rushtonites [21]. Rushto- increases in larger (presumably adult) specimens, with at nites, which has previously been linked to both the Mount least four cones within a 6.3 mm-long spine (figure 1e). The dis- Cap SCFs [10] and to particular forms of Mongolitubulus [17], tance from the apex of the spine to the tip of the most distal can thus be reinterpreted as a hallucigeniid lobopodian. internal cone represents 4–10% of the total spine length; in the A further spinose SSF with probable lobopodian affinities largest specimens, the tip of the most proximal cone is located is Rhombocorniculum [22]. Like the spines of Hallucigenia, at the mid-length of the spine. Rhombocorniculum exhibits a non-flaring base, a central longitudinal cavity and a perturbed cancellate ornament [23]. Its distinctive microstructure of longitudinal, edge-parallel or slightly inclined canals has been interpreted as indicating 3. ‘Small carbonaceous’ hallucigeniid spines accretionary growth, either internally (in the manner of In light of these new data, a suite of widespread but previously protoconodonts) [23] or by microvilli (as in annelids) [24]. enigmatic SCFs can be clearly identified as isolated hallucigen- However, the internal structure and related surface lineations iid spines. These specimens are comparable in size with the in Rhombocorniculum compare favourably with the equivalently smallest Burgess Shale spines (ca 1 mm) and exhibit an identical fine-scale longitudinal lineations observed in Hallucigenia spines ornamentation of inclined scales that becomes more diffuse from the Burgess Shale and as SCFs (figures 1f,g and 2b), and towards both base and tip, with local irregularities. As in the some specimens additionally exhibit external basal constrictions Burgess Shale, some specimens exhibit a cone-in-cone construc- (e.g. [21], plate 10.1; [24]), which conceivably correspond to the tion in their apical portion and bear fine-scale longitudinal nested cone structure of H. sparsa and related SCFs. Assem- lineations (figure 2a,b,g,h). Beyond this, variations in outline blages of Rhombocorniculum often include both right- and left- suggest that the SCFs represent a diversity of hallucigeniids. handed variants, and include forms that vary considerably in Slender specimens from the Mount Cap Formation (Cambrian their aspect ratio, degree of flattening and curvature [21]. All Series 2 and 3, Northwest Territories, Canada; figure 2a–e,g,h these features are compatible with a reconstruction as a lobopo- and fig. 3.5–3.7 [10]) are indistinguishable from the spines of dian scleritome similar to that of H. hongmeia [5], in which the H. sparsa from the Burgess Shale (see also fig. 5 of [11]). By con- paired dorsal spines vary in size, outline and curvature along trast, SCF specimens from the Kaili Formation (Series 3, the length of the body. As such, it is possible that the sur- Guizhou Province, China; fig. 7a–e [12]) are more variable in face features of H. hongmeia are equivalent to the similarly shape and include robust and sometimes strongly curved distributed scales on H. sparsa spines, although extensive weath- forms resembling the spines of Hallucigenia fortis from the ering undermines a detailed comparison (see the electronic Chengjiang Lagersta¨tte (Series 2, Yunnan Province, China supplementary material). [13]). A third distinct form is represented by a specimen from Together, Rushtonites and Mongolitubulus ( partim) allow the Forteau Formation (Series 2, Newfoundland, Canada; hallucigeniids to be recognized globally among SSF assem- figure 2i–k), which has a notably broad profile and is further blages from Cambrian Stages 3–4, expanding the known Downloaded from http://rspb.royalsocietypublishing.org/ on January 19, 2017

(a) (b) (c) 3 Ba 5th d 4th Ba 3rd 20131613 280: B Soc R Proc rspb.royalsocietypublishing.org Ba 6th 2nd Ba 1st 7th 6th 5th 4th 7th 3rd head 2nd b (d) 1st

decay fluids head

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Li C1 n Li

C1 o

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Figure 1. Hallucigenia sparsa from the Burgess Shale: (a,b) Smithsonian Institution, National Museum of Natural History (NMNH) 83935 (holotype), articulated specimen, showing seven pairs of spines, partially decayed towards the rear, presumed head to the right. (a) composite image of part and counterpart; (b) enlarge- ment of the basal part of the spines; (c,d) Royal Ontario Museum (ROM) 61513, complete specimen showing seven pairs of spines and backscatter image of boxed area (d); (e–i) ROM 57776, backscatter images (overview and close-ups of boxed areas) of spine showing four internal cones and lineations; (g) ROM 61513, backscatter image showing lineations and a distal cone; ( j–o) ROM 62269, backscatter images of several spines, showing elemental distribution of carbon (l ) and phosphorous (m) and details of ornamentation near spines’ mid-length (n) and base (o) (arrows indicate local disturbances in the rhomboid pattern); (p) ROM 61513, backscatter image showing details of ornamentation showing scales in positive relief (top left) and negative relief below the carbon film. Ba, basal region of spines; C, cone; Li, lineations. Scale bars: (a–d) 1000 mm; (e,j–m) 100 mm; ( f–i)50mm; (n–p)10mm. (Online version in colour.) Downloaded from http://rspb.royalsocietypublishing.org/ on January 19, 2017

(a) (c)(g)(h h)(i) j 4 sbryloitpbihn.r rcRScB20 20131613 280: B Soc R Proc rspb.royalsocietypublishing.org

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Figure 2. Hallucigeniid spines preserved as small carbonaceous fossils. (a–h) Isolated spines from the Mount Cap Formation (Little Bear biota), northwestern Canada: (a–b) Geological Survey of Canada (GSC) 136957, showing longitudinal striations within spine; (c–f) GSC 136958, showing that the spine does not flare at its base, where the ornament thins; (g,h) GSC 136959, cone-in-cone structure and lineations within spine, surface ornament diminishing towards apex; (i–k) GSC 136960, potential new hallucigeniid morph from the Forteau Formation, Newfoundland, showing diffuse ornament and straight sides near base. C, cone; Li, lineations. Scale bars: (a,c,g–i) 100 mm; (b,d–f,j,k)25mm. (Online version in colour.) Downloaded from http://rspb.royalsocietypublishing.org/ on January 19, 2017

palaeogeographic range of the group to include England [21], Shale-type deposits to include intracratonic as well as deeper- 5 Antarctica [19], Greenland [17], Australia [18], Mongolia [25] water settings, in regions of carbonate as well as siliciclastic sbryloitpbihn.r rcRScB20 20131613 280: B Soc R Proc rspb.royalsocietypublishing.org and Kazakhstan [16,26], and complementing the macroscopic deposition, and reveal a previously unrecognized global and SCF records from northwestern Canada and south distribution of the group (see electronic supplementary mate- China (see the electronic supplementary material, table S1). rial, figure S1). Combined with the record of reticulate With the addition of Rhombocorniculum, the first appearance of Microdictyon/Onychodictyon-type sclerites [5], it is clear that hallucigeniid spines can be extended to the latest Terreneuvian armoured lobopodians were substantially more widespread (Stage 2), and the geographical range further extended and ecologically important in early to middle Cambrian com- into Siberia, North America, Baltica, and the Mediterranean munities than their whole-body record alone would suggest. [24,27,28] Subsequently, they appear to have declined: a conspicuous decrease in diversity and range in the middle to late Cambrian is now seen across three different taphonomic modes that, to an 5. Construction and growth of hallucigeniid important extent, complement one another [4]. But how much spines of this decline can be explained by changing taphonomic win- dows, and how much represents authentic biological signal? Hallucigeniid spines lack an obvious modern analogue. Burgess Shale-type preservation requires a particular However, the preservation of specimens in three different tapho- combination of ocean and sediment chemistry, and Burgess nomic modes offers new insights into their construction Shale-type deposits decline in step with the increase in bio- and growth. Several lines of evidence suggest an originally bio- turbation seen towards the end of the Cambrian [3,37]. mineralized, phosphatic component. The spines preserved as SCFs, by contrast, require a fundamentally less demanding SSFs are often robustly mineralized, and fulfil a number of criteria set of preservational conditions than their macroscopic that have been used to distinguish biophosphatic SSFs from those carbonaceous counterparts [4]. But until late Cambrian and that have been diagenetically phosphatized; notably, they occur younger assemblages are better documented, the apparent in a broad range of lithologies and typically exhibit well- decline of hallucigeniid SCFs could be attributed to a preserved internal microstructures. By contrast, the Burgess sampling artefact. ‘Exceptional’ SSF preservation also Shale specimens of H. sparsa contain only weak traces of phos- occurs in a limited timeframe, diminishing in importance phate, and the SCFs were at most lightly mineralized: they lack after an early Cambrian (Stages 2–3) peak [38]. Nevertheless, a phosphatic component (although this may have been removed the original phosphatic component of many lobopodian during diagenesis and/or laboratory processing) and, as with the sclerites would increase their preservation potential outside Burgess Shale macrofossils, are flattened with no evidence of this window of ‘exceptional’ phosphatization, subject to brittle deformation. These observations are consistent with a the extent of biomineralization. Microfossils with a similar proposed link to Rhombocorniculum, whose seemingly high original composition offer a useful taphonomic comparison. organic content [23] perhaps allowed some original pliability Notably, the organophosphatic proto- and paraconodonts [29].Overall,hallucigeniidspines seem to have had a rigid yet are thought to have been lightly mineralized in life [39], flexible construction, with a degree of phosphatic mineralization include forms of similar size and shape to hallucigeniid that may have varied between taxa. A similar organophospha- spines, and occur as both SSFs and SCFs [12]. Despite these tic composition potentially explains the range of expression of similarities in taphonomic potential, they exhibit a much Microdictyon-type sclerites [5]. wider overall range than hallucigeniids, from the very early As ecdysozoans, hallucigeniids presumably moulted their Cambrian (Fortunian) to the early Ordovician [40]. Therefore, cuticle in order to grow. Some specimens of Microdictyon and the absence of hallucigeniids (and microdictyonids) after Onychodictyon show evidence of moulting, with a larger sclerite Cambrian Stage 5 may indicate a genuine decline in biologi- preserved attached to the base of a smaller sclerite [5,30–32]. In cal importance. When armoured lobopodians went extinct is Hallucigenia, the apparent ontogenetic increase in the number of a different question; a possible example has been figured cones within a spine seems to suggest growth by the retention from the early Ordovician Fezouata biota (fig. 1e of [41]). of moults, in the manner of some arthropod structures (for Whatever the fate of the armoured lobopodians, their example, conchostracan and eridostracine carapaces [33,34]). first appearance in the fossil record in early Stage 3 or However, this hypothesis is contradicted by the restriction the latest Terreneuvian (i.e. Cambrian Stage 2—to include of scalesto the outer surface and their non-uniform arrangement, Rhombocorniculum) does not coincide with the opening of a and by the absence of external discontinuities or multiple, super- taphonomic window, but with a polyphyletic explosion in imposed exterior walls. Although moulting may seem difficult defence and biomineralization [40]; it is likely to approximate to reconcile with the cone-in-cone construction of hallucigeniid their first evolutionary appearance. Their dramatic subsequent spines, the sclerotized claws and jaws of modern onychophorans radiation, even if short-lived, saw them become important bear a comparable accretion-like pattern [35], despite being members of Cambrian marine communities. moulted with the unhardened cuticle [36]. Notwithstanding the morphogenetic mechanism that produces this pattern, Acknowledgements. We thank Christian Skovsted and two anonymous reviewers for constructive comments on this manuscript. N. J. Butterfield which has yet to be determined, a cone-in-cone construction of kindly provided all samples from the Mount Cap formation. Parks sclerotized cuticular structures provides a link, and a potential Canada provided research and collection permits to ROM teams led by synapomorphy, between hallucigeniids and onychophorans. D. Collins; P. Fenton assisted with collections. Funding statement. This work was supported by Clare College, Cambridge (M.S.), the Natural Sciences and Engineering Research Council of 6. Distribution in space and time Canada (J.B.C., Discovery grant no. 341944), Sidney Sussex College, Cambridge (T.H.) and the Natural Environment Research Council Together, SSFs and SCFs extend the known range of (to N. J. Butterfield and T.H., NERC grant reference no. NE/ hallucigeniid lobopodians beyond ‘macroscopic’ Burgess H009914/1). This is ROM Burgess Shale research project 45. Downloaded from http://rspb.royalsocietypublishing.org/ on January 19, 2017

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