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Received 30 Dec 2013 | Accepted 7 Jan 2014 | Published 11 Feb 2014 DOI: 10.1038/ncomms4210 A new phyllopod bed-like assemblage from the Burgess Shale of the Canadian Rockies

Jean-Bernard Caron1,2,3, Robert R. Gaines4,Ce´dric Aria1,2, M. Gabriela Ma´ngano5 & Michael Streng6

Burgess Shale-type fossil assemblages provide the best evidence of the ‘Cambrian explosion’. Here we report the discovery of an extraordinary new soft-bodied fauna from the Burgess Shale. Despite its proximity (ca. 40 km) to Walcott’s original locality, the Marble Canyon fossil assemblage is distinct, and offers new insights into the initial diversification of metazoans, their early morphological disparity, and the geographic ranges and longevity of many Cambrian taxa. The arthropod-dominated assemblage is remarkable for its high density and diversity of soft-bodied fossils, as well as for its large proportion of new species (22% of total diversity) and for the preservation of hitherto unreported anatomical features, including in the chordate Metaspriggina and the arthropod Mollisonia. The presence of the stem arthropods Misszhouia and Primicaris, previously known only from the early Cambrian of China, suggests that the palaeogeographic ranges and longevity of Burgess Shale taxa may be underestimated.

1 Department of Natural History-Palaeobiology, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario, Canada M5S 2C6. 2 Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario, Canada M5S 3B2. 3 Department of Earth Sciences, University of Toronto, 25 Russell Street, Toronto, Ontario, Canada M5S 3B1. 4 Geology Department, Pomona College, 185 E. Sixth Street, Claremont, California 91711, USA. 5 Department of Geological Sciences, University of Saskatchewan, 114 Science Place, Saskatoon, Saskatchewan, Canada S7N 5E2. 6 Department of Earth Sciences, Uppsala University, Villava¨gen 16, 75236 Uppsala, Sweden. Correspondence and requests for materials should be addressed to J.-B.C. (email: [email protected]).

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urgess Shale-type deposits are critical to our understanding preservation of previously unknown or unreported anatomical of the ‘Cambrian explosion,’ because their soft-bodied features, and for the presence of taxa previously only known from Bbiotas offer far more palaeobiological and palaeo ecological the early Cambrian of China. information than is typically available from the fossil record1. A century of intensive collecting has revealed that these exceptionally preserved biotas (c. 45) occur globally2, yet most are Results characterized by relatively low-diversity faunas. Despite this Age and palaeoenvironmental setting. The new assemblage, effort, Walcott’s original Burgess Shale locality, the phyllopod discovered in 2012, occurs ca. 40 km southeast of Walcott’s Quarry bed3, remains unmatched for its exquisite preservation, in northern Kootenay National Park (Supplementary Fig. 1), in exceptional high diversity and abundance of soft-bodied taxa multiple exposures of a 2-m horizon of fine-grained claystones within a narrow stratigraphic interval4,5. Whether this assemblage near the top of the Stephen Formation (Figs 1,2). This strati- is typical of Cambrian marine communities, however, remains an graphic position and the trilobite fauna indicate that this is the open question6. The early Cambrian Chengjiang biota is also youngest assemblage yet identified from the Burgess Shale (Fig. 2 distinguished by a high diversity of soft-bodied taxa, many of and Supplementary Note 1). Local stratigraphic evidence confirms which are unique to that deposit, and by the preservation of key that the Marble Canyon assemblage, like the Walcott Quarry and anatomical features that provide particular insights into the most other soft-bodied assemblages of the Burgess Shale9,occurs origins of animal bodyplans7. Despite concerted collection efforts, in direct association with the Cathedral Escarpment, a major break our understanding of the global evolutionary and ecological in submarine topography (Supplementary Note 1). The new signals of the Cambrian ‘explosion’ is nonetheless hindered by the assemblage was preserved on the offshore margin of the scarcity and limited temporal distribution of well-preserved, escarpment, less than 3,000 m west of the locality at Stanley abundant and diverse Burgess Shale-type fossil assemblages. Glacier10, the only soft-bodied fossil assemblage presently known Here we report the discovery of arguably the most significant from atop the Cathedral Escarpment, in the ‘thin’ Stephen new Cambrian Burgess Shale-type fossil assemblage since that of Formation11. As in the Walcott Quarry4, proximity to the the Chengjiang biota in 1984 (ref. 8). The soft-bodied fossil escarpment promoted rapid entombment of fossil assemblages assemblage is noteworthy for its high proportion of new taxa— within or close to their original habitats. A distinct shallow-tier, which is surprising considering the locality’s close geographical low-diversity trace fossil assemblage that is unlike that of other and temporal proximity to the Walcott Quarry—and also for the Burgess Shale-type deposits is preserved in close vertical proximity

*

Figure 1 | Sedimentary facies. Sedimentary facies of the Stephen Formation at the Marble Canyon locality. (a,b) Carbonate mudstone and wackestone facies; (c–f) Shale facies. (a) Outcrop of carbonate mudstone and wackestone facies showing 2.25 m slump fold in lower field of view, B30 m above base of the Stephen Formation. (b) Outcrop of carbonate mudstone and wackestone facies showing 3–6 cm bedding separated by thin (o1–2.5 cm) claystone breaks that appear dark, B100 m below the Stephen-Eldon contact. (c) Outcrop of shale (calcareous claystone) in the upper Stephen Formation, B20 m below the Stephen-Eldon contact. In the study area, shales typically form resistant ledges, underlain by recessive thin bedded fine-grained carbonate lithologies. (d) Outcrop of shale in the upper Stephen Formation (B12 m below the Stephen-Eldon contact) showing two prominent dm-scale-deformed slump folds that are pervasive throughout the section and indicate deposition on a sloping surface. (e) Transmitted light micrograph of thin section of Marrella-bearing interval, showing mm-scale calcareous claystone laminae. Asterisk(*) indicates the position of the Marrella-bearing lamina, B14.2 m below the Stephen-Eldon contact. (f) Polished slab of fossil-bearing calcareous claystone from within the quarry interval, 2.99–3.08 m below the Stephen- Eldon contact. The prominent 3 cm-thick light-coloured claystone bed at the top of the image bears a particularly diverse and abundant soft-bodied fossil assemblage. Prominent dark-coloured bands at bed tops are enriched in carbonate, as observed in Burgess Shale-type deposits worldwide31. Scale bars, 1 m (a,c); 20 cm (b); 10 cm (d); 1 cm (f) and 2 mm (e).

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(Fig. 3e), the putative hemichordate Oesia15 (Fig. 3f), the annelid Burgessochaeta (Fig. 3g) and the arthropod Molaria (Fig. 3h),

Eldon previously known only rarely from the Walcott Quarry. Formation Liangshanella (Fig. 3i) is the most abundant taxon, as in the 5 2 m Walcott Quarry , followed by Oesia (Fig. 3f), the mollusc-like Quarry interval Haplophrentis (Fig. 3k) and the polychaete Burgessochaeta (Fig. 3g). Importantly, two arthropod taxa previously assumed to be endemic to the early Cambrian Chengjiang biota, the problematic Primicaris16 (Fig. 3j) and the nektaspid Misszhouia (Fig. 3l), also occur. The presence of these taxa within the Marble Canyon assemblage significantly expands their geographical and temporal ranges, and indicates that their absence from younger Burgess Shale-type assemblages was not the result of endemism or extinction, but was controlled by ecological and taphonomic factors. This finding, together with those from the recently described Early Ordovician Fezouata biota17, suggests that the longevity and geographical ranges of soft-bodied Cambrian taxa at both high and low taxonomic ranks may be severely Legend underestimated. Stephen Formation Wackestone The arthropod fauna. Among the new taxa recovered from the Nodular with very thin claystone laminae Marble Canyon locality, arthropods are prominent in both diversity and abundance, and include at least 12 new soft-bodied Mudstone morphotypes. Two of them are ‘great appendage’ stem arthro- Finely laminated pods, represented by an isoxyid with frontal appendages showing claystone and micrite distinct dinocaridid affinities (Fig. 3m), and a large leanchoiliid whose typical flagellate ‘short great appendage’ exhibits finely Shale Calcareous claystone dentate rami in addition to distal claw complex (Fig. 3n,o). These and thin-bedded micrite new forms will aid in understanding the relationships and dis- parity of megacheirans18–21 and bivalved arthropods22,23, two Slump folds groups that continue to play a pivotal role in debates surrounding Folds in thin-med. bedded carbonates the early evolution of arthropods. The new evidence emphasizes the predatorial function of leanchoiliid appendages and the likely connections between the dinocaridid and bivalved bodyplans, Carbonate mudstone 24 and wackestone which have only tentatively been explored so far , but are of Thin-med. bedded with critical importance to the evaluation of overall arthropod thin claystone laminae disparity. Another new bivalved arthropod (Fig. 3r) displays Dolostone sclerotized chelate cephalic appendages, shedding light on the Massive dolomite Cathedral Formation Clastics Sh anatomy of the problematic stem arthropod Branchiocaris Carbonates Mic Wac pretiosa. This confirms that an anterior, post-oral, chelate Figure 2 | The Stephen Formation in the vicinity of Marble Canyon. appendage appeared early, possibly deep within the stem-group 25 (a) Idealized stratigraphic section of the Stephen Formation at Marble of arthropods. The assemblage also yields the first Mollisonia Canyon, based on detailed measurements at Marble Canyon and specimen to reveal extensive details of cephalic appendages, observations at Mount Whymper, showing the location of the Marble together with eyes showing retinal and brain tissues, including Canyon fossil assemblage and quarry. (b) Photograph of the main quarry putative neuropils (Fig. 3p,q and inset). Mollisonia was previously 10 interval, comprising calcareous claystones. Mic, micrite; Sh, shale; Wac, known only from elements of the exoskeleton , with soft tissues wackestone. Scale bars, 10 m (a); 50 cm (b). never before observed. The new material suggests that the neglected taxon Houghtonites26 actually belongs to Mollisonia, and that this animal was an active benthic predator, based on the presence of large lateral eyes and long cephalic appendages. to soft-bodied fossils (Supplementary Figs 3–5), suggesting that periodic oxygenated conditions developed during deposition of the fossil-bearing interval12,13. A low-diversity shelly fossil assemblage Fidelity of preservation. The consistently high fidelity of pre- occurs in associated carbonate facies (Supplementary Fig. 6) and servation in the Marble Canyon material is striking, and expands may reflect transport from shallower water environments. the range of internal tissues preserved in Cambrian Burgess Shale-type fossils. These include a putative liver and heart in Metaspriggina (Fig. 3e), and preservation of branched tridental The Marble Canyon assemblage. The primary fossil locality (ca. caeca deep within the limbs of the new isoxyid arthropod 2 km east of Marble Canyon) has so far yielded 3,067 specimens (Fig. 3m). We also report for the first time the preservation (ca. 80% in situ) representing a total of 55 taxa (Supplementary of neural tissues in Burgess Shale material (Fig. 3p,q), which, Data 1). The fauna encompasses 11 metazoan bodyplans domi- as recently shown for Chengjiang arthropods27, promises to nated by vagile infaunal, epifaunal and nektobenthic taxa yield new phylogenetic information. Additional new anatomical (Supplementary Fig. 2). Two-thirds of the genera present are features include a putative gut and indeterminate organs in shared with the Walcott Quarry. These include the arthropods the enigmatic lophotrochozoan hyolith Haplophrentis (Fig. 3k), Alalcomenaeus (Fig. 3a), Branchiocaris (Fig. 3b), Marrella possible extruded gut content in Sidneyia (Fig. 3s), and (Fig. 3c) and Naraoia (Fig. 3d), the chordate Metaspriggina14 appendages in Liangshanella (Fig. 3i). Appendages in the

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my ey

gi he liv

ap

co+re ne ap

gc

Figure 3 | Faunal assemblage elements from Marble Canyon. (a) ROM 62967, Alalcomenaeus sp. (b) ROM 62968.1, Branchiocaris sp. (c) ROM 62969, Marrella splendens.(d) ROM 62970, Naraoia cf. compacta.(e) ROM 62938, Metaspriggina cf. walcotti with preserved eyes and internal organs (composite image of both part and counterpart—stitched images at white lines). (f) ROM 62971, Oesia cf. disjuncta.(g) ROM 62972, Burgessochaeta cf. setigera. (h) ROM 62973, Molaria spinifera.(i) ROM 62974.1, Liangshanella cf. burgessensis with preserved appendages. (j) ROM 62974.2, Primicaris cf. larvaformis. (k) ROM 62968.2, Haplophrentis cf. carinatus with preserved internal organs (arrow). (l) ROM 62975 Misszhouia cf. longicaudata.(m) ROM 62976, new isoxyid arthropod (new arthropod B), arrows indicate haemolymph channels. (n,o) ROM 62977, new leanchoiliid (new arthropod L), (n) overall view and (o) close-up showing spinose rami. (p,q) ROM 62978, Mollisonia symmetrica with preserved eyes and appendages, (p) overall view and (q) close-up showing neuropils, cornea and retina. (r) ROM 63014, new bivalved arthropod (new arthropod A). (s) ROM 62974.3, Sidneyia inexpectans, showing possible extruded gut content (arrow). ap, appendages; co þ re, cornea þ retina; ey, eyes; gc, gut content; gi, gill bars; he, heart; liv, liver; my, myomeres; ne, neuropils. Scale bars, 1 mm (i,j,o,q); 5 mm (a–c,e,g,h,k,m,p) and 10 mm (d,f,l,n,r,s).

trilobite Kootenia (Supplementary Fig. 7) are also exceptionally assemblages, or for the closely adjacent Stanley Glacier assem- preserved. blage10 (Fig. 4a, Supplementary Table 1). Differences in diversity and composition (Fig. 4b; Supplementary Table 2) between the Marble Canyon assemblage and that of Stanley Glacier are Discussion noteworthy, given the close proximity (ca. 3 km) of the two sites. To date, collection efforts at Marble Canyon have been limited to The density of fossils in the Marble Canyon assemblage, a single field season of 15 days. Yet, remarkably, the rarefaction normalized to volume of rock excavated, is significantly higher curve for Marble Canyon arthropods is markedly steeper than than that of the Chengjiang or Stanley Glacier localities, and is those for arthropods of the Walcott Quarry and Chengjiang comparable only to the Walcott Quarry (Fig. 4c; Supplementary

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Marble Canyon (this study) Stanley Glacier Data 2; Supplementary Note 2). Parallel trends in fossil density Walcott Quarry Mafang (Chengjiang) and diversity indicate that additional collection at Marble Canyon 45 holds great promise for the recovery of new taxa and for 40 enhancing the present understanding of the taxonomic diversity and morphological disparity of the Cambrian fauna. 35 Patterns in fossil associations point to the recurrence of a 30 similar community-type across the fossil-rich interval 25 (Supplementary Data 1). While this suggests that relatively 20 consistent taphonomic, ecological and environmental conditions 15 prevailed throughout the studied interval, it also highlights Generic diversity important differences in content between Marble Canyon and 10 other Cambrian soft-bodied assemblages elsewhere. Sessile 5 organisms, in particular sponges and brachiopods, which are Number of arthropods 5 0 especially abundant and diverse at the Walcott Quarry and

1 28 10 64 Chengjiang (and to a lesser extent at Stanley Glacier ), are 127 190 253 316 379 442 505 568 631 694 757 820 883 946

1,009 1,072 1,135 1,198 1,261 1,324 1,387 1,450 1,543 1,576 1,639 consistently rare at Marble Canyon. Differences in taxonomic composition, as well as in diversity and density, emphasize the Arthropoda role of palaeoenvironment in regulating ecological and Hemichordata taphonomic controls that determined the composition of soft- Mollusca (Hyolitha) bodied fossil assemblages, even across small spatial scales. Annelida While sampling methodologies, accessibility and collecting Algae efforts vary greatly among Burgess Shale-type deposits, this Chordata finding confirms that extraordinarily fossil-rich intervals of the Burgess Shale are neither limited to the type area nor to the lower Indet and middle parts of the formation, which have historically been Brachiopoda the focus of investigation. This discovery suggests that the Priapulida potential of the Burgess Shale to yield exceptional biotas across a Porifera spectrum of ecological, environmental and taphonomic gradients Ctenophora remains largely untapped. The particularly large proportion of Lobopodia new taxa that occur within the Marble Canyon assemblage, which Problematica lies in close temporal and geographical proximity to the best Chaetognatha sampled Cambrian soft-bodied assemblage, the Walcott Quarry, Cnidaria suggests that the present understanding of the diversity and Taxa Specimens Echinodermata disparity of the earliest complex ecosystems of the Phanerozoic remains in its infancy, and awaits future discoveries. 0% 70% 60% 50% 40% 30% 20% 10% 10% 20% 30% 40% 50% 60%

Specimens Taxa Methods –7 Field collections and repository information. All fossil localities visited during –4 the research are protected under the National Parks Act and all fossils and geo- –8 logical samples were collected under a Parks Canada collection and research permit –9 (YNP-2012-12054). The majority of specimens were collected in situ from a 2-m- –6 2 –10 thick interval (levels 1.75 to 3.5 m below Stephen-Eldon contact 1.5 m in All surface area) at the primary quarry site. A minority of specimens come from two –8 –11 fossiliferous intervals below the floor of the quarried interval ( 6.5 m, and –12 14.15 m to 14.25 m, respectively), while about 597 specimens (19% of total) were collected from talus along debris slopes derived primarily from the quarried –10 –13 interval. Of the 2,470 specimens identified from the quarried interval, 85% (2,082) –4 were collected and are now deposited at the Royal Ontario Museum (Invertebrate –8 Palaeontology collections). Shelly fossils from carbonate horizons were collected in the lab via acid maceration (dilute acetic and formic acids). –9 –6 All available exposures of the Stephen Formation in the vicinity of Marble –10 Canyon were measured, sampled and described in cm-scale detail in the field. –8 –11 Observations of sections on Mount Whymper were included in producing a generalized composite section (Fig. 2). Where extensive talus aprons were found to –12 Arthropods cover portions of the Stephen Formation, a laser rangefinder was used to determine –10 –13 the stratigraphic thickness of the covered interval. Samples were analysed in thin –14 section, polished slab and X-radiograph. Whole-rock chemistry was determined by –12 X-ray fluorescence using a PANalytical Axios X-ray fluorescence at the Pomona MF MC WQ MF MC WQ College. Bulk and clay mineralogy were determined by X-ray diffraction using a Rigaku Ultima IV diffractometer at the Pomona College. Figure 4 | Comparison of community attributes and density of specimens between Marble Canyon and other Burgess Shale-type deposits. (a) Rarefied generic diversity curves for arthropods. (b) Relative Fossil data sets. All fossils were identified to the lowest possible taxonomic rank abundance of taxa and specimens. (c) Violin plots of density. Black bars (usually species) and some specimens were prepared using a micro-engraving tool indicate interquartile range of log density; white dots indicate median equipped with a tungsten bit. Owing to lateral variation of individual claystone beds, fossil counts from in situ excavations were pooled into bins spanning 5 cm- of log density; surrounding coloured areas indicate Kernel density plots; thick intervals (Supplementary Data 1). Fossil assemblages used for comparative MC, Marble Canyon (magenta); MF, Mafang (black), WQ, Walcott purposes include the Walcott Quarry (Greater Phyllopod Bed)5,29, the Mafang Quarry (blue). locality of the Chengjiang deposit28,30 (fossil assemblages from event beds, only) and the nearby (o3,000 m) Stanley Glacier10 locality of the ‘thin’ Stephen Formation.

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Statistical methods. EstimateS 9.1.0 (http://www.viceroy.eeb.uconn.edu/Esti- 20. Haug, J. T., Briggs, D. E. G. & Haug, C. Morphology and function in the mateS/) was used to compute individual-based rarefaction curves to allow diversity Cambrian Burgess Shale megacheiran arthropod Leanchoilia superlata and the comparisons between different Burgess Shale assemblages. Density estimates were application of a descriptive matrix. BMC Evol. Biol. 12, 162 (2012). calculated for intervals with more than 100 specimens (for all phyla) and more than 21. Cotton, T. J. & Braddy, S. J. The phylogeny of arachnomorph arthropods and 32 specimens (for arthropods only; Supplementary Data 2; Supplementary Note 2). the origin of the Chelicerata. Trans. R. Soc. Edinb. Earth Sci. 94, 169–193 Tests and graphics were produced in R (http://www.r-project.org/), and violin plots (2004). were drawn using the ‘vioplot’ package. Kruskall–Wallis tests were significant for 22. Briggs, D. E. G. & Fortey, R. A. The early radiation and relationships of the all comparisons of density among the Mafang, Marble Canyon and Walcott Quarry major arthropod groups. Science 246, 241–243 (1989). assemblages. Mann–Whitney (or Wilcoxon) tests between the Mafang assemblage 23. Legg, D. A., Sutton, M. D., Edgecombe, G. D. & Caron, J.-B. Cambrian and either the Walcott Quarry assemblage or the Marble Canyon assemblage bivalved arthropod reveals origin of arthrodization. Proc. R. Soc. B Biol. Sci. resulted in P values 10 4. For the Walcott Quarry and Marble Canyon localities, o 279, 4699–4704 (2012). P values of Mann–Whitney tests for specimens and taxa in the whole assemblage 24. Vannier, J., Garcı´a-Bellido, D. C., Hu, S. X. & Chen, A. L. Arthropod visual were 0.43 and 0.14, respectively, thus insignificant and slightly insignificant for a predators in the early pelagic ecosystem: evidence from the Burgess Shale and confidence of 95%. When limiting the tests to arthropods, the P value was insig- Chengjiang biotas. Proc. R. Soc. London Ser. B 276, 2567–2574 (2009). nificant for specimen counts (0.36), but slightly significant for taxic counts (0.02). A one-sided version of the test finds that the density of arthropod morphotypes at 25. Simonetta, A. M. & Delle Cave, L. The Cambrian non-trilobite arthropods from Marble Canyon is greater than that of the Walcott Quarry (P value ¼ 0.01). Similar the Burgess Shale of British Columbia. A study of their comparative tests were run using the data from the Stanley Glacier assemblage; although the morphology taxonomy and evolutionary significance. Palaeontogr. Ital. 69, number of specimens overall was too low to compare with the others, density 1–37 (1975). estimates were found to be close to that of the Mafang assemblage. 26. Raymond, P. E. Notes on invertebrate fossils, with descriptions of new species. Bull. Mus. Comp. Zool. Harv. Univ. 55, 165–213 (1931). 27. Tanaka, G., Hou, X., Ma, X., Edgecombe, G. D. & Strausfeld, N. J. Chelicerate neural ground pattern in a Cambrian great appendage arthropod. Nature 502, References 364–367 (2013). 1. Conway Morris, S. Burgess Shale faunas and the Cambrian explosion. Science 28. Zhao, F. et al. Diversity and species abundance patterns of the early 246, 339–346 (1989). Cambrian (Series 2, Stage 3) Chengjiang Biota from China. Paleobiology 40, 2. Conway Morris, S. Burgess Shale-type faunas in the context of the ‘Cambrian 50–69 (2013). explosion’: a review. J. Geol. Soc. Lond. 149, 631–636 (1992). 29. Caron, J.-B. & Jackson, D. A. Taphonomy of the Greater Phyllopod Bed 3. Whittington, H. B. The Burgess Shale: history of research and preservation of Community, Burgess Shale. Palaios 21, 451–465 (2006). fossils. Proc. N. Am. Paleontol. Convention. 1969 (Part 1 Extraordinary Fossils): 30. Zhao, F., Caron, J.-B., Hu, S. X. & Zhu, M. Quantitative analysis of taphofacies 1170–1201 (1971). and paleocommunities in the Early Cambrian Chengjiang Lagersta¨tte. Palaios 4. Conway Morris, S. The community structure of the Middle Cambrian 24, 826–839 (2009). phyllopod bed (Burgess Shale). Palaeontology 29, 423–467 (1986). 31. Gaines, R. R. et al. Mechanism for Burgess Shale-type preservation. Proc. Natl 5. Caron, J.-B. & Jackson, D. A. Paleoecology of the Greater Phyllopod Bed Acad. Sci. USA 109, 5180–5184 (2012). community, Burgess Shale. Palaeogeogr. Palaeoclimatol. Palaeoecol. 258, 222–256 (2008). 6. Conway Morris, S. & Peel, J. S. A new helcionelloid mollusk from the Middle Acknowledgements Cambrian Burgess Shale, Canada. J. Paleontol. 87, 1067–1070 (2013). We thank Simon Conway Morris for comments on earlier drafts of the manuscript, and 7. Ou, Q., Shu, D. & Mayer, G. Cambrian lobopodians and extant onychophorans Gerd Geyer, Lars Holmer, Elena Naimark, David Rudkin and Mark Webster for iden- provide new insights into early cephalization in Panarthropoda. Nat. Commun. tification of brachiopods and trilobites and Fangchen Zhao for data from the Mafang 3, 1261 (2012). fossil assemblage. We thank Todd Keith (Parks Canada) and Peter Fenton (Royal 8. Zhang, W. T. & Hou, X. G. Preliminary notes on the occurrence of the unusual Ontario Museum) for logistical support, and Alan Byers and Diego Balseiro for assistance trilobite Naraoia in Asia. Acta Paleontol. Sinica 24, 591–595 (1985). in the field. Financial support for the 2012 expedition comes from the Royal Ontario 9. Collins, D., Briggs, D. E. G. & Conway Morris, S. New Burgess Shale fossil Museum (J.-B.C.), Uppsala University and the Swedish Research Council (M.S.), Pomona sites reveal Middle Cambrian faunal complex. Science 222, 163–167 College (R.R.G.), Natural Sciences and Engineering Research Council Discovery Grants (1983). (to J.-B.C. #341944 and to M.G.M. #311727), and from the US National Science Foun- 10. Caron, J.-B., Gaines, R., Ma´ngano, G., Streng, M. & Daley, A. A new Burgess dation (to R.R.G. #EAR-1046233). This is Royal Ontario Museum Burgess Shale project Shale-type assemblage from the "thin" Stephen Formation of the Southern number 50. Canadian Rockies. Geology 38, 811–814 (2010). 11. Gaines, R. R. A new Burgess Shale-type locality in the ‘‘thin’’ Stephen Author contributions Formation, Kootenay National Park, British Columbia: stratigraphic and J.-B.C. led the field expedition and prepared, identified and photographed fossil material paleoenvironmental setting. Palaeontogr. Canad. 31, 73–86 (2011). and conducted rarefaction analyses. R.R.G. and M.S. measured and described sections in 12. Gaines, R. R. et al. Burgess Shale type biotas were not entirely burrowed the field, and R.R.G. contributed stratigraphic and sedimentologic data. J.-B.C. and away. Geology 40, 283–286 (2012). R.R.G. wrote early drafts of paper, C.A. contributed a section on arthropods and sta- 13. Gaines, R. R. & Droser, M. L. The paleoredox setting of Burgess Shale-type tistical tests for density analyses, M.G.M. provided ichnologic data, M.S. provided data on deposits. Palaeogeogr. Palaeoclimatol. Palaeoecol. 297, 649–661 (2010). the shelly fauna from carbonate layers, and all authors participated in field work, dis- 14. Conway Morris, S. A redescription of a rare chordate, Metaspriggina walcotti cussed results and participated in development of conclusions. Simonetta and Insom, from the Burgess Shale (Middle Cambrian), British Columbia, Canada. J. Paleontol. 82, 424–430 (2008). 15. Conway Morris, S. The Burgess Shale animal Oesia is not a chaetognath: a reply Additional information to Szaniawski (2005). Acta Palaeontol. Pol. 54, 175–179 (2009). Supplementary Information accompanies this paper at http://www.nature.com/ 16. Zhang, X. L., Shu, D. G. & Erwin, D. H. Cambrian naraoiids (Arthropoda): naturecommunications morphology, ontogeny, systematics, and evolutionary relationships. J. Paleontol. 81, 1–52 (2007). Competing financial interests: The authors declare no competing financial interests. 17. Van Roy, P. et al. Ordovician faunas of Burgess Shale type. Nature 465, Reprints and permission information is available online at http://npg.nature.com/ 215–218 (2010). reprintsandpermissions/ 18. Hou, X. G. & Bergstro¨m, J. Arthropods of the Lower Cambrian Chengjiang fauna, southwest China. Fossils and Strata 45, 111–116 (1997). How to cite this article: Caron, J.-B. et al. A new phyllopod bed-like assemblage from the 19. Bergstro¨m, J. The oldest arthropods and the origin of Crustacea. Acta Zool. 73, Burgess Shale of the Canadian Rockies. Nat. 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6 NATURE COMMUNICATIONS | 5:3210 | DOI: 10.1038/ncomms4210 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved.

Supplementary Figure 1 | Location maps. a, Map of Canada and general location of study area (star). b, Detailed map of the study area in northern Kootenay National Park (British Columbia, Canada). The magenta dashed line indicates the approximate position of the Cathedral Escarpment in the study area, as inferred from abrupt changes in the thickness and stratigraphic architecture of the Stephen Formation. Blue boxes mark the positions of fossil localities lying offshore of the escarpment in the ‘basinal’ Stephen Formation at Marble Canyon (MC) and on Mt. Whymper (MW), yellow boxes show the locations of fossil localities atop the escarpment in the ‘thin’ Stephen Formation in the vicinity of Stanley Glacier (SG) and on Mt. Whymper (MW).

Supplementary Figure 2 | Histogram of relative abundance of main ecological groups per specimens and taxa at Marble Canyon. Data based on total number of specimens (3067) and taxa (55) from Marble Canyon. Vertical axis, relative frequency. IV=Infaunal Vagile, ES=Epibenthic Sessile, EV=Epibenthic Vagile, NK=Nektobenthic, Pe=Pelagic.

Supplementary Figure 3 | Field photographs of the ichnotaxon Fuersichnus isp. in shale layers at Marble Canyon. Horizon is approximately 11.85 m below the Stephen- Eldon contact, approximately 8 m below the primary fossil-bearing interval, and 2.25 m above a secondary soft-bodied fossil interval that includes Marrella splendens, 14.15- 14.25 m below the Stephen-Eldon contact. Isolated Fuersichnus isp. specimens also occur in discrete horizons within the main quarried interval, 1.75 to 3.5 meters below the Stephen-Eldon contact. a, General bedding-plane view of monospecific trace fossil assemblage. b, Close-up of bedding plane showing high density and typical banana-like morphology. c, General view of low-density assemblage on a bedding plane. d, Bedding plane exhibiting banana-like morphology and spreite indicative of lateral migration of the causative burrow. e, Cross-section view, showing penetrative bioturbation and disturbance of the primary sedimentary fabric. Scale bars = 2 cm (a), and 1 cm (b-e).

Supplementary Figure 4 | Field photographs of Fuersichnus isp. and Cheiichnus isp. in shale layers at Marble Canyon. Horizon is approximately 11.85 m below the Stephen-Eldon contact, approximately 8 m below the primary fossil-bearing interval, and 2.25 m above a secondary soft-bodied fossil interval dominated by Marrella splendens, 14.15-14.25 m below the Stephen-Eldon contact. a, General bedding-plane view showing high-density of Fuersichnus isp. and local presence of Cheiichnus isp. (Ch). b, Close-up of Fuersichnus isp. (Fu) and local presence of Cheiichnus isp. (Ch). c, Close-up of Cheiichnus isp., showing fine preservation of scratch mark ornamentation. Scale bars = 2 cm (a), and 1 cm (b-c).

Supplementary Figure 5 | Arthropod trackways, including examples occurring in close vertical proximity to intervals bearing soft-bodied fossils at Marble Canyon excavation sites. a. ROM 62979, trackway (approximately 14.11 m below the Stephen- Eldon contact) approximately 11 m below the primary fossil-bearing interval but within mm from a secondary soft-bodied fossil interval which includes Marrella splendens, 14.15-14.25 m below the Stephen-Eldon contact. b-c. ROM 62980, the arthropod Sidneyia (top right) and short trackway (top left and close up in c) (approximately 2.9 m below the Stephen-Eldon contact). Scale bars = 2 cm.

Supplementary Figure 6 | Shelly fossils from the carbonate mudstone and wackestone interval underlying the fossiliferous shales at Marble Canyon. Specimens found approximately 25 to 35 m below the Stephen-Eldon contact. a-c ROM 62981, Elrathina cf. marginalis, cranidium in dorsal, anterior, and left lateral view (talus from the carbonate interval); d, e, h, Itagnostus cf. interstrictus (28.3 m below the Stephen-Eldon contact); d, e, ROM 62982, 62983 two specimens in dorsal view; h, left lateral view of e; f, ROM 62984, Bathyuriscus sp., incomplete pygidium (28.3 m below the Stephen-Eldon contact); g, ROM 62985, Ptychagnostus cf. praecurrens, cephalon (talus from the carbonate interval); i, j, ROM 62986, Ehmaniella sp., juvenile cranidium in dorsal and right lateral view (27.0 m below the Stephen-Eldon contact); k, n, Prototreta n. sp. aff. P. interrupta (talus from the carbonate interval); k, ROM 62987, procline ventral valve in ventral view; n, ROM 62991, dorsal valve in ventral view with high blade-like median septum; l, ROM 62988, Eoobolus sp., exterior of incomplete dorsal valve (talus from the carbonate interval); m, p, ROM 62989, 62990, Linnarssonia sp. (talus from the carbonate interval); m, interior of dorsal valve with low median ridge; p, interior of fragmentary ventral valve with elevated apical process; o, q, ROM 63012, bradoriid, n. gen. n. sp., right? valve in lateral and ventral view (talus from the carbonate interval); r, ROM 62992, Mellopegma sp. aff. M. georginense, lateral view, note atypically straight ventral margin (28.3 m below the Stephen-Eldon contact). Scale bars = 10 mm (f), 5 mm (a-e, h), 2.5 mm (i, j), 1.5 mm (r), and 1 mm (g, k-g).

Supplementary Figure 7 | Agnostids and trilobites from shale intervals at Marble Canyon. a, ROM 63016.1, Itagnostus interstrictus (level -3.17 m). b, ROM 63016.2, peronopsoid species 1 (Laurie, 2006; Elena Naimark, Pers. Comm. 2013) (level -3.17 m). c, ROM 63017, Kootenia cf. burgessensis with preserved appendages (level -3.34 m). d, ROM 63018, Zacanthoides d, ROM 63018, Zacanthoides sp., inverted image of specimen preserved in negative relief (level -3.31 m). All levels given are in meters below the Stephen-Eldon contact. Scale bars = 2 mm (a, b), 10 mm (c, d).

Supplementary Table 1 | Arthropod Data matrix. Number of arthropods (in bold) used for rarefaction analyses for the Walcott Quarry (Greater Phyllopod bed), Stanley Glacier, and for the Mafang (Chengjiang) deposit.

Supplementary Table 2 | Relative abundance of specimens and taxa. Data comes from the Walcott Quarry (Greater Phyllopod bed), Stanley Glacier, and the Mafang (Chengjiang) assemblages.

Supplementary Note 1 | Agnostids and trilobite biostratigraphy and stratigraphic interpretations.

The Marble Canyon assemblage lies within the upper part of the Ehmaniella trilobite biozone (Ehmaniella burgessensis faunule) within the uppermost part of Cambrian Stage 5 as indicated by the presence of the trilobites Bathyuriscus sp., Ehmaniella cf. E. burgessensis, Itagnostus cf. interstrictus and Ptychagnostus cf. praecurrens.

The main locality lies less than 400 meters from the closest exposures of the typical ‘thin’ Stephen Formation, yet is distinguished by a significantly greater thickness and by fundamental differences in cycle architecture that reveal a sharp shift in depositional environments across the escarpment. Whereas the ‘thin’ Stephen Formation in the study area is approximately 35 meters thick and conformably overlies shallow water algal carbonates10,11, the basinal expression of the formation observed at Marble Canyon is approximately four times as thick (135 meters) and is separated from the underlying Cathedral Formation by a slide surface with at least six meters of local relief. The Marble Canyon section is consistently fine-grained compared to local expressions of the ‘thin’ Stephen Formation, which are characterized by grain-rich amalgamated carbonates that form clear cycle tops10,11. The lack of grain-rich carbonates and absence of well- developed depositional cycles at Marble Canyon indicates that the locality lay under sufficiently deep water that it was not subject to the pronounced changes in depositional energy during sea level oscillations that strongly affected immediately adjacent environments atop the escarpment.

Supplementary Note 2 | Density statistical tests.

1] Total density —

a] Specimens

Kruskal-Wallis rank sum test chi-squared = 22.7068, p-value = 1.173e-05

Wilcoxon rank sum test Walcott*Mafang W = 343, p-value = 2.821e-08

Wilcoxon rank sum test Walcott*Marble Canyon

W = 98, p-value = 0.4263

Wilcoxon rank sum test Mafang*Marble Canyon W = 0, p-value = 0.0001028

b] Species

Kruskal-Wallis rank sum test chi-squared = 24.8232, p-value = 4.071e-06

Wilcoxon rank sum test Walcott*Mafang W = 348, p-value = 2.508e-09

Wilcoxon rank sum test Walcott*Marble Canyon W = 78, p-value = 0.1401

Wilcoxon rank sum test Mafang*Marble Canyon W = 0, p-value = 0.0001028

1] Arthropod density

a] Specimens

Kruskal-Wallis rank sum test chi-squared = 21.7641, p-value = 1.879e-05

Wilcoxon rank sum test Walcott*Mafang W = 337, p-value = 2.295e-07

Wilcoxon rank sum test Walcott*Marble Canyon

W = 110, p-value = 0.3642

Wilcoxon rank sum test Mafang*Marble Canyon W = 0, p-value = 4.571e-05

b] Species

Kruskal-Wallis rank sum test chi-squared = 26.9073, p-value = 1.436e-06

Wilcoxon rank sum test Walcott*Mafang W = 347, p-value = 4.388e-09

Wilcoxon rank sum test Walcott*Marble Canyon W = 65, p-value = 0.02005

Wilcoxon rank sum test Mafang*Marble Canyon W = 0, p-value = 0.0004366

Tailed Wilcoxon rank sum test Walcott*Marble Canyon (alternative = greater) W = 65, p-value = 0.01002