Exceptionally preserved crustaceans from western Canada reveal a cryptic Cambrian radiation Thomas H. P. Harveya,1, Maria I. Vélezb, and Nicholas J. Butterfielda aDepartment of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ, United Kingdom; and bDepartment of Geology, University of Regina, Regina, SK, Canada S4S 0A2 Edited by Steven M. Stanley, University of Hawaii, Honolulu, HI, and approved December 16, 2011 (received for review September 16, 2011) The early history of crustaceans is obscured by strong biases in fossil Geological Context preservation, but a previously overlooked taphonomic mode yields The Deadwood Formation (broadly defined, to include the Earlie important complementary insights. Here we describe diverse crus- and Finnegan formations) encompasses a broad expanse of shal- tacean appendages of Middle and Late Cambrian age from shallow- low-marine, Middle to Late Cambrian sandstones and mudstones marine mudstones of the Deadwood Formation in western Canada. extending through eastern parts of the Western Canada Sedi- The fossils occur as flattened and fragmentary carbonaceous cuticles mentary Basin, the Williston Basin, and into the Black Hills of but provide a suite of phylogenetic and ecological data by virtue of South Dakota, its type locality (15, 16). In Canada, the formation their detailed preservation. In addition to an unprecedented range occurs primarily in the subsurface, with all of the specimens in this fi of complex, largely articulated ltering limbs, we identify at least study recovered from petroleum exploration drillcores in south- four distinct types of mandible. Together, these fossils provide the west Saskatchewan and southeast Alberta. Unoxidized mudstones earliest evidence for crown-group branchiopods and total-group from Ceepee Riley Lake 3-4-39-13W3 and Ceepee Reward 4-28- copepods and ostracods, extending the respective ranges of these 38-24W3 (Middle/Late Cambrian, Saskatchewan) (16) and Rio clades back from the Devonian, Pennsylvanian, and Ordovician. De- Bravo Ronald 1-6-38-15W4 (Late Cambrian, Alberta) (15) were tailed similarities with living forms demonstrate the early origins gently dissolved in hydrofluoric acid and the isolated SCFs in- and subsequent conservation of various complex food-handling dividually collected from the rinsed residues (see Materials and adaptations, including a directional mandibular asymmetry that Methods and SI Text for details of sample distributions and age). has persisted through half a billion years of evolution. At the same Among the several thousand recovered specimens are significant time, the Deadwood fossils indicate profound secular changes in subpopulations of cuticle fragments that bear distinctively ar- crustacean ecology in terms of body size and environmental distri- thropodan spines and setae, including an exceptionally rich di- bution. The earliest radiation of crustaceans is largely cryptic in the versity of crustacean body parts. fossil record, but “small carbonaceous fossils” reveal organisms of surprisingly modern aspect operating in an unfamiliar biosphere. Fossil Description and Identification The Deadwood crustaceans are distinguished from other ar- arthropods | phylogeny | taphonomy | Paleozoic thropodan remains by diagnostic cuticular ornamentations. They come from nine samples representing three separate assemblages, rustaceans are the dominant arthropods in the modern marine one from each drillcore (Table S1). Mandibles are the most widely Crealm and are renowned for their diversity, disparity, com- distributed elements and fall into four distinct categories: bran- plexity, and ecologic range (1, 2). Their fossil record, however, is chiopod-type, copepod-type, ostracod-type, and an unidentified heavily skewed toward biomineralizing post-Cambrian forms (3), morphology. Other crustacean remains include comparatively obscuring the higher-level relationships of crustaceans and their delicate arrays of spines and setae, which are generally less terrestrial mandibulate relatives, the myriapods and hexapods (4). abundant and informative, although one sample horizon has EVOLUTION Nonmineralizing (pan)crustaceans have been documented in the yielded a rich assemblage of extensively articulated branchiopod- Cambrian fossil record but, until recently, have been represented type limbs. almost exclusively by “Orsten-type” taxa of minute body size (< 2 Branchiopod-Type Mandibles. The first of two types of mandible mm) and limited appendage differentiation (5, 6). In contrast, the from the Riley Lake assemblage is distinguished by an extensive, larger-bodied crustacean-like forms preserved in Burgess Shale- D-shaped grinding (molar) surface (n =17)(Fig.1A–H). The type and other macroscopic assemblages are either assignable to specimens fall into at least three distinct “morphotypes” that ap- much deeper phylogenetic positions (1, 6, 7), or have yet to reveal pear to be independent of both size and preservational orienta- key diagnostic characters among the inner leg branches and tion/resolution. In the first morphotype (n =6)(Fig.1A–D), scaly EARTH, ATMOSPHERIC, mouthparts (8, 9). Notably, the only macroscopic Cambrian fossil lineations extend across the width of the molar surface, forming AND PLANETARY SCIENCES to exhibit convincing mandibles (“jaws”) is a Late Cambrian deep ridges at the straight/concave margin and a protruding fringe euthycarcinoid, a probable stem-group mandibulate (10). (sometimes also strong teeth) along the opposite edge (Fig. 1B). Despite this limited record, the identification of disarticulated The second morphotype (n =2)(Fig.1E and F)isdistinguished but unambiguously crustacean body parts among small carbona- by its opposite polarity (which is evident once images have been ceous fossils (SCFs) (11) in the Early Cambrian Mount Cap For- corrected for the “way-up” of slide-mounted specimens) and mation of NW Canada (12, 13) points to a cryptic but significant by lineations that do not extend across the width of the molar diversity of Cambrian crustaceans. Here we describe extensive SCF assemblages of exceptionally preserved filtering appendages and Author contributions: T.H.P.H., M.I.V., and N.J.B. performed research; T.H.P.H. analyzed mouthparts (mandibles) from the Middle and Upper Cambrian data; and T.H.P.H. and N.J.B. wrote the paper. ∼ Deadwood Formation of western Canada ( 488 to 510 Ma; The authors declare no conflict of interest. — Cambrian Series 3 Furongian) (14). By bridging a major tapho- This article is a PNAS Direct Submission. nomic gap in body size and preservational resolution, the Dead- 1To whom correspondence should be addressed. E-mail: [email protected]. wood fossils provide crucial phylogenetic and ecologic datapoints This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. for charting a major Cambrian radiation of crustaceans. 1073/pnas.1115244109/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1115244109 PNAS | January 31, 2012 | vol. 109 | no. 5 | 1589–1594 Downloaded by guest on October 1, 2021 Fig. 1. Fossil crustacean mandibles from the Middle and Late Cambrian Deadwood Formation. (A–H) Branchiopod-type mandibles from the Riley Lake assemblage. Morphotypes one (A–D) and two (E and F) are interpreted as the right and left mandibles from a single taxon, and morphotype three (G and H) as a distinct form. See Fig. S1 for detailed images of A, E, and F.(I–O) Copepod-type mandibles from the Riley Lake assemblage; detail I′ shows the platform and dorsal seta. (P) An ostracod-type mandible from the Rio Bravo Ronald assemblage; detail P′ magnifies the gnathal edge. Images have been reversed from slide-orientation in C, E, F, and H to show true polarity, and in J, K, N, and O for purposes of comparison. Grains of diagenetic pyrite show as opaque objects. See Table S2 for specimen numbers. (Scale bar, 50 μmforA–P;30μmforI′ and P′.) surface, but become confluent with an unornamented region various extant anostracan branchiopods (Fig. 2 A and B), which bounded by marginal nodes (Fig. S1). The third molar morpho- suggests that they come from a single taxon displaying a complex type (n =3)(Fig.1G and H) features a region with disconnected, pattern of mandibular asymmetry adapted for enhanced food- poorly aligned scales and no discrete bounding margin. In all three grinding efficiency (18, 21, 25). A comparable pattern of continu- morphotypes the mandibular profile, as far as it is preserved, ous scale rows on the right molar vs. a smooth region adjacent to appears to be similar: one or more long setae and a single stout dorsal marginal nodes on the left is a recognized synapomorphy spine are inserted in line with the more acute end of the molar (see character 15 in ref. 24) of extant anostracans and Lepidocaris, surface, beyond which the mandibular margin curves away form- a stem-anostracan from the Devonian Rhynie Chert (24, 25). The ing a pronounced “shoulder” (Fig. 1 A, C–E, G,andH). third fossil morphotype is sufficiently distinct to represent a sepa- Mandibles with extensive, scaly molar surfaces are known from rate—although still branchiopodan—taxon (18). among hexapods and myriapods as well as branchiopods, mala- Overall, the Deadwood molars range up to at least 230 μmlong, costracans, and remipedes (17). However, in both overall shape predicting a maximum body length of at least 10–15 mm based on and detailed ornamentation the fossil molars are conspicuously scaling relationships in extant anostracans (see figure S3 in ref. 13). similar to those of branchiopod