- Edited by Steven M. Stanley, University of Hawaii, Honolulu, HI, and approved December 16, 2011 (received for review September 16, 2011)
Abstract
The
early history of crustaceans is obscured by strong biases in fossil
preservation, but a previously overlooked taphonomic mode yields
important complementary insights. Here we describe diverse crustacean
appendages of Middle and Late Cambrian age from shallow-marine mudstones
of the Deadwood Formation in western Canada. The fossils occur as
flattened and fragmentary carbonaceous cuticles but provide a suite of
phylogenetic and ecological data by virtue of their detailed
preservation. In addition to an unprecedented range of complex, largely
articulated filtering limbs, we identify at least four distinct types of
mandible. Together, these fossils provide the earliest evidence for
crown-group branchiopods and total-group copepods and ostracods,
extending the respective ranges of these clades back from the Devonian,
Pennsylvanian, and Ordovician. Detailed similarities with living forms
demonstrate the early origins and subsequent conservation of various
complex food-handling adaptations, including a directional mandibular
asymmetry that has persisted through half a billion years of evolution.
At the same time, the Deadwood fossils indicate profound secular changes
in crustacean ecology in terms of body size and environmental
distribution. The earliest radiation of crustaceans is largely cryptic
in the fossil record, but “small carbonaceous fossils” reveal organisms
of surprisingly modern aspect operating in an unfamiliar biosphere.
Crustaceans
are the dominant arthropods in the modern marine realm and are renowned
for their diversity, disparity, complexity, and ecologic range (1, 2). Their fossil record, however, is heavily skewed toward biomineralizing post-Cambrian forms (3),
obscuring the higher-level relationships of crustaceans and their
terrestrial mandibulate relatives, the myriapods and hexapods (4).
Nonmineralizing (pan)crustaceans have been documented in the Cambrian
fossil record but, until recently, have been represented almost
exclusively by “Orsten-type” taxa of minute body size (< 2 mm) and
limited appendage differentiation (5, 6).
In contrast, the larger-bodied crustacean-like forms preserved in
Burgess Shale-type and other macroscopic assemblages are either
assignable to much deeper phylogenetic positions (1, 6, 7), or have yet to reveal key diagnostic characters among the inner leg branches and mouthparts (8, 9).
Notably, the only macroscopic Cambrian fossil to exhibit convincing
mandibles (“jaws”) is a Late Cambrian euthycarcinoid, a probable
stem-group mandibulate (10).
Despite
this limited record, the identification of disarticulated but
unambiguously crustacean body parts among small carbonaceous fossils
(SCFs) (11) in the Early Cambrian Mount Cap Formation of NW Canada (12, 13)
points to a cryptic but significant diversity of Cambrian crustaceans.
Here we describe extensive SCF assemblages of exceptionally preserved
filtering appendages and mouthparts (mandibles) from the Middle and
Upper Cambrian Deadwood Formation of western Canada (∼488 to 510 Ma;
Cambrian Series 3—Furongian) (14).
By bridging a major taphonomic gap in body size and preservational
resolution, the Deadwood fossils provide crucial phylogenetic and
ecologic datapoints for charting a major Cambrian radiation of
crustaceans.
Geological Context
The
Deadwood Formation (broadly defined, to include the Earlie and Finnegan
formations) encompasses a broad expanse of shallow-marine, Middle to
Late Cambrian sandstones and mudstones extending through eastern parts
of the Western Canada Sedimentary Basin, the Williston Basin, and into
the Black Hills of South Dakota, its type locality (15, 16).
In Canada, the formation occurs primarily in the subsurface, with all
of the specimens in this study recovered from petroleum exploration
drillcores in southwest Saskatchewan and southeast Alberta. Unoxidized
mudstones from Ceepee Riley Lake 3-4-39-13W3 and Ceepee Reward
4-28-38-24W3 (Middle/Late Cambrian, Saskatchewan) (16) and Rio Bravo Ronald 1-6-38-15W4 (Late Cambrian, Alberta) (15) were gently dissolved in hydrofluoric acid and the isolated SCFs individually collected from the rinsed residues (see Materials and Methods and SI Text
for details of sample distributions and age). Among the several
thousand recovered specimens are significant subpopulations of cuticle
fragments that bear distinctively arthropodan spines and setae,
including an exceptionally rich diversity of crustacean body parts.
Fossil Description and Identification
The
Deadwood crustaceans are distinguished from other arthropodan remains
by diagnostic cuticular ornamentations. They come from nine samples
representing three separate assemblages, one from each drillcore (Table S1).
Mandibles are the most widely distributed elements and fall into four
distinct categories: branchiopod-type, copepod-type, ostracod-type, and
an unidentified morphology. Other crustacean remains include
comparatively delicate arrays of spines and setae, which are generally
less abundant and informative, although one sample horizon has yielded a
rich assemblage of extensively articulated branchiopod-type limbs.
Branchiopod-Type Mandibles.
The
first of two types of mandible from the Riley Lake assemblage is
distinguished by an extensive, D-shaped grinding (molar) surface (n = 17) (Fig. 1 A–H).
The specimens fall into at least three distinct “morphotypes” that
appear to be independent of both size and preservational
orientation/resolution. In the first morphotype (n = 6) (Fig. 1 A–D),
scaly lineations extend across the width of the molar surface, forming
deep ridges at the straight/concave margin and a protruding fringe
(sometimes also strong teeth) along the opposite edge (Fig. 1B). The second morphotype (n = 2) (Fig. 1 E and F)
is distinguished by its opposite polarity (which is evident once images
have been corrected for the “way-up” of slide-mounted specimens) and by
lineations that do not extend across the width of the molar surface,
but become confluent with an unornamented region bounded by marginal
nodes (Fig. S1). The third molar morphotype (n = 3) (Fig. 1 G and H)
features a region with disconnected, poorly aligned scales and no
discrete bounding margin. In all three morphotypes the mandibular
profile, as far as it is preserved, appears to be similar: one or more
long setae and a single stout spine are inserted in line with the more
acute end of the molar surface, beyond which the mandibular margin
curves away forming a pronounced “shoulder” (Fig. 1 A, C–E, G, and H).
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 μm for A–P; 30 μm for I′ and P′.)
Mandibles
with extensive, scaly molar surfaces are known from among hexapods and
myriapods as well as branchiopods, malacostracans, and remipedes (17).
However, in both overall shape and detailed ornamentation the fossil
molars are conspicuously similar to those of branchiopod crustaceans (Fig. 2 A and B). The pronounced posterior “shoulder” is characteristic of the post-molar profile in branchiopod mandibles (21, 22),
and confirms that a distinct incisor process was absent during life.
This condition is shared with branchiopods crown-wards of Rehbachiella (23), a Cambrian stem-group form (see character 14 in ref. 24).
Moreover, the first and second fossil morphotypes show striking
similarities to the right- and left-handed mandibles, respectively, of
various extant anostracan branchiopods (Fig. 2 A and B),
which suggests that they come from a single taxon displaying a complex
pattern of mandibular asymmetry adapted for enhanced food-grinding
efficiency (18, 21, 25).
A comparable pattern of continuous scale rows on the right molar vs. a
smooth region adjacent to dorsal marginal nodes on the left is a
recognized synapomorphy (see character 15 in ref. 24) of extant anostracans and Lepidocaris, a stem-anostracan from the Devonian Rhynie Chert (24, 25). The third fossil morphotype is sufficiently distinct to represent a separate—although still branchiopodan—taxon (18).
Fig. 2.
Mandibles from modern crustaceans. (A and B) Gnathal edges (molars) from the right and left mandibles, respectively, of Chirocephalus diaphanus (Branchiopoda: Anostraca); reprinted with permission from ref. 18
(copyright 1991, Koninklijke Brill NV). Labels indicate anterior (A),
posterior (P), dorsal (D), and ventral (V); a and b indicate matched
opposing regions. (C) Gnathal edge of Calanus propinquus
(Copepoda; cranial side of female right mandible; image reversed);
arrow indicates dorsal seta. Image courtesy of Jan Michels. (D) Coxa with articulated palp of Macropyxis alanlordi (Ostracoda: Podocopa: Macrocyprididae). Image courtesy of Simone Nunes Brandão (19). (E) Mandibular (coxal) gnathal edge of Danielopolina exuma (Ostracoda: Myodocopa: Halocypridina); redrawn from ref. 20. (Scale bars, 100 μm for A, B, and D; 50 μm for C; E is not drawn to scale.)
Overall,
the Deadwood molars range up to at least 230 μm long, predicting a
maximum body length of at least 10–15 mm based on scaling relationships
in extant anostracans (see figure S3 in ref. 13).
The presence in the first and second morphotypes of a moderately sized
posterior tooth and an asymmetric “tooth-groove” system points to an
ecology of mixed benthic scraping and suspension feeding, as opposed to
more exclusive predation or suspension feeding (21).
Copepod-Type Mandibles.
A
contrasting type of mandible from the Riley Lake assemblage occurs as
cuticle fragments bearing arc-shaped arrays of up to six robust teeth (n = 32) (Fig. 1 I–O). The tooth row terminates in a protruding, bristly wedge-shaped platform (n = 12) (Fig. 1 I, J, L, and M),
confirming that the fossils represent entire gnathal edges rather than
fragmentary incisors. Below the platform is inserted a papposerrate seta
that is conspicuously longer and more robust than adjacent setae, and
projects in line with the tooth row (n = 5) (Fig. 1 I′ and M).
Variation in tooth outline (from broadly conical to narrow and strongly
bicuspidate) and in the degree of secondary ornamentation (on the
apical ridge and the basal slopes) depends in part on the angle of
fossil compression, which varies from side-on to oblique or
near-“vertical,” but also exhibits a trend toward more robust and highly
ornamented teeth in larger specimens. This observation aside, large and
small specimens exhibit similar numbers of teeth and similar relative
proportions of the toothed edge and bristly platform, and are reasonably
interpreted as ontogenetic variants of a single species.
Broadly
comparable mandibles are widespread among crustaceans, but this
particular combination of fine-scale elaborations (teeth, platform, and
protruding seta), their numbers, positions, and proportions, and their
overall ontogenetic consistency, are shared only with copepods—among
which close matches for the fossils are numerous (26–29) (Fig. 2C). In particular, the prominent projecting seta (Fig. 1I′)
is comparable in form and position to the potentially homologous
“dorsal seta” (sometimes a pair of setae) found in every major order of
nonparasitic copepods [i.e., Calanoida, Cyclopoida, Platycopioida,
Misophrioida, Harpacticoida and Mormonilloida (27, 29)] (Fig. 2C).
In
contrast, comparisons with mandibles in other crustacean groups appear
to be superficial. Certain cirripedes possess a tooth row that ends in a
protrusive bristly region, although the teeth are fewer and more robust
and there is no projecting seta (30).
The series of cusped teeth found in some branchiopods are either
restricted to very early ontogenetic stages [e.g., in anostracans (31)],
or are much broader and closely packed, and unaccompanied by terminal
platforms or setae [in notostracans and laevicaudatans (22, 32)]. Among the fossil Orsten-type crustaceans, the mandibles of Skara and Bredocaris are broadly similar in profile but do not exhibit bifurcated tooth cusps, platforms, or dorsal setae (33, 34), whereas Rehbachiella is distinguished by the disproportionate expansion through ontogeny of a flattened grinding region (23).
The
specific similarities to copepod mandibles allow predictions of body
size and diet in the Deadwood species. Scaling relationships between
gnathal edge and body length in various living copepods (35, 36)
predict a prosome length of around 4.5–7 mm (and a body length ∼1–2 mm
more) for the largest intact fossil (gnathal edge length ∼270 μm) (Fig. 1J). The fragmentary remains of larger mandibles (Fig. 1 N and O)
point to still larger individuals, possibly in the centimetric range. A
correlation between diet and mandibular morphology is well-established
for living planktic calanoid copepods [Itoh's “Edge Index” (37)].
Comparisons with the similar adaptations seen in the fossil taxon,
notwithstanding its comparatively large body size and unknown planktic
or benthic habit, predict a largely herbivorous diet for the larger
specimens with comparatively robust teeth, and a more omnivorous diet
for the smaller specimens with elongate cusps, a possible ontogenetic
distinction.
Ostracod-Type Mandible.
The
third type of Deadwood mandible is represented by a single specimen
from the Rio Bravo Ronald borehole that uniquely preserves the entire
proximal mandibular body (coxa) along with its intact gnathal edge (Fig. 1P).
The coxa exhibits an elongate overall shape that narrows to an acute
apex, a large proximal opening (the insertion point in life for soft
tissues), and a palp foramen (for the attachment of more distal parts,
which have not been preserved). The gnathal edge is particularly
complex: it bears a raised toothed blade (or possibly two superimposed
blades) adjacent to three long setae set back from the edge, an
intermediate region with short setae alongside a series of toothed cusps
and a stout hooked tooth, and a bristly protruding platform (Fig. 1P′).
Other mandibular remains in this assemblage are limited to two isolated
gnathal edges that likely represent a fourth distinct type of Deadwood
mandible, and are not considered further (Fig. S2).
In
both overall morphology and details of the gnathal edge, the more
complete Rio Bravo Ronald mandible compares most closely to those of
ostracod crustaceans (Fig. 2 D and E).
Similarly shaped, markedly elongate coxae with palp foramina of
equivalent size and position are characteristic of both major living
subgroups, Myodocopa and Podocopa, presumably reflecting the distinctive
orientation, musculature, and articulation of ostracod mandibles (38).
The complexity and form of the gnathal edge appear to be shared in
particular with halocyprid myodocopes, some of which express a similar
suite of characters including a raised toothed blade with adjacent long
setae, an intermediate region with a hook-shaped spine, and a protruding
grinding surface (Fig. 2E) (20, 39). The size of the fossil is consistent with an overall body (carapace) length of around 2 mm (19).
Branchiopod-Type Limbs.
A
contrasting assemblage of SCFs, from a single thin (∼5 mm) horizon in
the Ceepee Reward borehole, lacks mandibles but contains delicate setal
armatures in unrivalled abundance and degree of articulation (n = 150) (Fig. 3).
Most conspicuously, crustacean-type “filter plates” formed from a
series of coplanar plumose setae with intersetule distances of ∼1 μm,
plus accessory setae, occur commonly as isolated structures (n > 45) (Fig. 3 A and B) and sometimes within extensive setal arrays up to 800 μm across that reveal their wider anatomical context (n ∼11) (Fig. 3 C and D and Fig. S3). Specimens that preserve a continuous underlying cuticle are demonstrably derived from a single appendage (Fig. 3D) and show that filter plates were borne on limbs with a series of up to five nodose lobes (Fig. 3D′),
along with a diversity of contrasting armatures composed variously of
pappose, coarse plumose and, most distinctively, bifurcating serrated
(“saw-toothed”) setae (Fig. 3 C and D and Fig. S3).
The absence of articulations between the nodose lobes identifies them
as the endites of either an undivided limb stem or a poorly segmented
limb branch.
Fig. 3.
Fossil branchiopod-type limbs from the Middle Cambrian Deadwood Formation (Reward assemblage). (A and B) Isolated filter plates plus accessory setae; detail (A′) shows the diagnostic setulation of plumose filtering setae. (C and D) More extensive setal arrays preserving filter plates and other armatures in situ on limbs. (C) An array representing one or more appendages; detail C′ shows a filter plate (from center-right of image; rotated). (D) Part of a single appendage that preserves a filter plate (to left) and three protruding endites (arrowed); detail D′ shows the middle endite. See Table S2 for specimen numbers. (Scale bar, 60 μm for A and B; 15 μm for A′; 100 μm for C and D; 25 μm for C′; and 35 μm for D′.)
Filter
plates are widespread and multiply convergent structures among
crustaceans, but the arcuate outlines of the Deadwood examples and their
arrangement on extensive lobose appendages are shared only with the
phyllopodous thoracic filters of branchiopods (24).
In contrast, the mouthpart filters found in certain malacostracans and
the filter-like structures in various ostracods are much larger in
proportion to the overall appendage (40, 41),
whereas the thoracic filters of euphausiacean malacostracans (“krill”)
and leptostracans/phyllocarids are linear rather than arcuate, and are
not associated with such diverse accessory armatures (42–44).
Among branchiopods, the Deadwood filters share a strictly coplanar
setal arrangement with crown-group forms, in contrast to the more 3D
armatures of Rehbachiella (23); similar combinations of filter plates and protuberant endites are known, for example, in the notostracan/diplostracan-like Castracollis from the Devonian Rhynie Chert (24, 45).
Reconstructing the Deadwood fossils as a branchiopod crustacean with a
long series of filtering thoracic appendages, an overall body length of
at least several millimeters is likely for the more articulated arrays,
although a centimetric body size is suggested by isolated filters
constructed from substantially larger setae. A mixed scraping/filtering
ecology (rather than a wholly planktic mode of life) is suggested by the
juxtaposition of filter plates and saw-toothed armatures (25).
Discussion
Cambrian
arthropods have sometimes been “shoehorned” into modern clades, despite
having character combinations that support deeper, more stem-ward
phylogenetic positions (7, 46).
Conversely, the Deadwood fossils risk being assigned to inappropriately
derived positions because of their “modern” appearance but
disarticulated condition. Therefore, we conservatively assign them to
comparatively inclusive clades, identifying crown groups via a
synapomorphy shared with a subset of the crown (46).
To
summarize, the Middle/Late Cambrian branchiopod-type fossils can all be
assigned to a subset of the branchiopod total-group that excludes Rehbachiella. Furthermore, the mandibles that express anostracan-type right-left differentiation—a directional asymmetry (47)
conserved across half a billion years of evolution—can be assigned to
the crown. The Deadwood fossils thus extend the known range of
crown-group branchiopods, as well as those crown-wards of Rehbachiella, back some 80–100 Myr from the Lower Devonian Rhynie Chert (48).
Furthermore, filter plates and scraping armatures that are strikingly
similar to those preserved in the Deadwood assemblage occur in the Mount
Cap Formation (13) (Fig. S4), extending the known range of total-group branchiopods back to the late Early Cambrian (∼510 Ma).
The
Late Cambrian ostracod-type mandible can be assigned to the ostracod
total-group and perhaps to the crown, based on the halocyprid-like
construction of the gnathal edge. Ostracod-type carapaces are known from
the Early Ordovician and may extend back to the Cambrian in the guise
of particular bradoriids (49).
However, the Deadwood mandible provides the only appendage-based
evidence for ostracods before the Silurian Herefordshire Lagerstätte, a
unit that it predates by some 70 Myr (50).
The
Middle/Late Cambrian copepod-type mandibles are assigned to the copepod
total-group (stem or crown) based on a combination of characters
including isometric growth and a dorsal seta. The Deadwood fossils thus
extend the record of copepods (broadly defined) back some 190–210 Myr
from fragments extracted from a Pennsylvanian (∼303 Ma) bitumen clast (51); other pre-Holocene records are restricted to the Miocene and Cretaceous (27).
Taken
together, our results provide unambiguous evidence for a substantial
branching by the Late Cambrian of within-crown (pan)crustacean
lineages—a largely cryptic component of the Cambrian “explosion”—and
offer key calibrations for molecular clocks and time-scaled phylogenies (48).
Complementary Taphonomic Modes.
A
Cambrian radiation of crustaceans is not evident in either the
conventional “shelly” fossil record or, apparently, macroscopic Burgess
Shale-type biotas (1). However, it is revealed to a limited extent by the small-bodied (< 2 mm) forms preserved in Orsten-type assemblages (5, 6). Among these forms, Rehbachiella has been interpreted as a stem-branchiopod (24) and others, notably Skara, Yicaris, Bredocaris, and (possibly) the metanauplius Wujicaris, as stem-group members of various higher-level “entomostracan” taxa (52–55); pentastomid-like Orsten fossils may also be crustaceans (48).
Debates over the phylogenetic affinities of the Orsten taxa have
emphasized the difficulty in interpreting larvae and miniaturized adults
(56, 57),
and it is conceivable that their apparently more plesiomorphic
positions are an artifact of their developmental stage or smaller size (13).
Importantly, the Deadwood fossils, like those of the Mount Cap (13),
reveal the microscopic anatomies of both micro- and macroscopic
(millimetric to centimetric) individuals and therefore circumvent a
major taphonomic bias. That said, even the smallest Deadwood and Mount
Cap individuals exhibit previously unseen morphologies, perhaps because
they lived in comparatively shallow-marine environments that are
undersampled by both Burgess Shale-type and Orsten-type preservation.
Mandibles, at least, are emerging as a widespread and reasonably
abundant component of SCF assemblages, conceivably as indigestible
remains sedimented via fecal pellets (26, 35, 36) or simply as biostratinomically recalcitrant seabed detritus (58).
In any case, they offer clear potential for reconciling the Orsten
forms with adults and larger-bodied relatives for a new, high-definition
narrative of early mandibulate evolution.
Evolving Crustacean Form and Function.
The
fresh taphonomic perspective of SCFs provides the only direct evidence
for sophisticated particle-handling in larger-bodied Cambrian
arthropods. This characteristically crustacean-type ecology at the
interface of micro- and macroscopic nutrient cycling has otherwise been
loosely inferred from overall body form (1) and the proxy record of phytoplankton diversification (59). The detailed adaptations described here represent the acme of Cambrian differentiation within
appendages, an alternative (and potentially correlative) measure of
evolving arthropod complexity to the larger-scale tagmosis that has been
the focus of previous studies (e.g., ref. 2).
In part, the new fossils reinforce a picture of early origination and subsequent conservation in crustacean form and function (60).
At the same time, however, the small carbonaceous record provides
evidence for unanticipated ecologic turnover. In the modern oceans,
branchiopods are represented by a just a few species of small,
secondarily marine cladocerans; larger forms, comparable in size to
those of the Deadwood (up to ∼15 mm or more) and Mount Cap (∼50 mm), are
now entirely nonmarine (24). Furthermore, modern free-living copepods are almost all much smaller than the ∼5- to 10-mm (plus) Deadwood taxon (27).
In the modern world, visual predators—especially teleost fish—drive
down body size in planktic freshwater crustacean communities (61) and strongly constrain the complex behaviors and distribution patterns of krill (62, 63),
a group that shares with the Cambrian branchiopods the attributes of
centimetric body size, marine habitat, and (by convergence) thoracic
filtering. Significantly, the Deadwood and Mount Cap fossils reveal a
contrasting pattern of crustacean distribution in the comparatively
“unescalated” Cambrian biosphere.
Materials and Methods
Washed
mudstone samples of 5–20 g were immersed in 40% hydrofluoric acid for
2–5 d before being flushed with water over a 30- or 63-μm sieve.
Individual microfossils were picked from residues suspended in water
using a pipette, rinsed in distilled water, and transferred to glass
coverslips for mounting on glass microscope slides (using epoxy resin).
Specimens were studied using transmitted light microscopy, and final
images assembled from digital photographs taken at different focal
planes. Figured specimens are stored at the Geological Survey of Canada
(GSC), 601 Booth Street, Ottawa, ON, Canada, numbered sequentially from
GSC 135369 to GSC 135393 (Table S2).
Acknowledgments
We
thank staff at the Geological Subsurface Laboratory, Regina, and Energy
Resources Conservation Board, Calgary for help with core sampling;
geoLOGIC for generous access to subsurface data; Pier Binda for
discussion of Deadwood microfossils; and Jan Michels, Simone Nunes
Brandão, and Graziella Mura for providing images. This work is supported
by Sidney Sussex College, Cambridge, and Natural Environment Research
Council Grant NE/H009914/1.
Footnotes
- ↵1To whom correspondence should be addressed. E-mail: thph2@cam.ac.uk.
- Author contributions: T.H.P.H., M.I.V., and N.J.B. performed research; T.H.P.H. analyzed data; and T.H.P.H. and N.J.B. wrote the paper.
- The authors declare no conflict of interest.
- This article is a PNAS Direct Submission.
- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1115244109/-/DCSupplemental.
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