Abstract
Recent fossil discoveries from the lower Cambrian Emu Bay Shale (EBS) on Kangaroo Island, South Australia, have provided critical insights into the tempo of the Cambrian explosion of animals, such as the origin and seemingly rapid evolution of arthropod compound eyes, as well as extending the geographical ranges of several groups to the East Gondwanan margin, supporting close faunal affinities with South China. The EBS also holds great potential for broadening knowledge on taphonomic pathways involved in the exceptional preservation of fossils in Cambrian Konservat-Lagerstätten. EBS fossils display a range of taphonomic modes for a variety of soft tissues, especially phosphatization and pyritization, in some cases recording a level of anatomical detail that is absent from most Cambrian Konservat-Lagerstätten.
The lower Cambrian (Series 2, Stage 4) Emu Bay Shale (EBS) Konservat-Lagerstätte (Fig. 1) provides important information regarding the composition of early animal communities and a window on the Cambrian radiation in Gondwana. One of the most intriguing aspects of the EBS is that although it yields a biota that is taxonomically similar to Cambrian Burgess Shale-type biotas (Paterson et al. 2008), its nearshore depositional setting (Gehling et al. 2011) and disparate preservation styles (e.g. Briggs & Nedin 1997; Lee et al. 2011; Paterson et al. 2011) are at odds with our current understanding of typical Burgess Shale-type deposits and their associated taphonomic pathways and signatures (Gaines et al. 2008, 2012b). This has led Gaines (2014) to explicitly exclude the EBS from the global list of more than 50 known Burgess Shale-type deposits, pending detailed comparative study.
Geology of the area to the east of Emu Bay on the NE coast of Kangaroo Island, South Australia, showing the extent of the Emu Bay Shale at Big Gully, including the location of the main Konservat-Lagerstätte sites on the shoreline and at Buck Quarry (after Gehling et al. 2011).
Shelly fossils were first discovered in the EBS at Emu Bay in 1952 by Reginald Sprigg. In 1954, Brian Daily found large specimens of the trilobite Redlichia in the EBS at Big Gully, east of Emu Bay. However, the first description of soft-bodied EBS fossils was not published until the late 1970s (Glaessner 1979). The history of investigations on the EBS Konservat-Lagerstätte was documented by Paterson et al. (2008) and Jago & Cooper (2011).
Age, geology and palaeoenvironmental setting
The Emu Bay Shale is a formation of the lower Cambrian (Series 2) Kangaroo Island Group, a largely clastic shelf succession within the Stansbury Basin (Daily et al. 1980; Gehling et al. 2011; Jago et al. 2012). During deposition of the EBS and adjacent units, South Australia was located on the palaeoequator in the ‘tropical carbonate development zone’ (Brock et al. 2000), and formed a part of the East Gondwana margin (Torsvik & Cocks 2013). The EBS correlates with the lower Cambrian (Series 2, Stage 4) Pararaia janeae trilobite Zone of mainland South Australia, based on the presence of the trilobites Estaingia bilobata, Balcoracania dailyi and Redlichia takooensis (Jell in Bengtson et al. 1990; Jago et al. 2006; Paterson & Brock 2007; Paterson et al. 2008). This equates to the Canglangpuan Stage (= upper Nangaoan–lower Duyunian stages) of South China and the middle–upper Botoman of Siberia (Paterson & Brock 2007; Peng et al. 2012; Landing et al. 2013). Based on the calibrated 2012 Geologic Time Scale, the numerical age of the EBS is 514 ± 1 Ma (see Peng et al. 2012, fig. 19.3). The EBS is approximately coeval with the Balang and Guanshan biotas of China, but younger than the Chengjiang and Sirius Passet Lagerstätten (Peng et al. 2012).
The EBS is exposed in two areas of the northeastern coast of Kangaroo Island: (1) the type section on the western side of Emu Bay (Daily et al. 1980); (2) Big Gully, to the east of Emu Bay (Fig. 1; Gehling et al. 2011); it is only the latter site that hosts the Konservat-Lagerstätte. At Big Gully, the EBS unconformably overlies the Marsden Sandstone, a coarsening upward package of clastic sediments deposited in a shallow subtidal to shoreface setting. The base of the EBS represents a sequence boundary and is marked by a conglomerate (up to 2 m thick) that contains various clast types and sizes, including sandstone from the Marsden Sandstone. Above the conglomerate, there is a sharp transition into mudstones that contain the Konservat-Lagerstätte, which is restricted to the lower 10 m or so of the unit. Above this, sandstones become increasingly prominent and, towards the top of the formation, contain large arthropod traces. The EBS is conformably overlain by the red–brown feldspathic sandstones of the subtidal Boxing Bay Formation, which also contain abundant arthropod traces (Gehling et al. 2011).
The interval of the EBS containing the Konservat-Lagerstätte consists of dark grey, typically laminated micaceous mudstone, with common interbeds of siltstone (up to 5 cm thick) and fine sandstone (up to 20 cm thick) that probably resulted from intermittent sediment gravity flows (Gehling et al. 2011). The mudstones show signs of small-scale fluidization, with the siltstones or sandstones occasionally loading into the underlying mudstones, resulting in flame structures. The mudstones do not appear to be bioturbated (especially where the soft-bodied fossils occur) and, in combination with the presence of sedimentary pyrite (McKirdy et al. 2011) and pyritized soft tissues (Paterson et al. 2011), indicate anoxia below the sediment–water interface based on comparisons with Cambrian Burgess Shale-type deposits (Gabbott et al. 2004; Gaines & Droser 2005, 2010; Gaines et al. 2012a,b; Gaines 2014). Geochemical studies also indicate anoxic conditions within the sediment (Hall et al. 2011; McKirdy et al. 2011), perhaps owing to the sealing of the substrate by microbial mats (although there is no unequivocal physical evidence of them), thus generating a sharp redox boundary. If microbial mats were responsible for a permeability barrier at the sediment–water interface, this may provide a taphonomic alternative to the early sealing of sediments by pervasive carbonate cements that is typical of Burgess Shale-type preservation sensu stricto (Gaines et al. 2012b; Gaines 2014); interestingly, there are claims for microbial mats in the Sirius Passet Lagerstätte (Mángano et al. 2012). Moreover, EBS studies (McKirdy et al. 2011; Hall et al. 2011) suggested that the benthos and water column were well oxygenated, which is supported (in part) by the low organic carbon content in the mudstones, in addition to redox-sensitive trace element ratios (but see Gaines (2014, p. 132) regarding their reliability as redox proxies). However, low total organic carbon values (<1%) can also be explained by low primary productivity and/or high sedimentation rates diluting the organic matter. Notwithstanding, an oxic water column is further suggested by a diverse and abundant nektobenthic–pelagic fauna, but the question of fully aerobic versus dysaerobic–anaerobic conditions on the seafloor requires further investigation (discussed below).
The EBS seems to have been rapidly deposited in a relatively nearshore setting adjacent to an active tectonic margin that generated continual syndepositional faulting and slumping. The Konservat-Lagerstätte interval appears to form part of a localized, deeper-water micro-basin succession on the inner shelf that was subject to fluctuating oxygen levels, at least in the bottom waters (Gehling et al. 2011). This depositional setting is in stark contrast to the majority of other Cambrian Konservat-Lagerstätten, specifically Burgess Shale-type deposits that formed in outer shelf environments, either near or immediately adjacent to the seaward margins of expansive carbonate platforms (e.g. Burgess Shale), or offshore of broad clastic shelves (e.g. Chengjiang) (Gaines 2014).
The Emu Bay Shale biota: diversity and palaeobiogeographical affinities
Of the 50+ species now known from the EBS, around 30% possess biomineralized structures, the remainder being entirely soft-bodied. However, in terms of the relative abundance of specimens, biomineralized taxa prevail because of the numerical dominance of the trilobite Estaingia bilobata (up to 80% of individuals on any given bedding surface).
As in Cambrian Burgess Shale-type biotas (Caron & Jackson 2008; Caron et al. 2014; Zhao et al. 2014), species diversity and abundance in the EBS are dominated by panarthropods, which comprise 28 recorded species to date, with several yet to be described. The survey of the biota below is accordingly focused on arthropods, with taxonomic groups drawing on the classification of Legg et al. (2013). Other major groups represented include sponges, molluscs, brachiopods, cycloneuralian worms and a single species of annelid. Some groups of debated affinity that are known from other Cambrian Burgess Shale-type deposits are represented by single species in the EBS, including chancelloriids, the probably deuterostome ‘cambroernids’ (incorporating the rotadiscids), and the vetulicolians (see Box 1; Fig. 2).
Box 1. Nesonektris and the affinities of vetulicolians
Vetulicolians are Cambrian animals known from 15 named species that occur in the Chengjiang and Guanshan biotas of China, Sirius Passet and the Burgess Shale. An EBS vetulicolian, Nesonektris aldridgei García-Bellido et al. 2014, demonstrated that their distribution extended to East Gondwana. Vetulicolians were originally interpreted as bivalved arthropods because their bipartite body is divided into an anterior part that has some similarities to a carapace and a posterior part composed of segments separated by soft intersegmental regions. Arthropod affinities were challenged by the absence of limbs and by the discovery of features that were more consistent with alternative (specifically deuterostome) affinities. Based especially on a series of openings in the anterior part of the body interpreted as gill slits (Shu et al. 2010), the deuterostome hypothesis has generally found favour (Aldridge et al. 2007; Vinther et al. 2011; Ou et al. 2012; Smith 2012). Nonetheless, the question of whether vetulicolians belong to the deuterostome stem-group or are more closely related to one of the extant deuterostome subgroups (thus making them crown-group Deuterostomia) remains unclear. The bipartite division of the body had been argued to suggest affinities to tunicates (Lacalli 2002), implying membership of Vetulicolia within Chordata. This systematic position would predict the presence of a notochord in vetulicolians, and indeed an axial rod that runs through the posterior body part of Nesonektris displays some morphological and preservational features consistent with its identity as a notochord. In particular, specimens show the rod fragmenting into sections, similar to the early decay stages of the notochord in Amphioxus and jawless vertebrates (Sansom et al. 2013). In addition to their bipartite bodies, vetulicolians and tunicates share a thick cuticle, a terminally positioned mouth, and restriction of the notochord to the segmented posterior part of the body.
(a) Reconstruction of Nesonektris aldridgei; by Katrina Kenny. (b) Axial rod structure of N. aldridgei (SAM P46336a) interpreted as a putative notochord, with arrows showing offset blocks. (c) Phylogenetic position of vetulicolians within Deuterostomia, based on the analysis by García-Bellido et al. (2014); parsimony-bootstrap values (above branches) and Bremer support (below) are shown for analyses including/excluding the non-vetulicolian fossil taxa.
Arthropods
Trilobites
Five species have been identified in the EBS (Jell in Bengtson et al. 1990; Paterson & Jago 2006), two of which are abundant (Estaingia bilobata and Redlichia takooensis: Fig. 3a) whereas the remaining three are very rare (Balcoracania dailyi, Holyoakia simpsoni and Megapharanaspis nedini). The trilobites suggest strong biogeographical connections with South China and Antarctica; as outlined below, many of the non-biomineralized species in the EBS have their closest relatives in the Chengjiang biota and amplify the signal for affinities to South China. Estaingia is restricted to East Gondwana (Australia and Antarctica) and South China (Dai & Zhang 2012). Redlichia takooensis, by far the largest trilobite in the biota (articulated specimens up to 25 cm long), was originally described from South China. Holyoakia is otherwise known from the type species in the Central Transantarctic Mountains (Palmer & Rowell 1995). Balcoracania was originally documented from sites in South Australia, but subsequently found in Antarctica (Palmer & Rowell 1995). Balcoracania dailyi is noteworthy for having the largest number of thoracic segments (103) known from any trilobite anywhere in the world (Paterson & Edgecombe 2006).
Emu Bay Shale arthropods. (a) Redlichia takooensis (left, SAM P52235) and Estaingia bilobata (right, SAM P52236). (b) Kangacaris zhangi (SAM P45179b). (c) Australimicola spriggi (SAM P44482a). (d) New cheliceriform arthropod (SAM P45427). (e) Squamacula buckorum (SAM P15347a). (f) Tanglangia rangatanga (SAM P46331a, mirrored). (g) Oestokerkus megacholix (SAM P43631a, mirrored). (h) Isoxys communis (SAM P47179a). (i) Tuzoia australis (SAM P47994a). (j, k) Anomalocaris cf. canadensis (SAM P51398a); (j) pair of frontal appendages and oral cone; (k) detail of ventral spine. Scale bars: (a–f) 5 mm; (g–j) 10 mm; (k) 3 mm. All photos in Figures 2–6 taken with Canon EOS 50D, under natural or tungsten light from NE and NW at low angle. Illustrations composed and processed, for fine-tune light intensity across figures, with Adobe Photoshop CS3.
Other lamellipedian arthropods
The names Lamellipedia and Artiopoda refer to trilobites and their (mostly non-biomineralized) relatives. Emucaris fava and Kangacaris zhangi (Fig. 3b), both blind species, belong to the family Emucarididae, originally known only from the EBS (Paterson et al. 2010). The only other record of the family is a species from Chengjiang assigned to Kangacaris (Zhang et al. 2012). Another blind arthropod in the EBS, Australimicola spriggi (Fig. 3c), was originally classified in a lamellipedian group named Conciliterga, with which it shares its style of hypostome attachment (Paterson et al. 2012), but other phylogenetic analyses have grouped it with Cheloniellida, known from various species in the Ordovician, Silurian and Devonian (Stein et al. 2013).
Cheliceriform and ‘great appendage’ arthropods
A common EBS arthropod (Fig. 3d), the description of which is currently pending publication, has 11 trunk segments, a large paddle-shaped telson and massive gnathobases on its cephalic appendages, suggesting a relationship to Sanctacaris, Utahcaris and probably also Sidneyia (Conway Morris & Robison 1988; Legg 2014). Comparisons with Sidneyia have also been made in the case of another EBS arthropod, Squamacula buckorum (Fig. 3e; Paterson et al. 2012; Stein et al. 2013). Squamacula is otherwise recorded only in Chengjiang (Zhang et al. 2004), providing one of numerous biogeographical links between the EBS and South China.
Oestokerkus megacholix (Fig. 3g) belongs to the same family as the Burgess Shale and Chengjiang ‘great appendage’ arthropods Leanchoilia and Alalcomenaeus (Edgecombe et al. 2011). With these other leanchoiliids, it shares a long flagellum on each of three spine-bearing articles of the great appendage (the first head appendage). Another ‘great appendage’ arthropod, Tanglangia rangatanga (Fig. 3f), is the second known species of this genus, otherwise recorded only from Chengjiang. The Australian and Chinese species share a quadrate cephalic shield, a narrow trunk of 13 segments, and a styliform telson that is as long as the trunk (Paterson et al. 2015).
Bivalved stem-group arthropods
The genera Isoxys and Tuzoia, both of which have a ‘bivalved’ carapace, are known from many lower and middle Cambrian Konservat-Lagerstätten, and each is represented in the EBS by two species (García-Bellido et al. 2009). The common EBS species, I. communis (Fig. 3h), includes specimens preserving the eyes, the anteriormost cephalic appendage, a series of phosphatized midgut glands, and the trunk segments bearing biramous appendages extending behind the carapace. A second species of Isoxys, I. glaessneri, is smaller, with smooth valves and short cardinal spines. Tuzoia is characterized by coarse polygonal ornament, a spiniferous lateral ridge on each carapace valve, and marginal spines in stereotypical positions. The genus is mostly known from empty carapaces in all its occurrences worldwide (Vannier et al. 2007), and the EBS species Tuzoia australis (Fig. 3i) and a large unnamed form (Tuzoia sp.) are typical in this respect. Only a few EBS specimens preserve the large stalked eyes projecting outside the carapace margin.
Radiodontans
Anomalocaris is represented by two species in the EBS, distinguished by characters of the spiny armature of their frontal appendages (McHenry & Yates 1993; Nedin 1995; Daley et al. 2013). Anomalocaris briggsi is the more abundant, with the less common frontal appendage assigned to Anomalocaris cf. canadensis. A few Anomalocaris oral cones are known from the EBS, one of them being associated with the frontal appendages of A. cf. canadensis (Fig. 3j and k). Other body parts of Anomalocaris, including segmental flaps and setal blades that in the Burgess Shale and at Chengjiang are known to attach to the body flaps, cannot as yet be definitively assigned to one of the two species. The EBS material is interesting for revealing more abundant disarticulated body parts (especially flaps) than at other sites with radiodontans and for the pyritization of these recalcitrant tissues exposing some details not known from elsewhere. Notable examples of this are a series of bars within the strengthening rays on the body flaps, and the lenses of the compound eye (see Box 2; Fig. 4c and d). Coprolites in the EBS that contain skeletal hash of trilobites (including Redlichia and Estaingia), in addition to injuries in Redlichia (Conway Morris & Jenkins 1985), were attributed to predation by Anomalocaris (Nedin 1999), but durophagy is unlikely for A. briggsi at least; the slender spines on its frontal appendages most probably functioned as a feeding net (Daley et al. 2013).
Box 2. Acute vision in the early Cambrian
The early fossil record of arthropod vision is dominated by trilobites, in which the lens arrangements of holochroal compound eyes have long been investigated, largely because the visual surface is (like the exoskeleton itself) mineralized with calcium carbonate. In contrast, the eyes of non-biomineralized arthropods in Cambrian Burgess Shale-type deposits are mostly known from their outlines only, the visual surface typically being preserved as carbon films that do not reveal details of the ommatidial lenses. Two EBS arthropods differ from this picture because the visual surfaces of their compound eyes were replicated by authigenic mineralization in early diagenesis (the cuticle being replicated by either pyrite or calcium phosphate), thus recording the arrangements of lenses in higher fidelity than in typical Burgess Shale-type preservation. One of these eyes is known from several specimens of an arthropod of uncertain affinities (the eyes are all isolated, detached from the head and other body parts) (Lee et al. 2011). The eyes are mostly 7–9 mm across their long axis. The visual surface displays more than 3000 lenses arranged with the dense hexagonal packing of living arthropod eyes. This tally vastly exceeds the lens numbers of known Cambrian trilobites. Just as noteworthy as their number is a gradient in the diameter of lenses from the edges of the eye to the centre: these eyes have a specialized zone of enlarged central lenses. In living arthropods this region is called a ‘bright zone’, a zone of increased visual acuity, and is found in predatory forms such as robberflies. Together with calculations for the ‘eye parameter’ (which relates the size and arrangement of ommatidia to light levels), the EBS eyes suggest a predator capable of acute vision in dim light.
Other large (2–3 cm) isolated compound eyes in the EBS can be assigned to Anomalocaris based on their similarity to the stalked eyes known in articulated material of that genus in the Burgess Shale and at Chengjiang (Paterson et al. 2011). The EBS Anomalocaris eyes are remarkable for the number of lenses in the visual surface, exceeding 16000 on the exposed surface (and presumably a large number more on the unexposed surface). This is near the upper limit for arthropods throughout their geological history (including extant species). The size of the visual field and number and arrangement of lenses are all consistent with acute vision in Anomalocaris, as would be expected given other morphological indications for predatory habits in highly motile animals.
(a, b) Compound eyes of an unknown arthropod showing large central ommatidial lenses forming a light-sensitive bright zone or fovea (f), and a sclerotized pedestal (p); (a) SAM P43629a; (b) SAM P43687. (c, d) Compound eye of Anomalocaris; (c) part (SAM P45920a), showing visual surface (vs) and eye stalk (es), with the boundary indicated by white arrows; us, undetermined structure; (d) counterpart (SAM P45920b) showing details of ommatidial lenses.
Lobopodians
A single specimen of an armoured lobopodian has been discovered in the EBS (García-Bellido et al. 2013a). It is incomplete, but preserves five pairs of long, slender, annulated lobopods that bear setiform spines along the margins, followed by two pairs of shorter lobopods that terminate in a robust claw (Fig. 5a and b). By comparison with luolishaniid lobopodians, the slender appendages are the anterior batch. The trunk of the EBS lobopodian bears three long, robust spines arranged across the dorsal side of each body segment. These characters are shared with the Chinese early Cambrian luolishaniids Luolishania (Chengjiang biota) and Collinsium (Xiaoshiba biota); the latter strengthens the hypothesis that these armoured lobopodians are stem-group onychophorans (Yang et al. 2015).
(a, b) Luolishaniid lobopodian; (a) part (SAM P14848a); (b) counterpart showing detail of claw (SAM P14848b). (c) Myoscolex ateles (SAM P47027a). (d) Wronascolex antiquus (SAM P45224a). (e) Polychaete annelid (SAM P46333a). Scale bars: (a, c, e) 5 mm; (b) 500 µm; (d) 20 mm.
Myoscolex
Myoscolex ateles (Fig. 5c) represents a genus known only from the EBS. It was originally interpreted as an annelid (Glaessner 1979) based on its segmented body. New material, which included the first example of phosphatized muscle tissue then known from the Cambrian, prompted a reinterpretation as a relative of the Burgess Shale stem-group arthropod Opabinia (Briggs & Nedin 1997). This drew on structures identified as a proboscis, three possible eyes, and flaps associated with the body segments. However, a subsequent study reasserted an annelid identity (Dzik 2004), emphasizing rod-shaped phosphatized structures on the lateral and ventral parts of each body segment that were interpreted as chaetae. New specimens under study are suggestive of a position on the stem of Euarthropoda.
Palaeoscolecids (Cycloneuralia)
Palaeoscolecids are a group of worms with a robust, annulated cuticle that bears rows of ornamented sclerites. They are known from many Cambrian Konservat-Lagerstätten, either as whole-body compression fossils or as secondarily phosphatized (Orsten-type) microfossils. The structure of the protrusible proboscis is critical to recognizing affinities to Cycloneuralia, the extant clade or grade of moulting worms that includes priapulids, nematodes and nematomorphs (Wills et al. 2012). A large palaeoscolecid in the EBS was originally named Palaeoscolex antiquus by Glaessner (1979), but the combined information from soft anatomy and ornament of the sclerites prompted reclassification as Wronascolex, a genus originally described from Siberia (García-Bellido et al. 2013b). Specimens of W. antiquus (Fig. 5d) preserve the scalids (teeth) on the proboscis, the gut and the hooks at the posterior end of the body; the largest specimen reaches a length of 37 cm. A second, rare species in the EBS, Wronascolex iacoborum, is distinguished by differences in the body annulation and the density of sclerites on the annulations.
Spiralians (‘lophotrochozoans’)
Representatives of this group are rare in the EBS. Members include: linguliformean brachiopods, such as eoobolids and botsfordiids (Fig. 6a), the latter exemplified by a species attributed to Diandongia from Chengjiang (Zhang et al. 2003, 2008); a polychaete annelid with possible affinities to Burgessochaeta (Fig. 5e; Eibye-Jacobsen 2004); and hyolith molluscs (Fig. 6b).
(a) Botsfordiid brachiopod (SAM P44242a). (b) Ribbed hyolith mollusc (SAM P14805a). (c) Vetustovermis planus (SAM P46982b). (d) Chancelloriid (SAM P51310a). (e) Leptomitid sponge (SAM P45545a). (f) Hamptoniid sponge (SAM P45915). (g) Rotadiscid (SAM P45196). (h) ‘Petalloid’ (SAM P45583). Scale bars: (a) 3 mm; (b, f–h) 5 mm; (c–e) 10 mm.
Vetustovermis planus (Fig. 6c) was described from a single EBS specimen, an elongate oval body 75 mm long, originally interpreted as an annelid (Glaessner 1979). Better preserved specimens from Chengjiang, assigned to the same species, revealed a head with eyes and a pair of tentacles, and showed that the supposed body segments are transverse bars reinterpreted as gills (Chen et al. 2005). Recent discussion has focused on the likely synonymy between Vetustovermis and the Burgess Shale Nectocaris, and the debate over the possible relationship of nectocaridids to Mollusca (see Smith 2013, and references therein).
Sponges
The Porifera so far found in the EBS are all demosponges. The assemblage is dominated by leptomitids (Fig. 6e), some more than 15 cm long, accompanied by a few specimens of hamptoniids (Fig. 6f) and choiids. These families are present in many other Cambrian Lagerstätten (Carrera & Botting 2008; Wu et al. 2014), and thus do not provide significant palaeobiogeographical information at a high taxonomic level.
Problematica
Some controversial animals documented from other Cambrian Konservat-Lagerstätten also occur in the EBS, but are typically very rare, known only from a few specimens. These include chancelloriids, represented by a species possibly belonging to Chancelloria (Bengtson & Collins 2015; Fig. 6d), and rotadiscids, with a close affinity to Pararotadiscus (Zhu et al. 2002; Fig. 6g); Bengtson & Collins (2015) and Caron et al. (2010) have discussed affinities of chancelloriids and rotadiscids, respectively. However, the EBS has revealed an unusual taxon (informally referred to as ‘petalloid’; Fig. 6h) that is relatively common and unlike anything found in other Burgess Shale-type biotas. Its bract-like elements are superficially similar to those of Dinomischus (Conway Morris 1977; Chen 2004), but the EBS taxon lacks a calyx and stem.
Palaeoecology
The animal community entombed within the EBS Konservat-Lagerstätte appears to have an ecological structure similar to that of typical Burgess Shale-type biotas (e.g. Caron & Jackson 2008; Peel & Ineson 2011; Zhao et al. 2014), represented by an autochthonous (in situ) assemblage of benthic inhabitants, plus transported individuals of other benthic, nektic and pelagic species (discussed further below). The benthos is dominated by the trilobite Estaingia bilobata, occurring in numbers of up to 300 individuals per square metre (see density in Fig. 3j), including in situ moult ensembles. The other relatively abundant benthic taxa include (to a much lesser extent) the trilobite Redlichia takooensis, the palaeoscolecid Wronascolex antiquus and sponges, with the remainder being very rare (e.g. several artiopodan arthropods, lobopodians, polychaetes, brachiopods, hyoliths and chancelloriids; see Box 3). The other prevalent faunal elements of the EBS are represented by taxa that had probable pelagic, nektic or nektobenthic life modes, suggestive of a well-oxygenated water column. Some of the more common forms include a variety of arthropods, especially ‘bivalved’ taxa such as Isoxys and Tuzoia (García-Bellido et al. 2009; see also Vannier et al. 2007, 2009), Anomalocaris (Paterson et al. 2011; Daley et al. 2013), and, to a lesser extent, cheliceriform and ‘great appendage’ arthropods (Edgecombe et al. 2011; Paterson et al. 2015), and animals such as Myoscolex and the vetulicolian Nesonektris (Briggs & Nedin 1997; García-Bellido et al. 2014).
Box 3. Outstanding questions
Certain taxonomic groups that are usually represented in Cambrian Burgess Shale-type biotas are either very scarce in the EBS (e.g. annelids, lobopodians) or wholly lacking (e.g. echinoderms). Teasing out whether these rare occurrences or absences are biogeographically, environmentally, ecologically and/or taphonomically controlled (e.g. annelids are unknown from Chengjiang and are represented in the Guanshan biota by a single specimen, but are well represented in the Burgess Shale and Sirius Passet biotas; Parry et al. 2014; Liu et al. 2015) remains an important challenge. One of the biggest questions surrounding the EBS Konservat-Lagerstätte is how the unusual combination of a nearshore palaeoenvironmental setting and the variety of preservational modes seen in EBS fossils, such as the 3D relief of soft-bodied taxa and the range of early diagenetic mineralization of labile and recalcitrant tissues, relates to typical Burgess Shale-type deposits, if at all (Gaines 2014). This will require detailed microstratigraphic, sedimentological and geochemical analyses, including drill core samples.
The very limited diversity of autochthonous (in situ) benthic inhabitants and lack of bioturbation in the EBS, coupled with the dominance of Estaingia bilobata, may be clues in deciphering the conditions on the seafloor. A similar ecological abundance of a single trilobite species has been well documented from the Cambrian Wheeler Formation of Utah (Gaines & Droser 2003, 2005, 2010). Here, Elrathia kingii occurs in densities of up to 500 individuals per square metre and is interpreted as being an inhabitant of the exaerobic zone, a transitional area of the seafloor between dysoxic and truly anoxic bottom waters. Estaingia from the EBS may have occupied the same ecological niche. Low-oxygen conditions in the bottom waters may also explain the paucity of many other motile benthic organisms, and the extreme rarity or total absence of most fixosessile taxa (e.g. brachiopods and echinoderms, respectively); although the latter could also be due to the overall high, often turbid sedimentation rates evident in the EBS. The rarer motile benthic taxa most probably represent individuals that were either transported from their living environment (e.g. the trilobite Balcoracania dailyi, which typically inhabits shallow water, marginal marine settings; Paterson et al. 2007) or vagrants that lived near the boundary of the exaerobic zone and were more tolerant of the harsh low-oxygen conditions. The more common palaeoscolecids (particularly W. antiquus) and leptomitids may have also been dysaerobic specialists, as their modern phylogenetic and ecological analogues (e.g. priapulids and demosponges, respectively) are known to live under similar oxygen conditions (Oeschger et al. 1992; Levin 2003; Mills et al. 2014; and references therein). However, the ubiquitous occurrence of Cambrian palaeoscolecids (especially Wronascolex; García-Bellido et al. 2013b) and demosponges (Carrera & Botting 2008) in various palaeoenvironmental settings worldwide, in addition to the supposed burrowing habit of palaeoscolecids (Huang et al. 2014), suggests that perhaps the EBS forms occupied the periphery of the exaerobic zone where the sediment–water interface was more oxygenated and were subsequently transported a short distance into an optimal preservational setting (Gaines 2014).
Preservation of Emu Bay Shale fossils
Most studies on the taphonomy of EBS fossils have focused on the diagenetic aspects, specifically the early diagenetic mineralization of soft tissues, which is particularly prominent and varied compared with other documented Cambrian Konservat-Lagerstätten (Gaines 2014), but also late-stage diagenetic mineralization in the form of pink to white fibrous calcite that can replicate fossils (Nedin 1997). Examples of the former process include phosphatization of labile tissues such as muscle (Briggs & Nedin 1997; Nedin 1997) and gut structures (García-Bellido et al. 2009, 2013b; Edgecombe et al. 2011; Paterson et al. 2012), but also recalcitrant extracellular cuticle (Lee et al. 2011; Paterson et al. 2011); the last can also be pyritized (see Box 2).
Although there is still much work to be done in understanding these modes of preservation during diagenesis, various biostratinomic characteristics also require further investigation (Box 3). The most conspicuous of these is the prevalence of complete specimens of the trilobite Estaingia preserved dorsum-down throughout the Konservat-Lagerstätte interval; as confirmed by stratigraphic ‘way-up’ evidence in the sections; for example, load structures (see Gehling et al. 2011). Preliminary data indicate that on average, c. 75% of individuals within the mudstone horizons are preserved in this orientation. Specimens of Redlichia takooensis are also typically oriented in this manner. A likely explanation for this phenomenon (see Paterson et al. 2007) is that inversion resulted from decay gases building up beneath carcasses, causing them to become buoyant and eventually overturn (Babcock & Chang 1997). This scenario is supported by the exaerobic zone hypothesis (discussed above), whereby inhabitants could have asphyxiated en masse during an intermittent landward shift of the oxycline, leaving them to decay on the substrate in the absence of benthic scavengers or bioturbators; as mentioned above, there is no clear evidence of bioturbation in the EBS Konservat-Lagerstätte interval. Mass asphyxiation events owing to a fluctuating oxycline, which would have also affected parts of the water column, may also explain the abundance of free-swimming taxa within the EBS mudstones, especially Isoxys communis, the most common soft-bodied species in the EBS. Such forms are frequently preserved in either dorso-ventral or lateral aspect (with the largest and flattest surface area oriented parallel to bedding), suggestive of gravitational settling (see Zhang & Hou 2007), as opposed to turbid burial, which can result in oblique orientations (Caron & Jackson 2006; Gabbott et al. 2008; Gaines 2014). In the case of the free-swimming arthropods, the abundance and orientation of their remains may also be a consequence of moulting, as indicated by the common occurrence of ‘bivalved’ carapaces without trunks, and isolated elements (especially frontal appendages and body flaps) of Anomalocaris.
The EBS mudstones containing trilobites, especially those horizons comprising unequivocal in situ moult ensembles of Estaingia and Redlichia, and other free-swimming forms that are commonly preserved in prone, supine or lateral positions seem to indicate short periods of quiescent substrate conditions (affected by a fluctuating oxycline) prior to frequent burial events. The often poor fidelity or partial or total absence of certain anatomical structures (e.g. the appendages of some artiopodans; Paterson et al. 2010, 2012) may also relate to decay rate versus pre-burial residence time on the seafloor (Zhao et al. 2009; O’Brien et al. 2014), but the relationships between preservational fidelity, original histology and host sediment types (including mineralogy) should also be considered (Gaines et al. 2012b; Wilson & Butterfield 2014). However, several interbedded siltstone and fine sandstone layers often entomb complete trilobites and vetulicolians in chaotic orientations, again contrasting with the dorso-ventral or lateral orientations of these animals in mudstones, respectively; for example, the preservation styles of EBS vetulicolians in siltstones (García-Bellido et al. 2014, fig. 1A–F) compared with those in mudstones (García-Bellido et al. 2014, fig. 4C). This suggests that intermittent sediment gravity flows not only swept up members of the benthos, but captured free-swimming taxa as well, with only the biomineralized or heavily sclerotized forms preserving in these coarser sediments.
Understanding the preservational modes of soft-bodied fossils in the EBS is hindered by the extensive surficial weathering, as is the case in deposits such as those of Chengjiang (Gabbott et al. 2004; Forchielli et al. 2014). This was one of the reasons why Gaines (2014) excluded the EBS as a Burgess Shale-type deposit, which is defined by the occurrence of soft-bodied fossils preserved as 2D, primary carbonaceous remains. This strict definition of ‘carbonaceous compression’ fossils means that the EBS fails on both counts, as (1) the fossils show no signs of carbon films and (2) recalcitrant tissues in many soft-bodied taxa (such as Isoxys, Tuzoia, non-trilobite artiopodans and even Anomalocaris frontal appendages) have some degree of three-dimensionality (e.g. Fig. 3b, f and i). Whereas the absence of carbonaceous remains may simply be the result of weathering, the 3D nature of soft-bodied fossils within the EBS mudstones, excluding specific anatomical structures replicated by authigenic minerals (e.g. mid-gut glands), implies a different preservational mode from that of Burgess Shale-type deposits. This may be due, in part, to the presence of a silt fraction within the EBS mudstones that is otherwise lacking in Burgess Shale-type clay-rich beds containing 2D carbonaceous compression fossils (Gaines et al. 2012b).
Summary
The Emu Bay Shale Konservat-Lagerstätte provides critical information on the evolution, biogeography and ecology of Cambrian faunas from an East Gondwanan perspective. Overall, the EBS community appears to have been living in and under a well-oxygenated water column (within the photic zone) that was often subjected to a fluctuating oxycline. This resulted in the development of an exaerobic zone on the seafloor (below storm wave base) that was inhabited by dysaerobic specialists, but also acted as a preservational trap for many other benthic, nektobenthic and pelagic taxa that were transported into or settled down in this setting. Although the EBS contains a typical Burgess Shale-type biota, a unique combination of preservational modes in a nearshore setting sets it apart from other Burgess Shale-type deposits. It thus holds potential for reshaping our understanding of the exceptional preservation of Cambrian soft-bodied fossils.
Acknowledgements and Funding
Emu Bay Shale research has been supported by grants from the Australian Research Council (LP0774959, DP120104251,+ FT120100770, FT130101329), Spanish Research Council (CGL2009-07073, CGL2013-48877-P) and National Geographic Society Research & Exploration (#8991-11), with additional financial assistance from Beach Energy Ltd and the South Australian Museum. SeaLink has provided logistical support. We are grateful to the Buck family for access to the field area. We thank our friends and colleagues (in alphabetical order) R. Atkinson, M. Binnie, G. Brock, A. Camens, A. Daley, R. Gaines, M. Gemmell, J. Holmes, K. Kenny, P. Kruse, J. Laurie, X. Ma, B. McHenry, M. Mills, L. Reid, D. Rice, N. Schroeder, E. Thomson and members of the South Australian Museum Waterhouse Club for assistance in the field and laboratory, as well as providing fruitful discussions over the years. Thanks go to three anonymous referees for providing helpful reviews of the paper, and to R. Gaines for commenting on an earlier draft.
- © 2016 The Author(s)
References
The Emu Bay Shale Konservat-Lagerstätte: a view of Cambrian life from East Gondwana
