2. Geological and palaeoenvironmental context

The Emu Bay Shale forms part of the Kangaroo Island Group in the Stansbury Basin, which crops out on the north coast of Kangaroo Island (South Australia), and is interpreted as a nearshore delta complex (Gehling et al. Reference Gehling, Jago, Paterson, García-Bellido and Edgecombe2011; Jago et al. Reference Jago, Bentley, Paterson, Holmes, Lin and Sun2021). The Emu Bay Shale is considered to be c. 512 Ma (Pararaia janeae Zone; Cambrian Series 2, Stage 4) in age (Bengtson et al. Reference Bengtson, Conway Morris, Cooper, Jell and Runnegar1990; Paterson & Jago, Reference Paterson and Jago2006; Paterson & Brock, Reference Paterson and Brock2007; Jago et al. Reference Jago, Gehling, Betts, Brock, Dalgarno, García-Bellido, Haslett, Jacquet, Kruse and Langsford2020), based primarily on the co-occurrence of the emuellid trilobite Balcoracania dailyi Pocock, Reference Pocock1970 and an associated radiometric date of 511.87 ± 0.14 Ma in the Billy Creek Formation of the Arrowie Basin (Paterson & Edgecombe, Reference Paterson and Edgecombe2006; Paterson et al. Reference Paterson, Jago, Brock and Gehling2007; Betts et al. Reference Betts, Paterson, Jacquet, Andrew, Hall, Jago, Jagodzinski, Preiss, Crowley, Brougham, Mathewson, García-Bellido, Topper, Skovsted and Brock2018).

In the Big Gully area of Kangaroo Island, the Emu Bay Shale is 78 m thick at the shoreline and c. 61 m thick near Buck and Daily quarries, where the material considered here was sourced (c. 400 m inland; see García-Bellido et al. Reference García-Bellido, Paterson, Edgecombe, Jago, Gehling and Lee2009 for a detailed locality map). Here, the formation commences with a thin (up to 2 m) interval of polymict conglomerate, the base of which is interpreted as a sequence boundary separating it from the underlying Marsden Sandstone. Above this, the conglomerate transitions sharply into a package of dark grey, laminated mudstone with siltstone and fine sandstone event beds that become thicker and more common towards the contact with the sandstones of the overlying Boxing Bay Formation (Gehling et al. Reference Gehling, Jago, Paterson, García-Bellido and Edgecombe2011). The mudstone interval of the lower Emu Bay Shale is interpreted as representing a relatively deep-water prodelta environment, and hosts the Konservat-Lagerstätte that contains a diverse biota (50+ species, mainly within the basal c. 15 m of the formation), with many taxa considered to have been transported from shallower settings upslope, or having settled out of the water column (Paterson et al. Reference Paterson, García-Bellido, Jago, Gehling, Lee and Edgecombe2016). Exceptions include certain trilobite species, particularly the extraordinarily abundant Estaingia bilobata (with up to 600 individuals per square metre; JRP, unpublished data), as well as the redlichioids Redlichia takooensis Lu, Reference Lu1950 and R. rex Holmes, Paterson & García-Bellido, 2019 (Holmes et al. Reference Holmes, Paterson and García-Bellido2020). Intact moult configurations of these species suggest that they lived in or close to the low-oxygen environment of the prodelta setting, although were likely subject to occasional ‘mass kill’ events resulting from fluctuations of the oxycline (Paterson et al. Reference Paterson, García-Bellido, Jago, Gehling, Lee and Edgecombe2016). The prevalence of dorsum-down trilobite specimens in the deposit (up to 90% for E. bilobata; Drage et al. Reference Drage, Holmes, García-Bellido and Daley2018) may indicate a physiological response to oxygen stress.

3. Methods

All Estaingia bilobata specimens housed in the South Australian Museum (Adelaide, South Australia) palaeontological collection (SAMA P) were examined for evidence of malformations. Identified specimens were photographed under normal (fibre optic) lighting conditions using a Canon EOS 5D digital camera with a Canon MP-E 65 mm 1–5× macro lens.

The linear measurement dataset published by Holmes et al. (Reference Holmes, Paterson and García-Bellido2021 a) was used to determine where malformed Estaingia bilobata specimens were located in bivariate space compared to non-malformed specimens. The cephalic and trunk (thorax + pygidium) lengths in the dataset were used (Fig. 6a). Where possible, measurements from malformed specimens were added (Supplemental Information 1). Not all specimens documented here could be included due to partial preservation. Data were natural-log (ln) normalized and plotted. Data points were coded for malformation presence or absence.

Fig. 6. Measurements of Estaingia bilobata and bivariate plot showing distributions of malformations. (a) Reconstruction of E. bilobata showing measurements used in (b). (b) Bivariate space of E. bilobata. Most malformed specimens cluster with the largest specimens. Data found in Supplemental Data 1. Data were natural log normalized for plotting. Abbreviations: cl: cephalic length; tr: trunk (thorax + pygidium) length.

4. Terminology

5. Results

Examination of Estaingia bilobata specimens uncovered several examples of injuries, pathologies, and teratologies. We also found evidence for possible durophagous predation or post-mortem scavenging in the form of mangled exoskeletons.

5.a. Injuries

Six injured Estaingia bilobata are identified. Most injuries are unilateral, show L-, U-, W-shaped morphologies (Figs. 1, 2; Table 1) and are located on the trunk, showing evidence for pleural spine regeneration and rounding (Fig. 1c, d) and cicatrization (Figs 1e, f, 2a, b). However, there is a single specimen with a highly deformed posterior trunk showing fused thoracic segments (Fig. 2e, f). There is only one specimen that displays a cephalic injury, represented by a broken genal spine that has partially regenerated (Fig. 2c, d).

Table 1. Summary of injured Estaingia bilobata

6. Discussion

The specimens of Estaingia bilobata documented here show evidence for the three major groups of trilobite malformations (Owen, Reference Owen1985). This is rare among Cambrian trilobites, as the vast majority of malformed specimens record injuries, with limited evidence for teratologies and pathologies (Bergström & Levi-Setti, Reference Bergström and Levi-Setti1978; Bicknell & Paterson, Reference Bicknell and Paterson2018; De Baets et al. Reference De Baets, Budil, Fatka, Geyer, De Baets and Huntley2022). As such, E. bilobata presents a unique opportunity to study the palaeobiological significance of malformation types in one trilobite species from a single deposit.

The majority of observed Estaingia bilobata injuries (Figs. 1, 2a, b, e, f) are comparable to other documented examples of injured Cambrian trilobites (Rudkin, Reference Rudkin1979; Babcock, Reference Babcock1993; Bicknell & Pates, Reference Bicknell and Pates2020; Zong, Reference Zong2021 a, b). Indeed, select E. bilobata injuries are very similar to those observed on the co-occurring Redlichia takooensis and R. rex that have been attributed to failed predation (Conway Morris & Jenkins, Reference Conway Morris and Jenkins1985; Bicknell et al. Reference Bicknell, Holmes, Pates, García-Bellido and Paterson2022 a). It is highly likely that these injuries in E. bilobata also reflect failed predation. Evidence for cicatrization (Figs 1a, b, e, f, 2a, b) and regeneration (Fig. 1c, d) at injury sites indicates that these individuals survived and continued to moult after attacks. Other evidence for predation on, or post-mortem mastication of, E. bilobata is represented by the mangled exoskeletons (Fig. 5). Similar examples of R. takooensis have been interpreted as rare evidence of possible durophagy (e.g. Bicknell et al. Reference Bicknell, Holmes, Pates, García-Bellido and Paterson2022 a, fig. 1C–E). Such evidence of durophagy, combined with examples of failed predation, further bolsters the idea that E. bilobata was a key prey item within the Emu Bay Shale biota. This smaller trilobite species likely occupied a relatively low trophic level within the ecosystem (Jago et al. Reference Jago, García-Bellido and Gehling2016), especially given its extreme abundance (>80% of individuals across all known species), and yet injured specimens of E. bilobata are exceedingly rare. Further, most injured specimens cluster among the larger individuals in bivariate space. This may suggest that only larger individuals were capable of escaping and recovering from attacks, preserving records of failed predation. Alternatively, these specimens may preserve evidence of older injuries that recovered through subsequent moulting events. In either case, this pattern indicates a possible record of survivorship bias within the trilobite fossil record.

One injured specimen of Estaingia bilobata shows a substantially disrupted posterior thorax (Fig. 2e, f). This malformation is comparable to rare specimens of other Cambrian trilobite species with highly disrupted and wrinkled pleurae adjacent to the injury (Conway Morris & Jenkins, Reference Conway Morris and Jenkins1985; Bicknell et al. Reference Bicknell, Holmes, Pates, García-Bellido and Paterson2022 a). This condition is more commonly observed in the trunk of younger iso- and macropygous trilobites (Ormiston et al. Reference Ormiston, Logan and Fulton1967; Šnajdr, Reference Šnajdr1981; Owen, Reference Owen1985; Rudkin, Reference Rudkin1985). Disruption of pleurae indicates that the individual may have been attacked during the soft-shelled stage (shortly after moulting), resulting in a highly deformed exoskeleton that became fixed in subsequent moults (Conway Morris & Jenkins, Reference Conway Morris and Jenkins1985; Rudkin, Reference Rudkin1985).

Trilobite genal spine malformations are particularly rare (Owen, Reference Owen1985). Most malformed genal spines are represented by disrupted borders (e.g. Chatterton, Reference Chatterton1971; Cowie & McNamara, Reference Cowie and McNamara1978; Owen, Reference Owen1985; Babcock, Reference Babcock1993; Bicknell et al. Reference Bicknell, Pates and Botton2018 c), abnormal cephalic fringes (Owen, Reference Owen1983), or bifurcating genal spines (Owen, Reference Owen1985). Complete removal (Kay, Reference Kay1937) and recovery (Sinclair, Reference Sinclair1947; Hessin, Reference Hessin1988; Bicknell et al. Reference Bicknell, Smith, Bruthansová and Holland2022 c) of genal spines is exceedingly rare, as reflected by the single Estaingia bilobata specimen documented here. The documentation of only one genal spine injury (Fig. 2c, d) is noteworthy. Given the constrained anatomical region, a predator would unlikely have limited an attack to the genal area. As such, we can exclude failed predation as the most plausible explanation. Instead, the injury could reflect a complication during moulting or mechanical (non-predatory) damage that resulted in spine breakage (Owen, Reference Owen1983).

Teratological trilobite specimens with an additional ‘half-segment’ are almost completely unknown. To our knowledge, the only other example of an additional ‘half-segment’ within the thoracic region is a malformed Emuella polymera Pocock, Reference Pocock1970 that has multiple ‘half-segments’ (Pocock, Reference Pocock1974; Owen, Reference Owen1985; Paterson & Edgecombe, Reference Paterson and Edgecombe2006). One further record of this ‘half-segment’ condition is known from a Toxochasmops McNamara, Reference McNamara1979 pygidium from the Upper Ordovician (Katian) of Norway (Nielsen & Nielsen, Reference Nielsen and Nielsen2017). These rare teratologies likely record damage to a generative zone and the resultant propagation of additional, unaligned segments (Pocock, Reference Pocock1974; Owen, Reference Owen1985). It is noteworthy that two of the three examples represent early Cambrian forms, one of which (E. polymera) belongs to the family Emuellidae, which is characterized by unusually large numbers of trunk segments (Paterson & Edgecombe, Reference Paterson and Edgecombe2006). Emuellids in particular may have been more prone to teratologies as they added new segments through euanamorphosis (Paterson & Edgecombe, Reference Paterson and Edgecombe2006). These trilobites certainly had unusual patterns of trunk segment development compared with other forms (Holmes et al. Reference Holmes, Paterson and García-Bellido2021 a). This may have increased the likelihood of developmental malformations, indicating possible evidence for increased developmental plasticity within Cambrian trilobites compared to younger forms (Webster, Reference Webster2007). However, the rarity of these exceptional specimens suggests that these malfunctions seldom occurred.

Fused exoskeletal sections are rarely observed in thoracic pleurae (see Öpik, Reference Öpik1975, pl. 17), but more commonly recognized in pygidial regions (Strusz, Reference Strusz1980; Owen, Reference Owen1985; Babcock, Reference Babcock1993; Nielsen & Nielsen, Reference Nielsen and Nielsen2017; Bicknell & Smith, Reference Bicknell and Smith2021). Such teratologies have been attributed to genetic malfunctions (Nielsen & Nielsen, Reference Nielsen and Nielsen2017) and/or moulting complications producing a malformation that propagated in subsequent moults (Bicknell & Smith, Reference Bicknell and Smith2021). As the teratological thoracic segments (Fig. 4c, d) lack any evidence of an injury, this rare malformation was likely caused by a developmental abnormality that impacted a limited exoskeletal region. This may record segments failing to separate or articulate correctly when they budded off from the pygidium.

The morphologies of exceptionally preserved appendages in two Emu Bay Shale arthropod species have been linked to durophagy, potentially on Estaingia bilobata. Firstly, the short, stout gnathobasic spines on the biramous appendages of the very large trilobite Redlichia rex (Fig. 7e, f) have been shown to be comparable with other known durophages, such as the Cambrian Burgess Shale arthropod Sidneyia inexpectans Walcott, Reference Walcott1911 and the extant horseshoe crab Limulus polyphemus (Linnaeus, Reference Linnaeus1758) (Botton, Reference Botton1984; Bicknell et al. Reference Bicknell, Ledogar, Wroe, Gutzler, Watson and Paterson2018 a, b, Reference Bicknell, Holmes, Edgecombe, Losso, Ortega-Hernández, Wroe and Paterson2021, Reference Bicknell, Holmes, Pates, García-Bellido and Paterson2022 a; Holmes et al. Reference Holmes, Paterson and García-Bellido2020). This has permitted the linking of injuries identified on R. takooensis specimens with failed predation by the larger R. rex, and injuries to R. rex as possible instances of attempted cannibalism (Bicknell et al. Reference Bicknell, Holmes, Pates, García-Bellido and Paterson2022 a). Individuals of R. rex (and potentially R. takooensis, although morphological details of the appendages are unknown) may have also consumed E. bilobata, as supported by centimetre-scale coprolites containing E. bilobata remains (Daley et al. Reference Daley, Paterson, Edgecombe, García-Bellido and Jago2013, fig. 7E–H) that have been attributed to R. rex (Daley et al. Reference Daley, Paterson, Edgecombe, García-Bellido and Jago2013; Bicknell et al. Reference Bicknell, Holmes, Pates, García-Bellido and Paterson2022 a). The gnathobasic spines of the Emu Bay Shale chelicerate Wisangocaris barbarahardyae Jago et al., Reference Jago, García-Bellido and Gehling2016 (Fig. 7c, d) show similar morphologies to those of R. rex and other known durophages, and were likely also adapted for crushing biomineralized material (Jago et al. Reference Jago, García-Bellido and Gehling2016). This is supported by the presence of shelly cololites in certain specimens of W. barbarahardyae, some containing fragments of E. bilobata (Fig. 7a, b; Jago et al. Reference Jago, García-Bellido and Gehling2016, fig. 5c–g). Given the maximum reported size of W. barbarahardyae is c. 60 mm, this arthropod may have targeted and consumed E. bilobata meraspides. Juveniles of E. bilobata are abundant in the Lagerstätte interval and range from c. 1 to 5 mm in length (Holmes et al. Reference Holmes, Paterson and García-Bellido2021 a, b). This is consistent with the size of E. bilobata pleurae preserved within a W. barbarahardyae cololite (Fig. 7b). The size range and sheer abundance of E. bilobata within the Emu Bay Shale suggest that this small trilobite occupied an important position within the lower trophic levels of the local ecosystem, and was an important prey item for multiple species of predator.

Fig. 7. Examples of possible predators of Estaingia bilobata. (a–d) Wisangocaris barbarahardyae. (a, b) SAMA P55603a. Specimen showing shelly cololite containing E. bilobata fragments. (a) Near-complete specimen. (b) Close-up of cololite with sclerite fragments (white arrows). (c, d) SAMA P45629. Specimen showing series of gnathobases possibly used in durophagy of E. bilobata. (c) Near-complete specimen. (d) Close-up showing rows of gnathobasic spines. (e, f) SAMA P54942. Biramous appendage of Redlichia rex showing stout gnathobasic spines. (e) Complete specimen. (f) Close-up of stout gnathobasic spines.