Five new malformed trilobites from Cambrian and Ordovician deposits from the Natural History Museum

Geological context

The Ogygopsis klotzi (NHMUK PI I 4749) and Olenoides serratus (NHMUK PI IG 4437-9) figured in this study were collected from Mount Stephen in British Columbia, Canada, in Walcott’s (1908) “Ogygopsis Shale”, Burgess Shale Formation on the mountain trail 850 m above the town of Field. This is horizon is now placed within the Campsite Cliff Shale Member, a member that also outcrops at Mount Field and the Fossil Gully Fault (Fletcher & Collins, 1998; Fletcher & Collins, 2003). The association of articulated trilobite remains and with an underlying distal wedge facies suggests the unit was deposited in a deeper water, potentially euoxic setting (further from the carbonate platform forming the Cathedral Formation palaeocliff edge; Allison & Brett, 1995). Presence of the eponym for the Pagetia bootes Subzone places the member firmly within the restricted shelf Bathyuriscus–Elrathina Zone (Fletcher & Collins, 1998). This has been correlated with the upper portion of the open-shelf Ptychagnostus praecurrens Zone of North America (Robison & Babcock, 2011) and is correlated with the later portion of the Wuliuan Stage (Miaolingian) on the global scale (Peng, Babcock & Cooper, 2012).

The Paradoxides (Paradoxides) paradoxissimus gracilis (NHMUK PI OR 42440) figured here was collected from Jince in the Czech Republic at an unknown locality in the Jince Formation. The taxon is widely distributed over the entire Jince Basin, occurring at multiple outcrops throughout the Litavka River Valley region, hence the exact specimen location is impossible to determine (Fatka & Szabad, 2014). However, more generally P. (P.) paradoxissimus gracilis occurs in the green, fine-grained greywackes and shales within the middle levels of the Jince Formation, which is thought to correspond with the peak of a transgressive event identified in the unit (Storch, Fatka & Kraft, 1993; Fatka & Szabad, 2014). The occurrence of abundant articulated agnostids, paradoxidids, and a conocoryphid species (Fatka, Kordule & Szabad, 2004) suggests a deeper water environment, within the conocoryphid biofacies of Álvaro, González-Gómez & Vizcaïno (2003). The taxon is the eponym for the P. (P.) paradoxissimus gracilis Zone in the Příbram-Jince Basin within the Barrandian area (Fatka & Szabad, 2014 for a comprehensive discussion). Co-occurrence of the agnostid Hypagnostus parvifrons (Linnarsson, 1869) and the lower stratigraphic occurrence of Onymagnostus hybridus (Brøgger, 1878; Fatka, Kordule & Szabad, 2004; Fatka & Szabad, 2014) suggests the zone corresponds with the middle and higher levels of the Baltic P. (P.) paradoxissimus Zone (Axheimer & Ahlberg, 2003; Høyberget & Bruton, 2008; Weidner & Nielsen, 2014). This region likely corresponds to the Scandinavian, South Chinese, and Australian Ptychagnostus atavus and Ptychagnostus punctuosus zones, placing the formation in the early to mid-Drumian Stage (Miaolingian) globally (Peng, Babcock & Cooper, 2012).

The Ogygiocarella angustissima (NHMUK PI OR 59206) and Ogygiocarella debuchii (NHMUK PI In 23066) figured in this study were collected from two similarly aged deposits in Wales, United Kingdom. The Ogygiocarella angustissima specimen was apparently collected from Gwern-fydd, although this seems unlikely given the regional geology and lithology of the specimen. Lectotype material preserved in identical matrix has alternatively been suggested to be derived from “Harper’s quarry”, 500 m north-west of Welfield(near Builth), likely within the Llanfawr Mudstones Formation, Builth Inlier (Hughes, 1979 and references therein, also see updated stratigraphy in Davies et al., 1997; Fortey et al., 2000). The Ogygiocarella debuchii specimen conversely originates from Betton Quarry (near Shropshire) in the upper Meadowtown Formation, Shelve Inlier. Both units are dominated by fine mudstone and siltstone, likely being deposited on a relatively deep shelf environment nearby a volcanic arc (Fortey & Owens, 1987; Davies et al., 1997; Fortey et al., 2000; Owens, 2002). Known ranges of Ogygiocarella angustissima and Ogygiocarella debuchii suggest the taxa occur in either the Hustedograptus teretiusculus and/or Nemagraptus gracilis zones at these localities. However, without more precise details regarding the exact collection horizons (and associated graptolite or other shelly fauna) it impossible to determine which precisely (Hughes, 1979; Bettley, Fortey & Siveter, 2001). Hence, the figured material likely comes from somewhere within the regional Llandeilian(Llanvirn) or Aurelucian (Caradoc) stages. This correlates with the global Darriwilian (Middle Ordovician) to Sandbian (Late Ordovician) boundary (Bettley, Fortey & Siveter, 2001; Cooper & Sadler, 2012; Goldman et al., 2023).

On Ogygopsis klotzi

Records of injured Ogygopsis klotzi represent valuable insight into possible predator–prey dynamics within the Burgess Shale biota (Table 2). These injuries were originally thought to reflect predation by Anomalocaris canadensis (Whiteaves, 1892) (see discussion in Rudkin, 1979). However, recent three-dimensional (3D) kinematic, biomechanical, and computational fluid dynamic modelling have demonstrated that A. canadensis appendages were ineffective at handling biomineralised prey (De Vivo, Lautenschlager & Vinther, 2021; Bicknell et al., 2023b). More plausible predators are the co-occurring trilobites and other artiopodans that have reinforced gnathobasic spines on walking legs (Whittington, 1980; Bruton, 1981; Bicknell et al., 2018b; Holmes, Paterson & García-Bellido, 2020). Trilobite fragments within the gut contents of artiopodans (Zacaï, Vannier & Lerosey-Aubril, 2016; Bicknell & Paterson, 2018) and 3D biomechanical analyses of gnathobase-bearing appendages (Bicknell et al., 2018a; Bicknell et al., 2021) support this mode of durophagous predation. One other option is the mantis shrimp-like arthropod Yohoia Walcott, 1912 that may have damaged trilobite exoskeletons using its anteriorly directed raptorial appendages (Pratt, 1998; Haug et al., 2012).

The records collated in Table 2 represent the basis for developing a much larger dataset to explore Ogygopsis klotzi injury patterns. Documentation of injured specimens housed in other collections will expand this preliminary sample and permit the left–right behavioural asymmetry hypothesis to be re-addressed (Babcock & Robison, 1989; Babcock, 1993). Recent examination of injury patterns in Cambrian trilobites have demonstrated little evidence for injury asymmetry (Pates & Bicknell, 2019; Bicknell et al., 2022a; Bicknell et al., 2023a). However, with 80% of Ogygo. klotzi unilateral injuries being right sided, this injury distribution may indeed reflect a population-level pattern (Table 2). Illustrating this condition with a statistical dataset of one species (following Pates et al., 2017; Bicknell, Paterson & Hopkins, 2019; Bicknell et al., 2022a; Bicknell et al., 2023a; Pates & Bicknell, 2019) will uncover interesting injury patterns and represents a clear direction for exploring this topic further.

On Olenoides serratus

Predators of Olenoides serratus were similar to Ogygopsis klotzi as both species are from the Burgess Shale. It is worth considering how the Ol. serratus male mating claspers may have caused injuries (Losso & Ortega-Hernández, 2022). In modern female horseshoe crabs, males cause injuries to the medial region of during amplexus (Shuster Jr, 1982; Brockmann, 1990; Shuster Jr, 2009; Bicknell, Pates & Botton, 2018c; Das et al., 2021; Bicknell et al., 2022c). It is possible that male Ol. serratus may have caused similar medial injuries during mating. However, these reduced appendages did not produce the large, laterally located injuries documented here and in Table 3.

On Paradoxides (Paradoxides) paradoxissimus gracilis

The anterior indentations on the right pleural lobe of Paradoxides (Paradoxides) paradoxissimus gracilis (NHMUK PI OR 42440, Fig. 2B) reflect either two separate attacks that targeted the same exoskeletal region, or an additional moulting complication proximal to this injury. We suggest that both options are viable here as the posterior-most section of the injury (Fig. 2B, blue arrow) shows more recovery than anterior region. As trilobites recovered from injuries anterior to posterior (McNamara & Tuura, 2011; Zong & Bicknell, 2022), the more anterior region should show more evidence of recovery. This injured region has therefore experienced an additional traumatic event, although the exact cause is unknown. The posterior injury on the right pleural lobe (Fig. 2D) is morphologically comparable to injuries ascribed to predation (Babcock, 1993; Bicknell & Paterson, 2018) supporting the assignment of this injury to failed predation. The SSI observed on this specimen (Fig. 2D) reflects failed predation (Bicknell et al., 2022a) or a moulting complication. As P. (P.) paradoxissimus gracilis has long pleural spines, that may have been damaged while moulting, resulting in an isolated injury (Šnajdr, 1978; Conway Morris & Jenkins, 1985; Daley & Drage, 2016; Drage, 2019; Drage & Daley, 2016). This specimen highlights that more research into the moulting patterns of P. (P.) paradoxissimus gracilis may help differentiate these options.

Previously documented injured specimens of “P. gracilis” (Boeck, 1827) permit useful comparisons to understand the injuries observed here (Fig. 2; Šnajdr, 1978; Owen, 1985; De Baets et al., 2022). Injuries to Jince Formation Paradoxides are considered a result of moulting complications that arose from the flat morphology and elongate pleural spines common to Paradoxides (Šnajdr, 1978). However, as demonstrated here, failed predation cannot be fully discounted. The predators were likely co-occurring paradoxidids (Babcock, 1993; Fortey & Owens, 1999; Fatka, Szabad & Budil, 2009)—a proposal that further supports cannibalism within Cambrian trilobites (Conway Morris & Jenkins, 1985; Daley et al., 2013; Bicknell et al., 2022a). Additionally, the bivalved arthropod Tuzoia Walcott, 1912 may have targeted Paradoxides, as Tuzoia is considered a nektobenthic to pelagic predatory or scavenger (Fatka & Herynk, 2016; Izquierdo-López & Caron, 2022).

On Ogygiocarella

The abnormal recovery and fusion of ribs in Ogygiocarella debuchii (NHMUK PI In 23066; Fig. 4) in two pygidial regions indicates two different traumatic events. The injury on the left side shows no evidence of an indentation (Fig. 4C). This suggests that a moulting complication occurred, and the ribs recovered abnormally—a condition that was propagated through subsequent moulting events. Conversely, the ‘U’-shaped indentation and fused pygidial ribs on the right side (Fig. 4B) indicates a failed predation attempt that recovered abnormally.

Records of injured and malformed Ogygiocarella are limited(Table 4). However, the identification of five injured specimens since 2022 (Table 4) demonstrates that Ogygiocarella, specifically Ogygi. debuchii, represents another avenue for future research into injury patterns. There is also mounting evidence to support at least three distinct arthropods groups that could have targeted Ogygiocarella as prey. (1) The Middle Ordovician (Darriwilian) Castle Bank Biota fauna (Botting et al., 2023) includes a yohoiid-like arthropod that could have attacked these trilobites using raptorial appendages (Botting et al., 2023). (2) Ordovician eurypterids—forms known from Late Ordovician(Sandbian) aged Welsh deposits (Størmer, 1951; Tetlie, 2007)—have been highlighted as possible, albeit ineffective, predators of trilobites (Lamsdell et al., 2015; Bicknell, Melzer & Schmidt, 2022b; Schmidt et al., 2022). If they were the predators, eurypterids would have targeted trilobites during a soft-shelled stage. (3) The large asaphid trilobites themselves could have targeted each other and used gnathobasic spines on walking legs to process the biomineralised exoskeletons.

Beyond arthropods, nautiloids are commonly suggested as Ordovician predators of trilobites (Brett, 2003; Klug et al., 2018). These large cephalopods would have been able to grapple trilobites with tentacles and damage the exoskeletons with re-enforced beaks (Klug et al., 2018).