Exploring abnormal Cambrian-aged trilobites in the Smithsonian collection

Introduction

The Cambrian Explosion—a rapid and stunning increase in animal diversity and disparity during the earliest Paleozoic, over 500 million years ago—likely resulted from a combination of biological, ecological, and environmental factors (Smith & Harper, 2013; Zhang et al., 2014; Bicknell & Paterson, 2018). Among the ecological factors, the rise of predation has been considered a key evolutionary innovation that helped drive and shape morphological and diversity trajectories of different Cambrian groups (Vermeij, 1989; Conway Morris, 1998; Bengtson, 2002; Babcock, 2003; Wood & Zhuravlev, 2012; Bicknell & Paterson, 2018; Pates & Bicknell, 2019), including the rise of biomineralisation in the exoskeletons and shells of prey animals (Vermeij, 1989; Vermeij, 2013; Conway Morris & Jenkins, 1985; Babcock, 1993; Babcock, 2003; Conway Morris & Bengtson, 1994; Bicknell & Paterson, 2018). This biomineralisation also permitted the documentation of failed predation events, complications during moulting, as well as genetic, developmental and/or behavioural malfunctions in trilobites and other animals (Owen, 1985; Babcock, 1993; Babcock, 2007; Bicknell & Paterson, 2018).

Trilobites were an abundant, diverse, and disparate group of Paleozoic animals with biomineralised exoskeletons (Webster, 2007) that commonly record abnormal features. A range of Cambrian-aged trilobite abnormalities are known and have been used as a model system for exploring Cambrian predator–prey interactions (Owen, 1985; Conway Morris & Jenkins, 1985; Babcock & Robison, 1989; Babcock, 1993; Babcock, 2003; Lee, Choi & Pratt, 2001; Pates et al., 2017; Bicknell & Paterson, 2018; Vinn, 2018; Pates & Bicknell, 2019). Here, nine new examples of abnormal specimens from the Paleontological collection of the Smithsonian National Museum of Natural History (USNM PAL) are presented; a collection from which abnormal trilobites have previously been reported (Babcock, 1993; Bicknell, Pates & Botton, 2018d). These specimens aid the recent pulse in documentation of Cambrian predation traces and other abnormalities (Fatka, Budil & Grigar, 2015; Pates et al., 2017; Bicknell, Pates & Botton, 2018d; Bicknell & Pates, 2019; Klompmaker et al., 2019; Pates & Bicknell, 2019).

Methods

Cambrian-aged trilobite specimens in the USNM PAL were reviewed for evidence for abnormalities, as originally defined by Owen (1985). This definition has subsequently been used and further refined in studies of other abnormal arthropods (Babcock, 1993; Bicknell & Paterson, 2018; Bicknell & Pates, 2019; see section ‘Terminology’). Specimens were photographed using a Canon EOS REBEL T2i under LED (light-emitting diode) lighting. Measurements of abnormalities were made from photographs using ImageJ (version 1.52a; Schneider, Rasband & Eliceiri, 2012). Specimen ages were determined from the age of the host rock and comparisons to the literature, using the most recent geological timescale (Peng, Babcock & Cooper, 2012).

Results

Elliptocephala asaphoides Emmons, 1844, USNM PAL 18350a, Browns Pond Formation (=Schodack Formation) (Cambrian Stage 2, Series 4, age taken from Skovsted & Peel, 2007), eastern New York, USA. Figures 1A, 1B.

USNM PAL 18350a is preserved as an external mould with a ‘U’-shaped abnormality that truncates pleurae by 8 mm. Abnormality begins at thoracic segment 6, extends into thoracic segment 8, and is 15 mm long. The margin of the abnormality is cicatrised along thoracic segment 6, while thoracic segments 7 and 8 show no evidence for cicatrisation.

Mummaspis oblisooculatus Fritz, 1992, USNM PAL 443790, Mural Formation (Cambrian Series 2, Stage 4, age taken from Ortega Hernández, Esteve & Butterfield, 2013), Alberta, Canada. Figures 2A–2C.

USNM PAL 443790 is preserved as an external mould and displays a possible bilateral thoracic abnormality. Thoracic segments 3 and 4 on the left side have been truncated into an asymmetric ‘V’-shaped abnormality that is 3 mm long and slightly cicatrised (Fig. 2B). The thoracic segments are truncated pleurae by 9 mm. On the right side of the thorax, there is a potential SSI on thoracic segment 6 (Fig. 2C). However, closer examination of the specimen highlights that there are likely traces of more parts of the pleural spine. In this case, this feature reflects taphonomic alteration to the specimen, or poor breakage of the rock.

Olenellus thompsoni (Hall, 1859), USNM PAL 729428, Parker Formation (Cambrian Stage 2, Series 4, age taken from Webster & Landing, 2016), Vermont, USA. Figures 3A, 3B.

USNM PAL 729428 is preserved as an external mould with little relief and shows two abnormalities on the right posterior thorax. The more anterior abnormality has a ‘U’-shape, is observed on thoracic segments 7–9, and is slightly cicatrised. Thoracic pleurae 7 and 8 are fused together at the abnormality margin. The second abnormality is ‘W’-shaped, spans thoracic segments 11–13, and has a cicatrised margin. Both abnormalities truncate the thoracic pleurae by 6 mm.

Olenellus getzi Dunbar, 1925, USNM PAL 729422, Kinzers Formation (Cambrian Series 2, Stage 4), Pennsylvania, USA. Figures 4A, 4B.

USNM PAL 729422 is a partial specimen preserved as an external mould and displays two abnormalities on the right side of the thorax. The more anterior abnormality is an SSI on the 6th thoracic segment that shows no evidence of cicatrisation and truncates the pleura by 6 mm. Thoracic segment 7 shows possible evidence of two thoracic pleurae developing from the one thoracic segment. The split between these spines occurs ∼24 mm from the midline of the specimen. As the upper of the two pleurae shows terraced lines indicative of the ventral surface (Lieberman, 1999), it is possible that this specimen instead represents a fragment retained during moulting, or even the chance superimposition of a fragment on a complete specimen. Fragments on the specimen indicate that either of these two scenarios is possible; however, the alignment of the pleura with the segment, and its relative size, support a biological interpretation.

Nevadia weeksi Walcott, 1910, USNM PAL 56792a; USNM PAL 56792d, Pioche Formation (Miaolingian Series, Wuliuan, age taken from Kimmig, Meyer & Lieberman, 2018), Utah, USA Figs. 5A–5E.

USNM PAL 56792a is a partial specimen preserved as an external mould with an abnormality on the posterior right thorax (Figs. 5A, 5B). The abnormality is an SSI on the 16th thoracic segment. The pleura is terminated 2 mm from the thoracic axial lobe, rounded, and shows no evidence of cicatrisation. This abnormality truncates the pleura by 28 mm.

USNM PAL 56792d preserves the posterior section of the exoskeleton and has a bilaterally expressed injury. The plural spine on the 14th thoracic segment on the left side is an SSI that truncates the pleura by 10 mm (Fig. 5D). On the right thoracic side, the 11th and 12th segments show SSIs. The terminus of the 11th thoracic pleura is not rounded and truncated by at least 7 mm (Fig. 5E). The terminus of the 12th thoracic pleura is slightly rounded and truncated by at least 9 mm (Fig. 5E). No abnormalities on this specimen show evidence of cicatrisation.

Glossopleura gigantea Resser, 1939, USNM PAL 729419, Spence Shale Member, Langston Formation (Miaolingian Series, Wuliuan), Utah, USA Figs. 6A, 6B.

USNM PAL 729419 is preserved as an external mould and displays an abnormal right thorax. Abnormality is an SSI on the 4th thoracic segment that truncates the segment by 8 mm. The margin of the abnormality is rounded and slightly cicatrised.

Ogygopsis klotzi (Rominger, 1887), USNM PAL 729421, Stephen Formation (Miaolingian Series, Wuliuan), British Columbia, Canada. Figures 7A, 7B.

USNM PAL 729421 is preserved as an external mould and displays an abnormality on the left thoracic lobe. The abnormality has a shallow ‘W’-shape that begins at the 2nd thoracic segment, ends at ends at the 5th thoracic segment, is 10.5 mm long, and truncates the pleurae by 2 mm. Abnormality margin shows no evidence of cicatrisation. Thoracic pleurae 3 and 4 are fused together at the abnormality margin, while the margins of pleurae 2 and 5 are distorted about the fused section.

Elrathia kingii Meek, 1870, USNM PAL 729417, Wheeler Formation (Miaolingian Series, Drumian), western Utah, USA. Figures 8A, 8B.

USNM PAL 729417 is preserved as an external mould and displays an abnormality on the posterior right thorax that extends into the anterior pygidium. The abnormality has a ‘U’-shape, begins at the 10th thoracic segment, ends within the first 1 mm of the pygidium, is 4.6 mm long, and truncates the affected thoracic segments by 1.5 mm. The abnormality margin is slightly cicatrised and deforms thoracic segments 10–11.

Discussion

Comparing the nature of the abnormalities documented here with examples in other publications suggests that the specimens described in this contribution display repaired injuries, rather than examples of developmental or genetic aberrations (Owen, 1985; Conway Morris & Jenkins, 1985; Babcock & Robison, 1989; Babcock, 1993; Babcock, 2003; Babcock, 2007; Robison, Babcock & Gunther, 2015; Bicknell & Paterson, 2018; Bicknell, Paterson & Hopkins, 2019; Pates & Bicknell, 2019). The injuries that affect more than one thoracic segment and are located on thoracic areas that are unlikely to have been damaged by chance (Babcock & Robison, 1989; Babcock, 1993; Pates et al., 2017; Bicknell & Paterson, 2018) represent healed injuries, likely attributable to predation. Those injuries showing exoskeletal cicatrisation reflect an attack that occurred recently within the same intermoult period, as observed in modern arthropods (Ludvigsen, 1977; Bursey, 1977; Owen, 1985; Rudkin, 1985; Halcrow & Smith, 1986). Injuries that occurred during a soft-shelled stage, when individuals were likely more vulnerable to attacks, would likely have wrinkled and deformed the exoskeleton as it would not have been fully mineralised (Conway Morris & Jenkins, 1985; Bicknell & Paterson, 2018). Injuries lacking cicatrisation and showing partial regeneration likely occurred in prior moult stages (Owen, 1985; Pates et al., 2017). The SSIs observed in the studied sample may record attacks or moulting complications. In particular, the injuries on Nevadia weeksi likely reflect complications during moulting as the most elongated thoracic pleurae that would catch or not exit the old exoskeleton cleanly during ecdysis (Šnajdr, 1978; Owen, 1983; Conway Morris & Jenkins, 1985).

The studied sample presents possible evidence for injury patterns in an entirely qualitative context. This assessment provides potential support for an interpretation of injuries to trilobites caused by predators showing location specificity for the right side; if all injuries do indeed represent failed attacks (e.g., Babcock & Robison, 1989; Babcock, 1993). Six specimens have right-sided injuries, two specimens have potential bilateral injuries and one specimen has a left-sided injury. Although this sample size is too small to test for statistical significance, these data align with the thesis that either Cambrian predators attacked prey from the right side, Cambrian prey orientated themselves to have the right side attacked, or a combination of both (Babcock & Robison, 1989; Babcock, 1993; Eaton, 2019). Evidence for lateralised injury patterns in trilobite systems was also recently presented in the Silurian-aged Rochester Shale (Bicknell, Paterson & Hopkins, 2019). Conversely, Pates et al. (2017) and Pates & Bicknell (2019) reported no statistical evidence for this pattern in their studies of individual Cambrian taxa. As Pates & Bicknell (2019) outlined, studies of injury lateralisation that pool data on injuries from different time periods do not allow researchers to distinguish between potential causes of injuries, as the studied taxa are from different deposits. The true taxon-specific palaeoecological signal is therefore masked by variation in temporal and geographical conditions and it is unlikely that they all were under the same predatory selection pressures (Pates et al., 2017; Bicknell, Paterson & Hopkins, 2019; Pates & Bicknell, 2019). The identification of both Cambrian (Babcock, 1993; Eaton, 2019) and Silurian signals (Bicknell, Paterson & Hopkins, 2019), with the failure to detect a Cambrian signal (Pates et al., 2017; Pates & Bicknell, 2019), and post-Cambrian signal in other cases (Babcock, 1993) demonstrates that the causes of injury lateralisation are best considered on a case-by-case basis. Such an approach provides the best chance of identifying the root causes of an interesting ecological interaction.

No cephalic injuries were reported in this study. This rarity of cephalic injuries has been noted by previous workers (e.g., Owen, 1985; Babcock, 1993; Pratt, 1998). Biological explanations for this pattern could be that predators targeted the thorax and pygidium preferentially, a higher mortality rate of injuries to the head region, and/or trilobites protecting the head region through behavioural actions such as enrolment (Ortega Hernández, Esteve & Butterfield, 2013; Bicknell & Paterson, 2018; Pates & Bicknell, 2019). It is unlikely that it represents sampling bias, as specimens have been collated from a large number of collectors, and trilobite cephala and cranidia provide a wide range of taxonomic, morphometric, and phylogenetic characters and landmarks (e.g., Lieberman, 1999; Webster, 2015). Furthermore, in a bulk sample with no collection bias injured cephala were significantly rarer than thoracic injuries (Pates & Bicknell, 2019).

Conclusions

The current study of abnormal Cambrian trilobites within the Paleontological collection of the Smithsonian National Museum of Natural History presents nine new examples of injured specimens. These injuries display a range of morphologies that are attributed to failed predation and complicated moulting. The possible predatory groups are discussed, and euarthropods with gnathobases and other forms of robust spines are considered as the most probable predators. It is also highlighted that trilobites represent an ideal study system for documenting quantitative evidence for the Cambrian escalation event and responses of prey items to the first durophages.