Trilobites with malformations present important insight into the paleoecology of the wholly extinct arthropod group. This includes records of failed predation, developmental complications, and parasitic interactions. The documentation of malformed trilobites therefore allows for a more thorough understanding of these animals. Such summaries also permit larger-scale, synthetic works that consider patterns and processes associated with malformations to be developed. To expand the current record of malformed Cambrian through to Devonian trilobites, we report 16 novel specimens across 12 genera from deposits spanning Australia, Bolivia, Canada, the United States, and Wales. These specimens illustrate examples of injuries potentially caused by predation, molting, and accidental injury, teratological malformations, and pathological infestation. Possible predators; explanations for developmental, genetic, and recovery issues; as well as infestations are considered. Comparison of size distributions of malformed and nonmalformed Elrathia kingii indicates that primarily the largest specimens preserve malformations. This implies that either smaller specimens fully recovered from malformations or did not survive once the malformations were incurred. Continued documentation of malformed specimens will allow larger datasets to be compiled and further promote the use of malformations in understanding trilobite paleoecology.
INTRODUCTION
Trilobites are an iconic group of extinct arthropods (Hughes, 2007; Webster, 2007; Paterson et al., 2019; Paterson, 2020) and with over 22,000 species spanning the Cambrian to the end Permian (Adrain et al., 1998; Paterson, 2020; Peng et al., 2020a, 2020b), they are well documented within Paleozoic deposits (Sepkoski, 1981; Fortey, 2001; Babcock et al., 2017; Holmes and Budd, 2022). Their fossil record reflects their biomineralised exoskeleton that had a high preservational potential (Hughes, 2007; Holmes and Budd, 2022; Peng et al., 2020b). Importantly, this level of preservation, combined with the detailed taxonomic examination has allowed thorough exploration of topics in trilobite evolution and paleoecology (Brandt, 1996; Whittington, 1997; Westrop and Cuggy, 1999; Gaines and Droser, 2003; Farrell et al., 2011).
Malformed trilobites have been especially useful in understanding the paleoecology of the group (Owen, 1985; Babcock, 1993a, 1993b; 2003; 2007; Whittington, 1997). Three main malformation classifications can be defined—injuries, teratologies, and pathologies (see Terminology; Owen, 1985; Babcock, 1993b). Records of these malformations have allowed injury patterns (Oehlert, 1895; Hupé, 1953; Babcock and Robison, 1989; Babcock, 1993b; Pates et al., 2017; Bicknell et al., 2019; Zong et al., 2023), malformation recovery (Šnajdr, 1979; Conway Morris and Jenkins, 1985; Babcock, 1993b; McNamara and Tuura, 2011; Pates et al., 2017; Cheng et al., 2019; Zong and Bicknell, 2022; Bicknell et al., 2023a), and limits on body size and malformations (Bicknell et al., 2023a; Bicknell and Smith, 2022; Zong et al., 2023) to be explored. As a result, while malformations are known from other extinct arthropods (e.g., arachnids: Mitov et al., 2021; crustaceans: Bishop, 1972; Klompmaker et al., 2013, 2014; De Baets et al., 2022; and horseshoe crabs: Bicknell et al., 2018c, 2022c; De Baets et al., 2022), malformed trilobites are the most well-documented extinct arthropods (see Saito, 1934; Westergård, 1936; Resser, 1939; Palmer, 1958; Öpik, 1975, 1982; Šnajdr, 1978a; 1981; Owen, 1985; Babcock, 1993b, 2003, 2007; Bicknell and Paterson, 2018). Malformations are commonly recorded as anecdotal examples within larger taxonomic considerations (see notes in Owen, 1985; Babcock, 2007). However, more synthetic assessments of malformed trilobites have become more common (Owen, 1985; Babcock, 1993b; 2003; Bicknell et al., 2019, Zong et al., 2023).
The invertebrate paleontological collection in the American Museum of Natural History (AMNH) represents one of the largest active invertebrate fossil collection in North America. With over 100,000 trilobite specimens, this is an ideal target for documenting novel records of malformed trilobites. In considering this collection, 16 specimens across 12 genera are documented (figs. 1–13; table 1). Previous records of malformations for the species documented herein are also collated. Where possible, injury laterization patterns are considered, and malformations are contextualized using size data to further understand the distribution of malformations through ontogenetic sequences.
MATERIALS AND METHODS
Trilobite specimens within the AMNH were reviewed for possible malformations. Malformed specimens were photographed under LED light using an Olympus E-M1MarkIII camera. Most specimens were not coated prior to photography. However, when there was limited contrast between the fossil and matrix, specimens were coated with ammonium chloride to enhance contrast in photographs. Measurements of the specimens were gathered from images using ImageJ (Schneider et al., 2012).
Two-sided binomial tests were conducted to assess injury malformation stereotypy in Elrathia kingii (Meek, 1870) and Ogygopsis klotzi (Rominger, 1887) as both species have >10 documented malformations (tables 2–4). To limit the data to examples of records of failed predation, the E. kingii and O. klotzi specimens that show irrevocable evidence of predation were collated (see discussion in Babcock, 1993b, Terminology, and tables 2, 3). This constraint also limited us to considering specimens that are figured in the literature, or in the AMNH collection. These data were analyzed using the “binom.test” function (R Development Core Team, 2023) following (Pates et al., 2017; Supplemental Code 1 in the online supplement: https://doi.org/10.5531/sd.sp.70). The hypothesized probability of success was 0.5. This test assessed the following hypotheses:
H0: Injuries from failed predation are equally distributed on both sides of the exoskeleton.
H1: There are more injuries from failed predation on one side of the exoskeleton than the other.
In conducting these analyses, all injuries from failed predation were considered independent of each other. As such, specimens with bilaterally expressed injuries were treated as having one left and one right observation. Additionally, we reran the data presented in Babcock and Robison (1989) using the same implementation to compare our results to the original injury lateralization discussion.
For Elrathia kingii, size data from Hopkins (2021) were used to understand the distribution of malformed specimens in size space. Size data was measured from 229 specimens collected from a 1.5 meter interval at a single locality (North Antelope, House Range, Utah) and include meraspids (“juveniles” without the full complement of thoracic tergites) and holaspids (“adults” with the full complement of thoracic tergites). Four of these specimens showed malformations (figs. 4, 5; see also below). Measurements of the cephalon and pygidial length derived from eight additional malformed specimens previously reported in the literature (table 2) were added to the Hopkins dataset. Data were log10 transformed and plotted using R (R Development Core Team, 2023; Supplemental Code 1).
TERMINOLOGY
Malformation: Evidence for injuries, teratologies, or pathologies.
Injury: Exoskeletal breakage that occurred while the animal was still alive. This can record an attack, accidental injury, or molting issues (Owen, 1985; Babcock, 1993b; Bicknell et al., 2018c; Bicknell and Pates, 2020). Injuries do not extend across the entire specimen as these kinds of breakages reflect postmortem compaction (Leighton, 2011). Larger injuries have L-, U-, V-, or W-shapes (Babcock, 1993b; Bicknell et al., 2022a, 2023a) and smaller injuries are a single spine injury (SSI; Pates and Bicknell, 2019; Bicknell and Pates, 2020). Finally, injuries often show evidence for cicatrization and repair, but this depends on the degree of exoskeletal recovery. The origins of these injuries require examination of the injury location and morphology (Babcock, 1993b, 2003, 2007).
Teratology: External expressions of developmental, embryological, or genetic malfunctions observed on the exoskeleton (see Owen, 1985, and Babcock, 1993b). Although uncommon, they can be associated with injuries. These morphologies include addition or removal of nodes, segments, and spines, as well as aberrant rib and furrow morphologies (Owen, 1985; Babcock, 1993b; Bicknell and Smith, 2021).
FIGURE 1.
Malformed Xystridura sp. from the Beetle Creek Formation (Miaolingian, Wuliuan), Australia. AMNH-FI-140616. A. Semiarticulated specimen lacking librigena, dorsal view. B. Close up of box in A, showing SSI (white arrow). Scale bars: A, 10 mm; B, 5 mm. Specimen coated in ammonium chloride. Images converted to grayscale.
Pathology: Malformed exoskeletal sections resulting from parasitic activity or infections. These structures are often expressed as circular to ovate swellings (Šnajdr, 1978b; Owen, 1985; Babcock, 1993b; De Baets et al., 2022).
RESULTS
The specimens documented herein are described in detail below. This material is summarized in table 1.
Cambrian Trilobites
Xystridura sp.; AMNH-FI-140616. Beetle Creek Formation (Miaolingian, Wuliuan); Queensland, Australia (fig. 1). AMNH-FI-140616 is a molted specimen, consisting of a partial cephalon and thorax. The specimen is 52.6 mm long and 42.5 mm wide across the anterior thorax (fig. 1A). The specimen has an SSI that truncates the 5th thoracic pleura on the left side by 3.4 mm. Malformed pleural spine is rounded (fig. 1B).
Ogygopsis klotzi (Rominger, 1887); AMNH-FI-140617. Campsite Cliff Shale Member, Burgess Shale Formation (Miaolingian, Wuliuan); British Columbia, Canada (fig. 2). AMNH-FI-140617 is a molted exoskeleton that is 74.9 mm long and 38.4 mm across the anterior thorax (fig. 2A). The specimen has a pygidial malformation. This is an asymmetric V-shaped indentation on the left side that extends 4.9 mm from the pygidial margin toward the pygidial axial lobe (fig. 2B). There is cicatrization along the malformation border.
FIGURE 2.
Malformed Ogygopsis klotzi (Rominger, 1887), Campsite Cliff Shale Member, Burgess Shale Formation (Miaolingian, Wuliuan), British Columbia, Canada. AMNH-FI-140617. A. Semiarticulated specimen lacking librigena in dorsal view. B. Close up of box in A, showing V-shaped indentation. Scale bars: A, 10 mm; B, 5 mm. Specimen coated in ammonium chloride. Images converted to grayscale.
Olenoides serratus (Rominger, 1887); AMNH-FI-140614, Burgess Shale Formation, (Miaolingian, Wuliuan); British Columbia, Canada (fig. 3). AMNH-FI-140614 is an articulated exoskeleton that is 64.7 mm long and 41.2 mm wide across the cephalon (fig. 3A). The specimen has an L-shaped indentation on the left thoracic pleural lobe. This indentation truncates the 5th and 6th thoracic pleural spines by 1.8 mm and shows limited exoskeletal thickening (fig. 3B: black arrows).
Elrathia kingii (Meek, 1870); AMNH-FI-115591, 115736, 116781, 134438. Wheeler Formation (Miaolingian, Drumian); Utah (figs. 4, 5). AMNH-FI-134438 is a molted specimen that is 20.1 mm long and 12.5 mm wide across the anterior thorax (fig. 4A). The specimen has a malformation on the left thoracic pleural lobe (fig. 4D). The malformation consists of a W-shaped indentation that truncates the 8th and 9th thoracic pleurae by 0.6 and 0.9 mm, respectively. Additionally, the thoracic pleurae edges between these thoracic tergites are deformed, showing possible fusion proximal to the axial lobe. Both malformed pleural spines are rounded.
FIGURE 3.
Malformed Olenoides serratus (Rominger, 1887), Burgess Shale Formation, (Miaolingian, Wuliuan), British Columbia, Canada. AMNH-FI-140614. A. Articulated specimen in dorsal view. B. Close up of box in A, showing L-shaped indentation (black arrows). Scale bars: A, 10 mm; B, 5 mm. Specimen coated in ammonium chloride. Images converted to grayscale.
AMNH-FI-116781 is a molted specimen that is 31.9 mm long and 17.8 mm wide across the anterior thorax (fig. 4B). The specimen has a malformation on the right thoracic pleural lobe (fig. 4E). The malformation is a W-shaped indentation that truncates the 11th and 12th thoracic pleurae by 2.0 and 1.4 mm respectively. Both malformed pleural spines are rounded.
AMNH-FI-115591 is a molted specimen that is 26.7 mm long and 16.6 mm wide across the anterior thorax (fig. 4C). The specimen has a malformation on the left thoracic pleural lobe (fig. 4F). The malformation is an SSI that truncates the 1st thoracic pleura by 2.0 mm. The malformed pleural spine is rounded.
TABLE 2.
Summary of malformed Elrathia kingii documented within the literature. Interpretations of the malformations reflect proposals in the original literature and our assessment of the novel specimens presented herein.
TABLE 3.
Summary of malformed Ogygopsis klotzi documented within the literature. Interpretations of the malformations reflect proposals in the original literature and our assessment of the novel specimens presented herein.
AMNH-FI-115736 is a molted specimen that is 37.7 mm long and 22.7 mm wide across the anterior thorax (fig. 5A). The specimen has three malformations on the left thoracic pleural lobe (fig. 5B). The anterior malformation is an SSI that truncates the 3rd pleural spine by 1.5 mm. The posterior malformation is an SSI that truncates the 5th pleura by 3.5 mm. Both have rounded pleural spines. Furthermore, a 0.3 mm in diameter ovate structure is located 1.7 mm from the truncated edge of the 5th pleura.
Hemirhodon amplipyge Robison, 1964; AMNH-FI-140613. Duchesnay Unit, Chancellor Group (Miaolingian, Drumian); British Columbia, Canada (fig. 6). AMNH-FI-140613 is an articulated specimen that is 90.8 mm long and 52.6 mm wide across the cephalon (fig. 6A). The specimen has two thoracic malformations (fig. 6B, C). One on the left pleural lobe; a V-shaped indentation that extends 9.6 mm from the exoskeletal border and impacts the 6th and 7th pleurae (fig. 6B). The other on the right pleural lobe; an SSI that truncates the 6th thoracic pleura by 3.6 mm (fig. 6C). Both malformations are cicatrized.
FIGURE 4.
Malformed Elrathia kingii (Meek, 1870) from the Wheeler Formation (Miaolingian, Drumian), Utah, showing thoracic malformations (A, D: AMNH-FI-134438; B, E: AMNH-FI-116781; C, F: AMNH-FI-115591). A. Semiarticulated specimen lacking librigena in dorsal view. B. Semiarticulated specimen lacking librigena in dorsal view. C. Semiarticulated specimen lacking librigena in dorsal view. D. Close up of box in A showing W-shaped indentation (black arrows) and deformed thoracic pleurae. E. Close up of box in B showing W-shaped indentation (black arrows). F. Close up of SSI on left side of thorax (black arrow). Scale bars: A–C, 5 mm; D–F, 1 mm. A, C. Specimen coated in ammonium chloride; images converted to grayscale.
Modocia typicalis (Resser, 1938); AMNH-FI-116562, AMNH-FI-116559. Marjum Formation (Miaolingian, Drumian), Utah (fig. 7). AMNH-FI-116562 is a damaged, articulated specimen that is 42.4 mm long and 30.7 mm wide across the cephalon (fig. 7A). The specimen has a malformation on the left pleural lobe (fig. 7C). This is an SSI that truncates the 11th thoracic pleura by 3.5 mm compared to the right side. The malformed pleural spine is rounded.
TABLE 4.
Binomial analyses of injury patterns for Elrathia kingii, Ogygopsis klotzi, and the Babcock and Robison (1989) data. The original p-values presented in Babcock and Robison (1989) are also presented in brackets. The significance threshold for p-values was <0.05. x, number of specimens with left-sided injuries; n, total number of injury observations; α, tested significance level.
AMNH-FI-116559 is a molted specimen that is 10.7 mm long and 6.5 mm wide across the anterior thorax (fig. 7B). The specimen has two malformations on the left pleural lobe (fig. 7D). One is an SSI that truncates the 10th thoracic pleura by 0.35 mm, and a second SSI that truncates the 11th thoracic tergite by 0.42 mm. Both malformed pleural spines appear rounded. The 5th and 6th thoracic tergites show no rounding and are broken postmortem.
Ordovician Trilobites
Ogygiocarella debuchii (Brongniart, 1822); AMNH-FI-62055. Llanfawr Mudstones (Middle to Late Ordovician, Darriwilian to Sandbian boundary), Wales, UK (fig. 8). AMNH-FI-62055 is an external impression showing a partial cephalon, thorax, and pygidium. The specimen is 76.6 mm long and 59.9 mm wide across the pygidium (fig. 8A). The specimen has a pygidial malformation (fig. 8B). The specimen has a shallow U-shaped indentation along the right pygidial posterior margin (left side in life) that is 9.3 mm long and extends 0.9 mm from the pygidial margin. Impressions of faint, concentric terrace ridges observed on other sections of the pygidium are not present proximal to the malformation.
Acidaspis cincinnatiensis (Meek, 1873); AMNH-FI-1413. McMillan Formation (Upper Ordovician, Katian), Ohio (fig. 9). AMNH-FI-1413 is an isolated, partial pygidium that is 19.7 mm wide (fig. 9A). The specimen has a malformation on the left, 3rd (hypertrophied) posterior marginal spine (fig. 9B). The spine is truncated by 4.3 mm compared to the same spine on the right side. The malformed spine also shows rounding distally.
Isotelus iowensis (Owen, 1852); AMNH-FI-62046. Elgin Member, Scales Formation, Maquoketa Group, (Upper Ordovician, Katian), Illinois (fig. 10). AMNH-FI-62046 is an isolated pygidium that is 32.2 mm long and 42.5 mm wide (fig. 10A). The specimen has a W-shaped indentation, extending a maximum of 2.8 mm from the edge of the left pygidial margin (fig. 10B).
Silurian Trilobites
Dalmanites limulurus (Green, 1832); AMNH-FI-140615. Rochester Shale (Wenlock, Sheinwoodian), New York (fig. 11). AMNH-FI-140615 is a partially preserved, articulated specimen consisting of a damaged cephalon, complete thorax, and partial pygidium. The specimen is 42.7 mm long and 33.2 mm wide across the cephalon (fig. 11A). The specimen has a 2.8 mm wide ovate structure on the 3rd thoracic tergite of the left pleural lobe (fig. 11B). This malformation has deformed the 1st and 2nd pleurae, resulting in them bowing anteriorly.
Devonian Trilobites
Dalmanites pleuroptyx (Green, 1832); AMNH-FI-71576. Kalkberg Formation, Helderberg Group, (Lower Devonian, Lochkovian), New York (fig. 12). AMNH-FI-71576 is a plaster cast of a partial, isolated, pygidium that is 62.1 mm long and 55.4 mm wide along the anterior (fig. 12A). The specimen has a malformation on the right side (fig. 12B). The specimen is deformed at the ?11th and ?12th pygidial ribs (? denotes uncertainty regarding rib count due to specimen damage; fig. 12B: black arrows). The ribs are fused 9.1 mm from the pygidial axis. The fusion has produced an L-shaped indentation in the ?11th rib 5.9 mm from the pygidial axis (fig. 12B: white arrow).
FIGURE 6.
Malformed Hemirhodon amplipyge Robison, 1964, from the Duchesnay unit, Chancellor Group (Miaolingian, Drumian), British Columbia, Canada (AMNH-FI-140613). A. Articulated specimen in dorsal view. B. Close up of box in A, showing V-shaped indentation on the left side of thorax. C. Close up on SSI on right side of thorax (black arrow). Scale bars: A, B, 10 mm; C, 5 mm. Specimen coated in ammonium chloride; images converted to grayscale.
Vogesina sp. AMNH-FI-140618. Belén Formation (Lower to Middle Devonian, Pragian to Eifelian), Bolivia (fig. 13). AMNH-FI-140618 is an isolated pygidium that is 19.6 mm long and 22.4 mm wide (fig. 13A). The specimen has a malformation on the right side (fig. 13B), including deformed pygidial ribs on ribs 2, 3, and 4. The second rib has a distal, exsagittal increase in length reflecting a hooklike shape, the 3rd rib is deformed into a reverse S-shape, and the 4th rib has a U-shaped morphology.
Patterns in Malformations
Possible malformation patterns associated with evidence of failed predation can be explored by collating all previous examples of malformations for the species documented here (tables 2, 3, 5–8). To our knowledge, malformations in Acidaspis cincinnatiensis, Isotelus iowensis, Dalmanites limulurus, Dalmanites pleuroptyx, and Vogesina sp. are figured here for the first time. Hemirhodon amplipyge (table 6), Modocia typicalis (table 7), Ogygiocarella debuchii (table 8), and Olenoides serratus (table 5) each have fewer than five documented malformed specimens in the literature. This small sample size precludes the statistical examination of malformation patterns in these species (table 9). However, patterns for Elrathia kingii and Ogygopsis klotzi can be considered (tables 2, 3).
FIGURE 7.
Modocia typicalis (Resser, 1938) from the Marjum Formation (Miaolingian Series, Drumian), Utah. (A, C, AMNH-FI-116562; B, D, AMNH-FI-116781). A. Semiarticulated specimen lacking librigena in dorsal view. C. Close up of box in A showing possible SSI and rounded pleural spine (black arrow). B. Semiarticulated specimen lacking librigena in dorsal view. D. Close up of box in B showing two possible SSIs (black and white arrows). Scale bars: A, 7 mm; B, 2 mm; C, D, 1 mm.
FIGURE 8.
Malformed Ogygiocarella debuchii (Brongniart, 1822) from the Llanfawr Mudstones (Middle to Late Ordovician, Darriwilian to Sandbian boundary), Wales, UK (AMNH-FI-62055). A. Articulated specimen in ventral view. B. Close up of box in A, showing U-shaped indentation (white arrow) and lack of pygidial ribs. Scale bars: A, 10 mm; B, 5 mm. Specimen coated in ammonium chloride; images converted to grayscale.
Examination of Elrathia kingii specimens revealed that 75% of malformations attributed to failed predation are located on the right exoskeletal side, while 25% of such malformations extend from the thorax to the pygidium (table 9). For Ogygopsis klotzi specimens, 67% of malformations attributed to failed predation were located on the right exoskeletal side, 36% on the pygidial region, and 8% extending from the thorax to the pygidium (table 9). Expanding this consideration to injury stereotypy, binomial analyses of malformation distribution for both species show no statistical support for left-right malformation stereotypy (table 3). Reanalysis of the Babcock and Robison (1989) datasets indicated significant injury lateralization pattern in the dataset that considered Cambrian-aged trilobites (table 4; p = 0.001) but not post-Cambrian-aged trilobites (table 4, p = 0.1214).
FIGURE 9.
Possible malformed Acidaspis cincinnatiensis (Meek, 1873) from the McMillan Formation (Upper Ordovician, Katian), Ohio (AMNH-FI-1413). A. Pygidium in ventral view. B. Close up of box in A, showing reduced pygidial spine. Scale bars: A, 5 mm; B, 2 mm.
Examining the malformed Elrathia kingii using the Hopkins (2021) size dataset illustrates malformed specimens compared to nonmalformed individuals in bivariate size space (fig. 14). Most malformed specimens fall within the same space as the largest specimens in the dataset. Malformed specimens therefore cluster at the end of the ontogenetic trajectory. One specimen (AMNH-FI-134438) is located within the smaller nonmalformed specimens. None of the malformed specimens are meraspids.
DISCUSSION
Injuries
Considering malformations documented here, 13 specimens show evidence of indentations in or removal of an exoskeletal region. The malformations on Xystridura sp. (fig. 1), Ogygopsis klotzi (fig. 2) Olenoides serratus (fig. 3), Elrathia kingii (figs. 4, 5), Hemirhodon amplipyge (fig. 6), Ogygiocarella debuchii (fig. 8), Acidaspis cincinnatiensis (fig. 9), and Isotelus iowensis (fig. 10) are comparable to malformations considered injuries (see Rudkin, 1979; Owen, 1985; Babcock, 1993b, 2003, 2007; Budil et al., 2010; Fatka et al., 2015; Bicknell and Pates, 2020; Zong, 2021a; 2021b; Bicknell et al., 2022a, 2023a; Zong et al., 2023). Importantly, as many of these injuries show cicatrization and regeneration, we propose that these specimens survived the injuries.
FIGURE 10.
Malformed Isotelus iowensis (Owen, 1852) from the Elgin Member, Scales Formation, Maquoketa Group (Upper Ordovician, Katian), Illinois (AMNH-FI-62046). A. Pygidium in dorsal view. B. Close up of box in A, showing W-shaped indentation (black arrows). Scale bars: A, 10 mm; B, 5 mm.
Three main divisions of the injuries are documented: possible failed predation, accidental injury, and molting complications. Injuries with L-, U-, V-, and W-shaped indentations (figs. 2, 3, 4A, B, D, E, 6A, B, 8, 10) are comparable to injuries ascribed to failed predation attempts (Rudkin, 1979; 1985; Babcock, 2007; Bicknell et al., 2022e). Furthermore, these species lack large spines that would have caused complications in molting (Conway Morris and Jenkins, 1985; Bicknell and Pates, 2020; Bicknell et al., 2022a).
In contrast, the SSIs on Xystridura sp. (fig. 1), Elrathia kingii (figs. 4C, F, 5), and Hemirhodon amplipyge (fig. 6C) are small injuries located on thoracic pleurae that lack large spines. We can therefore exclude these injuries as evidence of molting complications and are considered possible records of accidental injury.
One injured Elrathia kingii shows the disruption of thoracic pleurae proximal to an injury (fig. 4D). Given the proximity of this malformation to an injury, these deformed pleurae likely reflect abnormal recovery from an attack, as opposed to a teratological malformation. The specimen may have been attacked during the soft-shelled stage (shortly after molting), and the exoskeleton was heavily deformed as a result. This sort of deformation could have been fixed within subsequent molts (Conway Morris and Jenkins, 1985; Rudkin, 1985; Bicknell et al., 2023a).
Cambrian Predators
Records of injured Cambrian trilobites have traditionally been ascribed to predation by radiodonts (Rudkin, 1979; Nedin, 1999; Moysiuk and Caron, 2021; Zhang et al., 2023). However, recent three-dimensional modelling of Anomalocaris canadensis Whiteaves, 1892, has demonstrated that some radiodonts were ineffective at processing biomineralized prey (De Vivo et al., 2021; Bicknell et al., 2023c) and others have been reinterpreted to be suspension or filter feeders (Vinther et al., 2014; Potin and Daley, 2023). As such, other cooccurring arthropods may have caused these injuries. Trilobites and other artiopodans with reinforced gnathobasic spines on walking legs are likely options (Whittington, 1980; Bruton, 1981; Briggs and Whittington, 1985a; Robison, 1991; Bicknell et al., 2018b; Holmes et al., 2020). These arthropods are thought to have processed prey similarly to modern horseshoe crabs (Whittington, 1975; Botton, 1984; Bicknell et al., 2018a, 2021). Records of trilobite-rich coprolites (Daley et al., 2013; Bicknell et al., 2022a) and cololites in artiopodan guts (Zacaï et al., 2016; Bicknell and Paterson, 2018) support this hypothesis.
FIGURE 11.
Malformed Dalmanites limulurus (Green, 1832) from the Rochester Shale (Wenlock, Sheinwoodian), New York (AMNH-FI-140615). A. Articulated specimen in dorsal view. B. Close up of box in A, showing the neoplasm on the third thoracic tergite (white arrow). Scale bars: A, 10 mm; B, 5 mm. Specimen coated in ammonium chloride. Images converted to grayscale.
Another possible predator group are the carnivorous priapulid worms (Conway Morris, 1977; Vannier and Chen, 2005; Schwimmer and Montante, 2007; Kimmig and Strotz, 2017; Bicknell and Paterson, 2018; Kimmig and Pratt, 2018; Pratt and Kimmig, 2019). Biomineralized prey—brachiopods, hyolithid conchs, and small trilobite fragments—have been found in Cambrian priapulid worm guts (Babcock and Robison, 1988; Conway Morris, 1977; Schwimmer and Montante, 2007; Vannier, 2012). The rows of teeth in priapulid pharynxes could have captured small, slow-moving benthic prey for consumption (Huang et al., 2004; Vannier and Chen, 2005). However, trilobites considered here are at least one order of magnitude larger than material documented within gut priapulid contents (Vannier and Chen, 2005). As such, carnivorous worms are excluded here as possible producers.
FIGURE 12.
Plaster cast of malformed Dalmanities pleuroptyx (Green, 1832) from the Kalkberg Formation, Helderberg Group (Lower Devonian, Lochkovian), New York (AMNH-FI-71576). A. Pygidium in dorsal view. B. Close up of box in A, showing deformed and fused pygidial pleurae (black arrows) and the L-shaped indentation (white arrow). Scale bars: A, 10 mm; B, 2 mm. Specimen coated in ammonium chloride; images converted to grayscale.
Ordovician Predators
The Ordovician saw the rise of more arthropod predator groups that could have targeted Isotelus iowensis and Ogygiocarella debuchii. Similar to Cambrian deposits, large trilobites and other benthic arthropods with reinforced gnathobasic spines on walking legs are proposed as possible predators (Bicknell et al., 2022d). Ordovician eurypterids (Caster and Kjellesvig-Waering, 1964; Tollerton, 2003; Lamsdell et al., 2013, 2015; Hawkins et al., 2018; Bicknell et al., 2022b; Braddy and Gass, 2023; Wang et al., 2023)—large marine chelicerates—have also been highlighted as possible predators of trilobites. While the effectiveness of these chelicerates in processing trilobites is debated (Lamsdell et al., 2015; Bicknell et al., 2022b, 2024; Schmidt et al., 2022), they likely used anteriorly directed raptorial appendages to gather recently molted trilobites for processing with gnathobasic spines on walking and swimming legs (Selden, 1981; Poschmann et al., 2017; Bicknell et al., 2018b, 2020b, 2023b).
FIGURE 13.
Malformed Vogesina sp. from the Belén Formation (Lower to Middle Devonian, Pragian to Eifelian), Bolivia (AMNH-FI-140618). A. Pygidium in dorsal view. B. Close up of area with deformed pleurae (black arrows). Scale bars: A, 5 mm; B, 1 mm. Specimen coated in ammonium chloride; images converted to grayscale.
One more option is Ordovician archaeostracan phyllocarids (Collette and Hagadorn, 2010; Bicknell et al., 2020a; Liu et al., 2022, 2023)—crustaceans that used large, reenforced mandibles (Signor and Brett, 1984; Brett and Walker, 2002; Brett, 2003) to consume mollusks, arthropods, and carrion (Bergström et al., 1987; Vannier et al., 1997; Bergmann and Rust, 2014; Liu et al., 2022). However, as Ordovician phyllocarids are, at maximum, 5 cm long (Racheboeuf and Crasquin, 2010; Fatka et al., 2022; Liu et al., 2023), they were much smaller than injured Ordovician trilobites. As such, it seems trilobites and possibly eurypterids are the most likely arthropods to have caused the observed injuries.
The other major predatory group that could have caused the injuries are cephalopod mollusks—animals identified as apex predators in Ordovician paleoecosystems (Brett and Walker, 2002). Indeed, cephalopods have commonly been suggested as causes for injured Ordovician trilobites (Rudkin, 1985; Babcock, 2003; Brett, 2003; Klug et al., 2018; Bicknell et al., 2022d) and the presence of trilobites within the crop of Ordovician cephalopods strongly supports this idea (Brett and Walker, 2002). It seems plausible that cephalopods could have gathered Ordovician trilobites with tentacles for subsequent processing with a reenforced beak.
FIGURE 14.
Measurements of Elrathia kingii and bivariate plot showing distributions of malformations. A. Bivariate space of E. kingii. Malformed specimens cluster with the largest specimens. B. Reconstruction of E. kingii showing measurements used in A. Data found in Supplemental Data 1 (available online: https://doi.org/10.5531/sd.sp.70). Data were log10 transformed for plotting. Abbreviations: cl, cephalic length; pl, pygidium length.
Teratologies
Teratological malformations for trilobites often reflect the addition, removal, or deformation of spines, furrows, ribs, tergites, and nodes (Owen, 1985; Babcock, 1993b). Within the examined specimens, we documented examples of teratologies in Dalmanities pleuroptyx (fig. 12), and Vogesina sp. (fig. 13) specimens. Teratologies located in the pygidial regions are expressed as abnormal rib morphologies that are grouped into (1) deformed and deflected ribs (figs. 12, 13) and (2) fusion of ribs (fig. 12).
Deformed pygidial ribs and furrows are well documented teratologies in the trilobite fossil record (Šnajdr, 1958, 1981; Přibyl and Vaněk, 1973; Strusz, 1980; Owen, 1985; Budil et al., 2010; Nielsen and Nielsen, 2017). These malformations are commonly attributed to genetic or embryological malfunctions (Owen, 1985). We consider this likely for the deformed ribs documented herein. The prevalence of these malformations on the pygidium suggests that this exoskeletal section may have been more susceptible to experiencing genetic or developmental complications.
Fused pygidial ribs and furrows reflect genetic malfunctions or abnormal recovery from injuries (Ormiston et al., 1967; Šnajdr, 1981; Owen, 1985; Rudkin, 1985; Nielsen and Nielsen, 2017; Bicknell and Smith, 2021). For the example considered here (fig. 12B), the fused ribs are associated with deformed ribs and show no evidence of an injury. These likely have a genetic or embryological origin.
TABLE 5.
Summary of injured Olenoides serratus documented within the literature.
Pathologies
The presence of pathological structures on trilobites presents important insight into the role of trilobites as possible parasite hosts (Jell, 1989; Babcock, 2003; De Baets et al., 2022). Within the malformed specimens considered here, we identified three examples of circular to ovate structures that are comparable to other examples of neoplasms (see reviews in Šnajdr, 1978a; 1978b; Owen, 1985; Babcock, 2003; De Baets et al., 2022). To date, neoplasmic growths have been reported in Cambrian bathynotids (Elicki and Geyer, 2013), estaingiids (Bicknell et al., 2023a), paradoxidids (Westergård, 1936; Bergström and Levi-Setti, 1978; Šnajdr, 1978a; Babcock, 2003, 2007), proasaphiscids (De Baets et al., 2022), redlichids (Bicknell et al., 2022a); Ordovician asaphids (Owen, 1985; Hughes, 1993; 2001), cheirurids (Ludvigsen, 1977; Conway Morris, 1981), dalmanitids (Vokáč, 1996); Silurian harpetids (Šnajdr, 1978b), tropidocoryphids (Šnajdr, 1981); and Devonian dalmanitids (Šnajdr, 1987), scutelluids (Šnajdr, 1960), styginids (Rábano and Arbizu, 1999), and tropidocoryphids (Šnajdr, 1981). The neoplasmlike structures presented here expand the record of trilobite neoplasms into Alokistocaridae (Elrathia kingii), and Calmoniidae (Vogesina), while bolstering the records of neoplasms on dalmanitid trilobites (Dalmanites limulurus). Furthermore, it seems that when large neoplasms develop on the thorax (fig. 11), exoskeletal sections could have deformed around the neoplasm and additional molting events may have increased the neoplasm size.
Possible explanations for neoplasm causes are limited due to the sparse fossil record of possible producers (Šnajdr, 1978b; Owen, 1985; Babcock, 2003; De Baets et al., 2022). However, likely causes can be suggested using modern systems. These include “viruses, bacteria, protists, fungi, algae, multicellular plants, and parasitic animals” (De Baets et al., 2022: 193). Continued examination of modern arthropods, such as crustaceans and horseshoe crabs, might present new insight into neoplasm in trilobites.
Ambiguous Cases
The identified Modocia typicalis specimens documented here show possible evidence for SSIs (fig. 7). However, we are unable to unambiguously state that these are indeed examples of injuries, as they appear to have been somewhat overprepared. They are included here to highlight that care must be taken when documenting malformations on prepared specimens.
TABLE 6.
Summary of malformed Hemirhodon amplipyge within the literature.
The figured Acidaspis cincinnatiensis specimen shows possible evidence for truncation of a hypertrophied pygidial spine (fig. 9). As these spines are large, it is possible that this individual experienced complications during molting (Drage and Daley, 2016; Drage et al., 2018; Bicknell and Pates, 2020). However, the specimen was repaired on the right side, so we cannot unambiguously state that this represents an injury.
Malformation Patterns over Geological Time
Considering the examples presented here (table 1, figs. 1–13) there is an apparent bias for injured Cambrian and Ordovician specimens and Silurian and Devonian forms with teratologies. While this pattern has been observed in other trilobite malformation meta-analyses (Owen, 1985; Bicknell and Smith, 2021, 2022), injured Silurian trilobites have also been documented (Rudkin, 1985; Babcock, 1993a; Whiteley et al., 2002; Bicknell et al., 2019). This topic remains an open question that cannot be fully addressed here. Indeed, we highlight that detailed examination of trilobite malformations is likely needed to explore this topic more thoroughly. Regardless, we present an array of explanations for this pattern:
The decrease in injured trilobites in younger deposits reflects a transition to different prey groups after the Ordovician. In this situation, trilobites were targeted less commonly, although some predation continued into at least the Silurian.
The evolution of eurypterids and jawed fishes—large, pelagic predators—resulted in the complete consumption of targeted trilobites. In this case, a notable record for trilobite-rich coprolites in post-Cambrian deposits is expected. However, these coprolites are markedly rare (Rolfe, 1973; Toom et al., 2020; Bicknell et al., 2023d, 2024).
An increased abundance of genetic malformations in younger forms may reflect some level of chromosomal plasticity (Babcock, 2007), despite a proposed reduction in plasticity in non-Cambrian trilobites (Webster, 2007) and the increased within-family conservation of segmentation patterns across the Paleozoic (Hopkins and To, 2022). This possibility requires more detailed consideration of patterns reflecting longer-term, genetic complications in trilobites.
Genetic malformations reflect smaller population sizes within geographically limited areas within younger forms. This would have resulted in genetic bottlenecks and possible inbreeding. However, this is not innately testable within the fossil record.
Sampling bias produced the pattern. As injuries are often more pronounced malformations compared to teratologies (Owen, 1985), when fewer injuries are identified, teratologies are more commonly noted. However, considering an exceptionally large sample of Estaingia bilobata Pocock, 1964, from the Cambrian (Series 2, Stage 4) Emu Bay Shale (Paterson et al., 2016; Drage et al., 2018; Bicknell et al., 2023a; Drage et al., 2023) resulted in the record of three teratologies and six injuries (Bicknell et al., 2023a). As such, the presence of injuries within a sample should not impact the identification of teratologies.
TABLE 7.
Summary of malformed Modocia typicalis within the literature. Note the malformed specimens documented here are considered uncertain examples, due to possible over preparation of the specimens.
Malformation Lateralization from Failed Predation
Lateralization in trilobite malformations reflecting failed predation has been explored since Babcock and Robison (1989) presented the possibility that Cambrian trilobite injury lateralization indicated predator preference (Babcock and Robison, 1989; Babcock, 1993b; 2003; 2007). Previous approaches focused on larger samples sizes with multiple species and binned data. In doing so, they overcame a core limitation in understanding injury patterns—the rarity of injured trilobites in the fossil record. This dataset shows exceptionally strong (p = 0.001) statistical support for lateralization in failed predation on Cambrian trilobites. Examination of injury lateralization in single species study systems has provided different interpretations of the injury pattern. Injured Redlichia takooensis Lu, 1950, from the Emu Bay Shale (Cambrian Series 2, Stage 4) (Bicknell et al., 2022a), Eccaparadoxides pradoanus (Verneuil and Barrande in Prado et al., 1860) from the Murero Formation (Miaolingian, Drumian) (Pates et al., 2017), and olenelloid species from the Ruin Wash Lagerstätte (Cambrian Series 2, Stage 4) (Pates and Bicknell, 2019) lack evidence for injury lateralization. The Ogygopsis klotzi and Elrathia kingii specimens showing evidence for failed predation (tables 2–4) reflect these single species patterns. We fail to demonstrate statistical support for lateralization in injuries from failed predation in O. klotzi, but note weak (p = 0.146) support for this pattern in E. kingii. Our results differ from Babcock and Robison (1989) due to at least two compounding conditions:
Our datasets consist of smaller sample sizes compared to Babcock and Robison (1989). This was an unavoidable outcome of examining patterns within single species (see next section). This decreased the power of the statistical tests compared to the larger dataset.
The means of performing the binomial tests were likely different. We could not reproduce the results presented in Babcock and Robison (1989) using functions available in the R Statistical Programming Language. The “binom.test” function may have calculated p-values differently from the original work.
TABLE 8.
Summary of malformed Ogygiocarella debuchii within the literature.
These differences limit the scope for interpreting patterns of failed predation in Ogygopsis klotzi and Elrathia kingii. We fail to reject the null hypotheses for both datasets. However, the E. kingii dataset suggests that there might be evidence for injury laterization in this species. Additional examples of injuries from failed predation for E. kingii and rerunning of these analyses are therefore needed to address this topic further.
Malformation Distribution
To date, four datasets have examined the location of malformed and nonmalformed specimens in size space (Bicknell et al., 2022a, 2023a; Bicknell and Smith, 2022; fig. 14). In all cases, the majority of malformed specimens cluster among the largest individuals in bivariate spaces. This provides evidence for survivorship bias (Bicknell et al., 2023a), specifically that only the largest individuals could recover from malformations. An alternative explanation is that surviving small individuals that had experienced a malformation completely regenerated over successive molts is belied by the lack of small molts showing evidence of malformations. For some datasets, it is possible that these patterns reflect sample bias. However, the Elrathia kingii dataset considered here represents an unbiased, bulk collection where all observed specimens were collected in the field from a 1.5 m section (n >450 specimens with over 200 articulated specimens). In this dataset, no meraspid specimens show malformations. Further, the proportion of specimens with malformations is 1.7% of the examined articulated specimens examined. While detailed, collectionwide consideration is needed to generalize beyond this species, it does indeed seem that the lack of minute specimens with injuries is a biological record.
Ichnospecies Consideration
Predation traces have recently been defined as ichnospecies for brachiopods, with a broader application to shelled prey (Nicol and Leighton, 2023). This raises the question of whether ichnospecies should be presented for injuries to arthropods. In principle, there is taxonomic and likely paleoecological use in applying this same system. However, injuries can be expressed distinctly in different exoskeletal regions (Owen, 1985). Additionally, trilobites recovered from injuries during subsequent molts (Pates et al., 2017). Categorizing the trace fossils consistently is therefore complicated by injury recovery, as the morphology and extent of injury expression changes across molts. This situation contrasts with how mollusks preserve injuries as the shell grows. We have therefore opted to leave the documented injuries in a more open nomenclature.
TABLE 9.
Summary of malformation patterns presented in tables 2,3, 5–8. Species in bold are considered further in the text.
ACKNOWLEDGMENTS
This research was funded by an MAT Program Postdoctoral Fellowship (to R.D.C.B). We would like to thank Bushra Hussaini (AMNH) and Hilary Ketchum (AMNH) for help with collections. We thank Nicolas Campione for discussions regarding binomial testing. Finally, we thank Loren Babcock and Olev Vinn for their constructive feedback that has improved the scope and direction of the manuscript.
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