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Preservation of the gastrointestinal system in Olenoides (Trilobita) from the Kaili Biota () of Guizhou, China

JIH-PAI LIN

LIN, J.-P., 2007:09:03. Preservation of the gastrointestinal system in Olenoides (Trilobita) from the Kaili Biota (Cambrian) of Guizhou, China. Memoirs of the Association of Australasian Palaeontologists 33, 179-189. ISSN 0810-8889.

A specimen of the Olenoides from the middle Cambrian Kaili Biota was found to contain extensive dark stains. Spectral analyses show that the stains contain the elements C, P, S, Ca and Fe. These are elements that commonly form minerals associated with microbial decay of organic matter. The dark stains are interpreted to be remnants of the alimentary tract. Distinctive organs include a stomach region in the cephalon and a post-stomach alimentary canal extending through the thoracic axis to the pygidial terminus. This fossil demonstrates that trilobite gut traces could survive exoskeletal dissolution processes in fine-grained siliciclastic settings. Organic preservation of nonbiomineralised organs of may be more common in similar settings. Based on the information on body size, appendage morphology, and gut contents inferred from the Kaili and specimens, Olenoides was a heterotroph that could feed on either entirely soft-bodied invertebrates or organic remains, or both, depending on the availability of food sources.

J.-P. Lin ([email protected]), School of Earth Sciences, 125 South Oval Mall, Ohio State University, Columbus, OH 43210 USA. Received 22 June 2007.

Keywords: trilobite taphonomy, colour markings, digestive system, feeding, cuticle diagenesis, .

SKELETAL remains of trilobites are abundant and Lin (2006) described the taphonomy of Kaili in Palaeozoic rocks, but preserved soft parts are naraoiids and reviewed Cambrian and rare (see Babcock 2003; and references therein). trilobite gut preservation in the literature. Based Specimens studied here were collected from the on exceptionally preserved material from the Kaili Kaili Formation of Guizhou, China, and the unit Biota and other important Burgess Shale-type contains abundant trilobite faunas throughout deposits, Lin et al. (2006a) described unusual its entire thickness, with >100 described internal organs and important morphologic (Yuan et al. 2002). The Kaili also contains one characters of Skania and closely related species of the earliest middle Cambrian Burgess Shale- that have possible roots. On the type deposits, sharing many faunal elements (see other hand, although Kaili also contains abundant http://hdl.handle.net/1811/24227) with the older specimens of large bivalved (e.g., Chengjiang Biota (Chen 2004; Hou et al. 2004) Tuzoia), there is no soft-part preservation reported and the younger Burgess Shale Biota (Briggs et al. from Kaili material (see Vannier et al. 2007). 1994). The biota, facies description, and regional Kaili trilobites have been well documented for stratigraphy of the Kaili Biota were discussed and biostratigraphic correlation since the 1960s (Lu reviewed in Zhao et al. (2002, 2005) and Lin et 1963; Yuan & Zhao 1999; Peng & Babcock 2001; al. (2005). Zhao et al. 2001; Yuan et al. 2001, 2002), but the Chinese colleagues (Zhao et al. 1994b, 1996, cuticle diagenesis of Kaili trilobites has not been 1999, 2001, 2002) have illustrated many Kaili studied in detail (see Lin et al. 2006b, fig. 1C). The arthropods with soft-part preservation, but material studied here consists of three trilobites, most of their systematic descriptions are yet including two specimens of Olenoides paraptus to be completed. Recently, Zhao et al. (2003) Zhao, Ahlberg & Yuan, 1994 and one ptychopariid reported the appendages of Marrella. Zhu et trilobite, which have dark axial markings. One al. (2004) reported the gut glands and the gut specimen was illustrated previously (Zhao et al. contents filled with trilobite fragments of a large 2005, pl. 3, fig. 3), and two additional specimens nonbiomineralising arthropod. Lin & Zhao (2005) were discovered during reexamination of museum 180 AAP Memoir 33 (2007)

Fig. 1. Olenoides paraptus Zhao, Ahlberg & Yuan, 1994 from the Kaili Formation (Cambrian), Guizhou Province, South China. A, specimen with dark markings; OSU 50492, immersed in a hand sanitiser containing 62% ethyl alcohol before photography. B, enlarged view of the cephalon (indicated by a rectangle in A) showing patches of condensed organic matter; backscattered electron image. C, enlarged view of condensed organic matter (indicated by a rectangle in B) containing polygonal cracks and clusters of pyrite framboids (white spots); backscattered electron image. D, spectral analysis of the dark organic stains (indicated as a square in C) containing calcium phosphate. E, spectral analysis of the trilobite mould (indicated as a square in B) containing iron oxides (e.g., limonite) but lacking calcium and phosphorus. See text for further discussion. Scale bars = 20 mm (A); 1 mm (B); 60 µm (C). AAP Memoir 33 (2007) 181 collections. Results from compositional analyses under SEM were conducted at the Microscopic on the dark axial markings on one of these fossils and Chemical Analysis Research Center of The are presented herein. Ohio State University (Columbus, USA). The specimen was later photographed using a 105 PRESERVATION OF KAILI TRILOBITES mm f/2.8D AF Micro-Nikkor lens attached to a Trilobites are common in the shales and silty Nikon D100 digital camera. The specimen was shales throughout the Kaili Formation at several wetted with Purell Instant Sanitizer containing localities (Yuan et al. 2002; Lin et al. 2005). They 62% ethyl alcohol immediately before digital can be preserved with some relief in fine-grained photography to highlight contrasts between the siliciclastic settings, but the original calcareous dark stains and the matrix. cuticle is typically lost during diagenesis. Trilobite exoskeletons were generally composed RESULTS entirely of low-Mg calcite (Dalingwater 1973; Dark markings Wilmot & Fallick 1989; Dalingwater et al. Observed colour markings on Kaili trilobites are 1993, 1999; Fortey & Owens 1999a), although preserved on internal moulds (Fig. 1A). Under there are exceptions which have a phosphatic SEM (Fig. 1B-C), the dark markings consist of outer layer (e.g., Ellipsocephalus polytomus and organic matter with polygonal cracks and pyrite Calymene cf. C. beyeri; Teigler & Towe 1975; framboids (individual framboids are up to 2 µm Dalingwater et al. 1991). Most biomineralising in size; pyrite clusters are up to 6 µm in size). No organisms in the Kaili Biota, such as trilobites, distinctive sedimentary particles are observed articulated brachiopods (Huang et al. 1994), within the dark markings (Fig. 1C). EDS analyses and monoplacophorans (Mao & Zhao 1994; show that the dark regions are dominated by Zhao et al. 2002), are preserved as moulds. A the elements C, P, S, Ca and Fe (Fig. 1D). This few echinoderms, which have skeletons of low- is consistent with the composition of decayed Mg to high-Mg calcite (Dickson 2001), have organic matter based on actualistic taphonomic retained their calcareous plates with stereomic experiments (Allison 1988; Allison & Briggs microstructures (Lin et al. in press). 1991a, b; Briggs & Kear 1994; Briggs 2003). In addition, well preserved Kaili trilobite The trilobite internal mould is now composed of specimens often have a calcareous crust between clay minerals with iron oxides (Figs 1E, 2D). The part and counterpart. The calcareous crusts have dark markings appear to be composed principally better impressions of the trilobite body outline of organic carbon with minerals derived from than either part or counterpart (e.g., Zhao et al. microbial decay, including calcite, apatite and 2005, pl. 3, fig. 1). The crusts are undoubtedly pyrite (Briggs & Wilby 1996; Borkow & Babcock composed of secondary calcite because they 2003). Similar organic preservation occurs on extend beyond the fossil margins. Naraoia material from the same deposit (Lin However, apparently there was insufficient 2006). calcite in the Kaili sediment so that the secondary calcite did not accrete to form calcite nodules Remnants of the calcareous exoskeleton nucleated around the trilobites, such as the trilobite In addition to the dark markings along the axis, nodules from the late Cambrian (Furongian) several thoracic segments bearing a peculiar Wujiajiania sutherlandi Fauna near Tanglefoot pattern are visible in BSE images (Fig. 2A-B). The Creek, British Columbia (Chatterton & Ludvigsen pattern is a mosaic of dark-coloured patches on a 1998). generally lighter-coloured background. Some of the more regular light-coloured areas surrounded MATERIAL AND METHODS by the dark-coloured patches are approximately The trilobite specimen subjected to compositional 100 µm in size and the narrow portion of the analysis was selected from the Kaili collections at surrounding dark-coloured patches is at least the Guizhou University of Technology (GUT), now 38 µm in width. Spectral analyses indicate that a branch campus of Guizhou University, Guiyang, the dark-coloured patches contain calcium (Fig. China. The fossil is now deposited in the Orton 2C) and the light-coloured background does not Geological Museum of Ohio State University (Fig. 2D). The geometry and composition of the (OSU), Columbus, Ohio, USA. The specimen was mosaic pattern is here interpreted as remnants of uncoated but wrapped with aluminium foil (see the trilobite’s calcareous exoskeleton, which has Skinner 2005) for scanning electron microscopy survived diagenesis and dissolution from intense (SEM). Backscattered electron (BSE) images of weathering in a humid climate (cf. preserved the uncoated specimen were taken using a JEOL Kaili echinoderm plates in Lin et al. in press). JSM-820 SEM. A total of 11 elemental analyses The mosaic pattern resembles the geometry of using energy-dispersive spectrometry (EDS) the cavity-bearing, laminated, outer layer of 182 AAP Memoir 33 (2007)

Fig. 2. Backscattered electron photomicrographs of the O. paraptus mould from the Kaili Formation (Cambrian) with traces of calcareous cuticles; OSU 50492. A, enlarged view of the thoracic segments. B, enlarged view of the mosaic pattern with dark- and light- coloured regions on the pleurae. C, spectral analysis of a dark-coloured area (indicated by the white arrow in B) containing the calcium peak. D, spectral analysis of the light-coloured background (indicated by the black arrow in B) lacking the calcium peak. Scale bars = 2 mm (A); 1 mm (B).

Calymene cuticle (Dalingwater et al. 1993, pl. in several fossil marine invertebrates, including 9, figs 1-2) or Osmólska cavities (Størmer 1980, trilobites. In trilobites, some of these have been text-fig. 3; McAllister & Brand 1989, fig. 4A-D), interpreted as relics of original pigments, while which are tiny cavities connected to canals within others are considered to be organic stains derived the cuticle (Whittington & Wilmot 1997, p. 77). from muscle attachment sites on the exoskeleton, depending on the position, regularity, pattern, POSSIBLE ORIGINS OF COLOUR and size of the colour markings (see Whittington PATTERNS IN TRILOBITES 1997; Fortey & Owens 1999a). Shu et al. (1995) Colour markings (e.g., Kobluk & Mapes 1989; proposed a third origin by interpreting the Hollingsworth & Barker 1991) have been reported paired dark markings preserved on a number AAP Memoir 33 (2007) 183 of specimens of Eoredlichia intermedia as gut On the other hand, Whittington (1975, 1980) glands because the positions of the dark markings reexamined museum collections and also collected vary among specimens and those markings never additional material of the Cambrian Burgess overlap with the pairs of the supposed muscle Shale trilobites with exceptionally preserved scars. appendages, including Olenoides serratus This study indicates a fourth possible origin; and burgessensis, first described by that the dark markings are relict remains of an Walcott (1911, 1912). Whittington (1975, 1980) alimentary canal. Unlike muscle attachment sites compared O. serratus with the marine chelicerate preserved as paired dark stains (e.g., Harrington Limulus and interpreted that O. serratus was 1959, figs 69-70; Šnajdr 1990, p. 71; Whittington a predator/scavenger based on appendage 1992, pl. 9; Rudolph 1994, taf. 33; Gutiérrez- morphology. Although he was familiar with Marco & Bernárdez 2003, p. 216) or paired the earlier studies emphasising filter-feeding in midgut diverticula (Chatterton et al. 1994, figs trilobites (see Bergström 1969; and references 1-5; Shu et al. 1995, figs. 14-15, pl. 1, fig. 8), the therein), Whittington (1975, p. 134) stated that preserved alimentary tract is mostly tubular on the “I have preferred to emphasize the function of axis (e.g., Brett et al. 1999, fig. 8-5; Whiteley et the gnathobases and ventral spines of the leg al. 2002, fig. 2.12C, pl. 78). branches of O. serratus in food catching and transport along the midline, and to regard the TRILOBITE ALIMENTARY TRACTS outer braches as primarily used in respiration AND INFERRED TRILOBITE TROPHIC and swimming.” With additional material, STYLES including newly moulted specimens, Whittington Previous studies (1980) provided a revised model focusing on the Chatterton et al. (1994), Babcock (2003) and Lin maneouvreability of appendages and reinforced (2006) reviewed and discussed previous studies his predator/scavenger interpretation for O. on various aspects of soft-part preservation serratus. Furthermore, Whittington & Almond in trilobites and closely related arthropods. (1987) studied Walcott’s specimens of T. eatoni Important studies that are critical to understanding and revised Cisne’s interpretations considerably the anatomy and feeding habit of Olenoides based on some carefully prepared specimens with are reviewed herein. Thus, although Müller & fully exposed appendages. Based on the new Walossek (1987) reported exceptionally preserved reconstruction, Whittington & Almond (1987, Agnostus pisiformis with phosphatised soft parts, p. 42) concluded that “T. eatoni, while able to the feeding habit of agnostid trilobites is not trap particles in suspension, was predominantly discussed. a benthic deposit feeder, scavenger and predator, Modern debate on trilobite digestive tracts that dug into the mud using particularly the and/or feeding mechanisms began in the 1970s. larger anterior and middle thoracic leg branches Stürmer & Bergström (1973) used X-rays to reveal in search of food.” They also noted that T. eatoni trilobite soft-part preservation. Cisne (1975, 1981) is distinctly different from O. serratus in having restudied the pyritised a large number of pygidial appendages that eatoni, first reported by Beecher (1893), with an diminish rapidly in size toward the terminus enhanced X-ray imaging method. He compared and in lacking posterior cerci. Based on such T. eatoni with marine , including differences, Whittington & Almond (1987, p. cephalocarids, branchiopods and phyllocarids, 43) interpreted Olenoides, along with other large and concluded that T. eatoni had a relative small arthropods in the same deposit as being more mouth and a narrow oesophagus connected to specialised as benthic scavengers/predators. an anus and could only feed on particulate food They also observed that Triarthrus, Phacops, material such as deposited detritus (see Cisne Rhenops and Cryptolithus collectively have 1975, p. 52-54; 1981, p. 124-127). Cisne (1981, posterior appendages arranged in a way similar p. 126) stated that “the only direct fossil evidence to those of Marrella (see Briggs & Whittington of the food [for T. eatoni] are clouds of finely 1985) and suggested these arthropods have more particulate, pyritic material emanating from the generalised trophic styles, including suspension gut, probably gut contents squeezed from the body filter feeding, detritus deposit feeding, scavenging by post-mortem compression...This is consistent and capturing prey. with the deduction from anatomy. Individual Chatterton et al. (1994) regarded the paired particles in the clouds are very small, irregular, structures preserved on several specimens and otherwise not readily identifiable. Such of the trilobite Pterocephalia from British material is commonly seen in the body cavities Columbia as paired diverticula and suggested of specimens, though its origin is not so clear as that Pterocephalia, Olenoides and the nektaspid in the cases mentioned above.” arthropod Naraoia had similar digestive systems. 184 AAP Memoir 33 (2007)

They inferred the presence of detrital minerals in the Pterocephalia digestive system as evidence for deposit feeding behaviour. Babcock (2003) and Babcock & Peel (in press) reported that some trilobites are preserved with mud-free and sclerite-free alimentary tracts, and interpreted large trilobites, such as Isotelus, Buenellus and Chotecops, as predators that fed on soft-bodied invertebrates. In addition, Babcock (2003) provided ample trace fossil evidence, including Rusophycus-type arthropod resting traces intersecting with Planolites-type worm burrows reported by Jensen (1990), to further support their hypotheses. On the other hand, apparently mud-filled guts in some nonbiomineralising arthropods such as naraoiids have traditionally been considered as direct evidence for a deposit-feeding trophic style (e.g., Chen et al. 1997; Hou & Bergström 1997; Edgecombe & Ramsköld 1999; Bergström 2001; Chen 2004; Hou et al. 2004). Butterfield (2002) demonstrated subcellular features preserved in the alimentary system of Leanchoilia superlata (see García-Bellido & Collins 2007) and suggested Fig. 3. Interpretive drawing of the dark markings some arthropods from the Burgess Shale, preserved on O. paraptus (OSU 50492; Fig. 1A); including Odaraia, Canadaspis, Perspicaris, scale bar = 10 mm. Sidneyia, and Opabinia were predators/scavengers with midgut glands types of trilobite digestive systems identified similar to modern chelicerates. Vannier & by Chatterton et al. (1994) may be the result of Chen (2002) interpreted Cambrian naraoiids as incomplete preservation of trilobite soft-parts in epibenthic scavengers/predators based on modern the fossil record. analogues. However, Lin (2006) studied the In order to interpret Pterocephalia as a taphonomy of Kaili naraoiids and suggested that deposit feeder, more detailed examination of a three-dimensionally preserved alimentary tract preserved gut contents is required because the surrounded by a flattened carapace indicates the detrital minerals (mainly indicated by the Si, existence of a taphonomic phase – the selective, Al, K and Na; Chatterton et al. 1994) could syndiagenetic, anaerobic microbial decay on originate either from contamination during internal organs, and does not necessarily imply sample preparation (at least for Na based on the a deposit-feeding habit. The study by Butterfield presence of Cl; Chatterton et al. 1994, p. 296) or et al. (2007, p. 537) showed that the three- from the rock matrix that is mainly calcareous dimensionally preserved gut-caecal system of mudstone (Chatterton & Ludvigsen 1998, p. 1). Burgessia from the Burgess Shale had resulted The latter is the cause for Mg, Si, and Al signals from a late diagenetic aluminosilicate replacement in the Olenoides gut (Fig. 1D) because the Kaili of a pre-existing carbonate phase. specimen was analyzed at 15keV, which is a relatively high accelerating voltage allowing Pterocephalia gut and feeding habit backscattered electrons to penetrate relatively After reviewing the evidence presented by wider and deeper beyond the target surface, the Chatterton et al. (1994), the paired structures SEM therefore picking up ‘noise’ from the rock in Pterocephalia are considered to be traces of matrix immediately around and beneath the target trilobite internal organs (possible gut glands) area. Orr (2002) had applied a similar principle in based on the concurrence of C, Ca, P and Fe. imaging organic structures of fossil arthropods in However, judging from relatively better preserved the shallow subsurface. trilobites, including Eoredlichia intermedia and Kuanyangia (Sapushania) bella, from the Olenoides gut and feeding habit Chengjiang Biota (Shu et al. 1995, figs 14-15, The preserved digestive tract of Olenoides pl. 1, fig. 8; Chen et al. 1996, p. 71-72, fig. 189; paraptus includes a stomach region in the glabella Chen & Zhou 1997, fig. 65; Chen 2004, fig. and a post-stomach alimentary canal in the 433; Hou et al. 2004, fig. 16.44a), the different post-cephalic axis (Fig. 3). There are transverse AAP Memoir 33 (2007) 185 elements (perhaps the same metameric features thus, Olenoides is unlikely to be a mud-eater. as in O. serratus; Whittington 1980, text-fig. However, there are diverse feeding mechanisms 4, pl. 19) either connected to, or superimposed among marine arthropods (e.g., Russell-Hunter on the alimentary canal (Fig. 3), but no paired 1979, pp. 245-247; Levinton 1982, pp. 269-291; organic features in the post-cephalic axis can be Brusca & Brusca 1990, pp. 595-666). Based identified based on the optical and SEM images on modern analogues, several trophic styles, (Figs 1A, 2A). The alimentary canal is not including suspension filter feeding of particulate perfectly centered and slightly off to the right of organic matter, grazing on microbial/algal growth, the sagittal line. Kaili trilobites in general are not or predation/scavenging on entirely soft-bodied as well preserved as Burgess Shale specimens due organisms and/or organic remains, would result to different burial conditions (Caron & Jackson in both mud-free and sclerite-free gut contents. 2006) and fossilisation processes (Butterfield et Judging from abundant trilobite occurrences al. 2007), but even the best preserved O. serratus in early Palaeozoic marine strata worldwide, specimen (Whittington 1980, text-fig. 4, pl. 19) generalised feeding habits with multiple feeding contains a displaced alimentary tract. However, mechanisms are the primitive conditions for the alimentary canal of the Kaili specimen is most trilobites (see Fortey & Owens 1999b). relatively more even in diameter while the Based on soft-part anatomy and appendage Burgess Shale material exhibits an alimentary morphology obtained from the Kaili and Burgess tract that tapers posteriorly. Such a discrepancy Shale material, Olenoides was predominately a is probably due to the difference in taphonomic scavenger/predator (Whittington 1975, 1980). history rather than the anatomical difference between the two species. CONCLUDING REMARKS On the other hand, Yuan et al. (2002, pl. 13, fig. Unlike previous interpretations of trilobite colour 3) figured one specimen of O. paraptus from Kaili markings mentioned above, the dark markings containing at least three pairs of dark stains in the present on the Kaili trilobite Olenoides paraptus glabella. Its pattern is different from the stomach are interpreted as traces of the alimentary tract region described here (Fig. 3) and the spacing that stained the internal mould during diagenesis. between the paired structures is too narrow to be The organic preservation includes an outline of a the supposed muscle stains. Thus, those paired stomach region in the glabella and an alimentary dark markings in the glabella of O. paraptus are canal in the axis. Soft part preservation indicates interpreted here as remains of paired diverticula that the studied specimen of Olenoides is a or gut glands (e.g., Chatterton et al. 1994, figs 1-3, carcass, not a moult (see Chatterton et al. 1994; 4-4, 4-3; Shu et al. 1995, figs 14, 15A-B). Lin 2006). Chatterton et al. (1994, pp. 295-296) interpreted The study also indicates that Olenoides has the short lateral evaginations connected to the an alimentary tract that is both mud-free and alimentary canal in the Burgess Shale specimen sclerite-free (Fig. 1A-D). Based on Whittington’s of Olenoides as probably homologous to the (1975, 1980) studies, the spines on the Olenoides paired structures preserved in Pterocephalia. As walking appendages would help to capture soft mentioned above, similar metameric features are bodied organisms and the spinose gnathobases present in the Kaili specimen. However, when the would be useful for immobilising and/or crushing alimentary canal is preserved, the paired axial prey. Thus, Olenoides was predominately a markings (either muscle stains or gut glands) scavenger/predator that fed entirely on soft- are usually not visible (Fig. 3), and vice versa bodied organisms. It is possible that Olenoides (Yuan et al. 2002, pl. 13, fig. 3). Chatterton et al. had other feeding mechanisms, but it can not (1994) also showed a number of Pterocephalia have been a mud-eater due to a lack of identifiable specimens exhibit a similar preference in soft-part sedimentary particles in the alimentary tract in preservation. Whether such selective preservation both Kaili and Burgess Shale specimens. of organic markings indicates a taphonomic bias or an anatomical difference (e.g., different ACKNOWLEDGEMENTS organs) is uncertain. Therefore, the homology This contribution is part of the author’s doctoral between the lateral evaginations in Olenoides dissertation at The Ohio State University, and the paired structures in Pterocephalia cannot Columbus. Many thanks to W. I. Ausich and J. St. be confirmed. John for improving the English and J. R. Paterson Is Olenoides a deposit feeder (Chatterton et al. for technical and editorial support. This project was 1994), or a scavenger/predator (Whittington 1975, funded by an Ohio State University Presidential 1980)? This study shows that the gut content Fellowship, an International Dissertation/MA of Kaili Olenoides under high magnification Thesis Research Travel Grant, Alumni Grants for (up to 70X) (Fig. 1C) is clearly sediment-free; Graduate Research and Scholarship, Geological 186 AAP Memoir 33 (2007)

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