Phosphatized coprolites from the middle Cambrian (Stage 5) Duyun fauna of China

    Phosphatized coprolites from the middle Cambrian (Stage 5) Duyun fauna of China Cen Shen, Brian R. Pratt, Xi-guang Zhang PII: DOI: Reference:

S0031-0182(14)00291-0 doi: 10.1016/j.palaeo.2014.05.035 PALAEO 6884

To appear in:

Palaeogeography, Palaeoclimatology, Palaeoecology

Received date: Revised date: Accepted date:

31 October 2013 25 May 2014 27 May 2014

Please cite this article as: Shen, Cen, Pratt, Brian R., Zhang, Xi-guang, Phosphatized coprolites from the middle Cambrian (Stage 5) Duyun fauna of China, Palaeogeography, Palaeoclimatology, Palaeoecology (2014), doi: 10.1016/j.palaeo.2014.05.035

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ACCEPTED MANUSCRIPT Phosphatized coprolites from the middle Cambrian

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Cen Shen a,b, Brian R. Pratt c, Xi-guang Zhang a*

Key Laboratory for Palaeobiology, Yunnan University, Kunming, Yunnan 650091,

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China.

Faculty of Land Resources Engineering, Kunming University of Science and

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(Stage 5) Duyun fauna of China

Technology, Kunming, Yunnan 650091, China c

Department of Geological Sciences, University of Saskatchewan, Saskatoon,

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Saskatchewan S7N 5E2, Canada

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Abstract

Minute phosphatized coprolites have been recovered from the middle Cambrian (Stage 5) Gaotai Formation in Duyun, Guizhou, southern China. They occur as

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ellipsoidal, rod-like and coiled or sinusoidal objects that can be classified into four morphotypes. Three of these consist of finely crystalline (‘amorphous’) apatite that replaced digested organic matter and possibly muddy sediment, while a fourth is composed of bioclasts belonging to the prey animals of either palaeoscolecid dermal sclerites, bradoriid carapaces or lingulate brachiopod valves. Pellets occur in elongate clusters of up to about 100 ellipsoids. These clusters indicate that the producers’ digestive systems were able to compress ingested material into individual pellets which were then expelled en masse without being shaped by muscle contractions in the latter portion of the intestine and anus. On the other hand, rod-like faeces with irregular annular grooves 1

ACCEPTED MANUSCRIPT indicate a process of extrusion of digested material involving strong muscle contraction and compaction. Rods packed with sclerites and valves indicate that

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these hard parts are undigested organism fragments. Sinusoidal faeces point to

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ingestion of a great deal of material before extrusion, and possibly accompanied

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by movement of the anus-bearing posterior. The coiled morphotype suggests defecation of loosely compacted material from a long animal with a correspondingly long gut. Pellet clusters were produced either by a suspension

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feeder or a deposit feeder. Two or more types of invertebrates consumed organic

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matter and possibly lime mud, probably as deposit-feeders, while at least one other preyed upon worms, bradoriids and/or brachiopods. The different shapes

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and contents of these uniquely preserved coprolites confirm that the middle

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Cambrian benthic community exhibited a complex trophic structure involving a wide array of nutritional behaviours, including predator–prey and scavenger

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cycles.

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relationships, possibly along with prey selectivity in the context of prey life

Keywords: coprolites, paleoecology, phosphatization, Middle Cambrian, China

1. Introduction Fossil coprolites as faecal pellets, faecal strings and extruded bodies left by ancient animals have long been known as a distinct category of trace fossils. Although many invertebrate coprolites exhibit their own specific morphology, most lack distinguishing characteristics that allow the identity of the producer to be determined (e.g., Kraeuter and Haven, 1970). Because of disaggregation on the seafloor, scavenging, compaction and diagenesis, there is little chance for them to be preserved

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ACCEPTED MANUSCRIPT together with their producers. Thus it is only under exceptional circumstances that fossil coprolites can survive taphonomic barriers. Because they are directly related to

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trophic activities of their producers, coprolites offer nonetheless useful information

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about the environment and ecology where they formed, as well as the palaeobiology

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of the producer, including the role of predation (Edwards et al., 1995; Chin, 2002; Vannier and Chen, 2005; Aldridge et al., 2006). Sometimes organism remains are visible in coprolites (Scott, 1977; Chin et al., 1998; Northwood, 2005; Wedmann and

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Richter 2007; Zatoń and Rakociński, 2014), and their identity along with the coprolite

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morphology can be used for inferring the likely producers (Eriksson et al., 2011; Edwards et al., 2012; Izumi, 2013). Faecal pellets may act as a proxy for deducing

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important factors such as water-column productivity (Kiel, 2008). It is well known

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that much fine-grained sediment in modern shallow seas consists actually of faecal or pseudo-faecal pellets which behave hydraulically as silt and fine sand.

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Fragments of animal skeletons and shells found as gut contents, such as that of arthropods (Zhu et al., 2004), hyolithid conchs with or without the operculum

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attached, and articulated brachiopod valves (Vannier, 2012), or faecal pellets within trace fossils left by unknown burrowing animals (Zhang et al., 2007), are regarded as documenting in situ feeding strategies. Cambrian coprolites or faecal pellets have been observed isolated in the sediment matrix, and examples consist of monospecific aggregates of densely packed bradoriid carapaces or hyolithid conchs (Chen, 2004), or phosphatocopine carapaces (Eriksson and Terfelt, 2007). Possible faecal pellets have also been reported from the Cambrian Series 2, Stage 3 (provisional; formerly upper Lower Cambrian), which are seen as aggregates of densely accumulated hyolithid conchs or bradoriid carapaces along with some trilobite and waptiid sclerites (Vannier and Chen, 2005). From the same time interval, spheroidal particles

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ACCEPTED MANUSCRIPT consisting of compressed and cracked palaeoscolecid cuticles and small phosphatocopine carapaces are likely feacal (Zhang and Pratt, 2008) which are in

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contrast to the flat or slightly curved bioclasts of the same taxa which are also

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recovered from the same limestone bed. Faecal pellets preserved underneath trilobite

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exoskeletons appear as randomly distributed aggregates or burrow fills (Bruthansová and Kraft, 2003). Such cases may be related to a specialized but not yet fully understood feeding strategy of an unknown animal inhabiting these sites, or due to a

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preservational bias granted by the exoskeletons.

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In general, however, fossilized faeces present an under-exploited palaeontological resource. In this paper we describe various kinds of faecal matter that have been

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replicated by amorphous apatite from the Cambrian Series 3, Stage 5 (formerly the

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Middle Cambrian) of southern China. The striking degree of preservation by synsedimentary phosphatization adds a new dimension to the understanding of the

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palaeoecological attributes of these marine limestones.

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2. Geological setting

The middle Cambrian (Stage 5) Gaotai Formation varies greatly in thickness (2–45 m) in central Guizhou, and consists mainly of thin- to medium-bedded, locally sandy and/or silty dolomite, shale and siltstone (Yin, 1996). It overlies thin beds of oolitic limestone of the uppermost Qingxudong Formation (Cambrian Stage 4). Numerous trilobite taxa have been reported from the succession exposed near Balang village in Duyun (Chien, 1961), and the basal beds yield many exoskeletons of the eodiscoid Pagetides qianensis Zhang and Clarkson, 2012. As key index fossils these trilobites verify the age of the fossil assemblage. 4

ACCEPTED MANUSCRIPT Near the base of the formation by Balang village (34°11'5"N, 139°52'12"E), there are two horizons of light-grey or yellowish limestone nodules separated by 1.2 m of

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shale and thin-bedded dolomite that have yielded phosphatized fossils (Fig. 1). The

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coprolites examined herein, as well as numerous previously described bradoriids and eodiscoids (Zhang, 2007; Zhang and Clarkson, 2012), and rare scalidophoran embryos and chitinozoans (Zhang et al., 2011; Shen et al., 2013a) were all collected

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from the upper horizon. Recently, with continued excavation, the upper horizon of

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limestone nodules was revealed to be not thin-bedded but a large, lenticular, concretionary limestone body up to 0.45 m thick, with a diameter about 1.2 m. Within

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separated by shale laminae.

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the lens there are several layers of light-grey or yellow fossiliferous limestone nodules

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The Gaotai and Qingxudong formations were deposited predominantly in an overall shallow-marine setting, but the nodular and shaly aspect of the strata

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containing the phosphatized fauna suggests a somewhat deeper water, low-energy depositional environment for the fossiliferous interval.

3. Material and Methods Some 600 kg of the limestone nodules were digested in dilute (4–5%) acetic acid, essentially following the laboratory process essentially introduced by Müller (1985) and improved by Shen et al. (2013b). Phosphatized microfossils were then picked from the insoluble residue under a stereomicroscope. The biota includes numerous lingulate brachiopod valves and disarticulated eodiscoid trilobite exoskeletons, plus

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ACCEPTED MANUSCRIPT many bradoriid carapaces, sponge spicules, polymeroid trilobite exoskeletons, hyolithid conchs and opercula, various small shelly fossils of problematic affinities,

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rare scalidophoran embryos (Zhang et al., 2011) and chitinozoans (Shen et al., 2013a),

3A–I, 4A–J).

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along with faecal pellets (Fig. 2A–H) and various other coprolite forms (Figs. 2I–P,

All specimens dealt with in this study are housed in the Key Laboratory for

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Paleobiology, Yunnan University (YKLP).

4. Coprolite morphotypes

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Based on their external morphology, essential structure and internal contents, the

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coprolites can be referred to four morphotypes (Table 1). Three forms are composed

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of finely granular (‘amorphous’) apatite which is secondary after organic matter and/or lime mud. One form consists of bioclasts with variable amounts of finely

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granular apatite.

4.1 Muddy ellipsoids (Fig. 2A–H) Some 30 specimens are referred to this form and they consist of clusters of up to about 100 loosely packed pellets of a consistent prolate spheroid shape. These smaller pellets are 200–300 µm long and 80–120 µm wide; the length:width ratio is consistently 2.5. They are quite uniform in size in each cluster. Clusters range from a crudely ovate to a roughly cylindrical shape; cluster terminations narrow in the former but are blunter in the latter. Pellets exhibit a variable orientation; most are approximately parallel to the long axis of the cluster, with others oriented obliquely at

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ACCEPTED MANUSCRIPT various angles to it (Figs. 2A–D, 5A–D), including some roughly at right angles to it (Figs. 2B–D, 5B–D). The surface of the pellets is smooth, and their interiors are

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composed of dense amorphous apatite without recognizable structure or contents.

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Some clusters are composed of larger pellets in the form of two to half a dozen or so individual cylinders oriented subparallel to the long axis (Fig. 2E, F). In two specimens the largest pellets are about 1 mm long and 0.2 mm in diameter (Fig. 2G,

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H).

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4.2 Muddy strings (Fig. 2I–K)

Three specimens formed curved strings, one tightly meandering within the same plane

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and taking a sinusoidal shape (Fig. 2J), and the other two spiraling

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three-dimensionally (Fig. 2I, K). The surface of the coiled ones is irregular and finely

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pitted, and the diameter is about 200–300 µm. The diameter of the sinusoidal coprolite varies from about 200 to 350 µm and is widest in the middle. Its outer

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surface bears many striae that are oriented oblique to transverse, i.e., 45–90°, to the long axis. These are more or less straight and are variably continuous around the cylindrical coprolite. 4.3 Muddy rods (Fig. 2L–P) The 12 specimens referred to this form display a greater variation in morphology and outline, and each is relatively large, with a length range of 0.8–2.1 mm, and a diameter range of 0.3–0.4 mm, and having a more or less straight cylindrical shape. The surface is smooth, but many have indistinct, shallow concentric grooves whose spacing ranges from variable to fairly regular. No bioclastic debris is present within.

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ACCEPTED MANUSCRIPT 4.4 Bioclastic rods (Figs. 3A–I, 4A–J) Fourteen specimens are characterized by consisting of tightly packed bioclasts, either

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palaeoscolecid worm dermal sclerites (Fig. 3A–F), bradoriid carapaces (Fig. 3G–I), or

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lingulate brachiopod valves (Fig. 4A–J). Worm sclerites, bradoriid carapaces and lingulate valves are not found together, however. Each of these coprolites is a straight to curving cylindrical cluster 1.2–2.0 mm in length and 0.4–0.8 mm in diameter.

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Button-shaped sclerites are variable in size, and mostly oriented parallel to the

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coprolite exterior, facing both in and out (Fig. 3A–C, F). The pattern of protuberances suggests the sclerites seem to belong to a single palaeoscolecid species and the size

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range probably reflects the different ranks of sclerites (cf. Ivantsov and Wrona, 2004);

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isolated palaeoscolecid cuticles may be present as flat pieces in Cambrian

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phosphatized fossil assemblages (Fig. 3L, M), but do not occur within the Duyun fossil assemblage. Like the pellets consisting of worm cuticles reported elsewhere

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(Zhang and Pratt, 2008), the bradoriid carapaces were compressed into cylindrical clusters (Fig. 3G, H); when not in faecal pellets carapaces of the same taxon are present as either articulated (Fig. 3J) or isolated valves. For the brachiopod-bearing coprolites, many valves are still articulated; a few display broken and worn shells preserved as isolated valves (Fig. 4E). In individual cylinders valves are uniform in size, within 75% of each other (Fig. 4C, F, I). Some articulated valves are juvenile forms (Fig. 4G). At least two taxa seem to be present, one a simple lingulate with concentric growth lines (Fig. 4A, F, K, L), while the other, a botsfordiid, has a pitted shell with a pair of large conical protuberances (Fig. 4I, J, M).

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5. Interpretation

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Here we identify these fossils as coprolites instead of an inorganic sedimentary

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feature based primarily on a number of observations: 1) most of them have an elongated shape with rounded or pointed terminations, which was more likely produced inside the guts of predators, scavengers or deposit-feeders, than made by

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purely inorganically means such as passive infilling of a burrow; 2) the orientation of

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the ellipsoidal pellets in each cluster is largely parallel to the long axis of the cluster, although there is some variation especially with pellets at right angles, which is

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reasonably explained by the cluster having passed through the gut whose long axis is

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parallel to the body; 3) the bioclastic rods consisting of compacted worm sclerites,

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bradoriid carapaces or brachiopod valves belonging to the same taxon possibly indicate prey selectivity; and 4) in the case of the worm sclerites, they are densely

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packed and thus are unlikely to be simple an exuviation. Because isolated bioclasts belonging to the same taxa are abundant in the Duyun fauna and approximately the same size, purely inorganic accumulations would likely be mixtures of these bioclasts. Pseudofaeces are produced by filter-feeding invertebrates when they reject suspended material; in the case of extant oysters and mussels they are loose aggregates bound by mucus, and they tend to disintegrate rapidly. Regurgitated material—‘regurgitites’ of Vannier and Chen (2005)—is usually diffuse, poorly formed and uncompressed. The well-formed, compressed nature of the objects described here argues against this possible origin.

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ACCEPTED MANUSCRIPT 5.1 Preservation, content and producers Without direct evidence assigning these coprolites to producers based on extant

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analogues is difficult in most cases. Members of large taxonomic groups can produce

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a wide variety of shapes of faecal pellets. The variation in size of the pellets in the clusters may be due to the variably sized producers representing different growth stages but belonging to the same taxon. Alternatively, the smaller pellets represent one

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producer while the larger pellets belong to another. Possibly some of the clusters with

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only a few pellets are due to incomplete preservation—larger clusters may have been broken into small pieces—this could have happened during or soon after excretion,

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but also during the sample preparation process.

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The isolated, more or less curved coprolites bearing indistinct annular grooves or

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shallow indentations may have been produced by a deposit-feeder, since no organism fragments have been observed inside these coprolites. The indistinct grooves probably

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represent peristaltic contractions involved in compressing the digested material near the end of the gut or muscle contractions as the faeces was extruded. The sinusoidal form could have been extruded by a worm, such as a deposit-feeding polychaete, for example, akin to Burgessochaeta Conway Morris, 1979, although the tightly arranged concentric striae are difficult to explain. Coiled forms can be produced by a variety of invertebrates including some tunicates (e.g., Kraeuter and Haven, 1970; Arakawa, 1971). The poor preservation of the single example may be an artefact of the apatite replacement or because the soft faecal matter was not compacted in the gut. Despite the limited number of specimens, the lingulate valves in the bioclastic

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ACCEPTED MANUSCRIPT rods appear to indicate size-sorting, with the mean size of valves varying from rod to rod. One interpretation for this size-related dietary difference may simply reflect the

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fact that as in extant predator-prey systems the sizes of targeted prey increased with

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increasing predator size (e.g. Palmer, 1988). All the same, the Duyun predators appear to have preyed upon only juvenile brachiopods and relatively small palaeoscolecids. By contrast, the Chengjiang and Kaili predators which appear to have been relatively

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larger in size consumed either large number of bradoriids or hyoliths (Chen, 2004) or

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eodiscoid holaspides, seemingly including fully grown trilobite instars (Zhu et al., 2004). Although the coprolites from Sweden, with their compressed circular outline,

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also contain small phosphatocopines, their average size is larger (Eriksson and Terfelt,

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2007). In general, prey size selectivity in the Duyun deposit was probably governed

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by the size of the mouth and diameter of the gut of the predator. In most cases the lingulate valves are still articulated which suggests that: 1) the

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predator swallowed each individual whole without crushing or disarticulating its valves; 2) the relative narrowness of the gut may have prevent disarticulation; or 3) it just represents the material still remaining in the gut of a carcass which was buried while it was in the process of digesting the brachiopods. Within some coprolites, however, the lingulate valves do appear to have been disarticulated and worn, and these may have been particles on the seafloor that were consumed inadvertently, although there are no elements of other admixed bioclasts belonging to other taxa. The detailed preservation of most valves indicates that the coprolite producers did not secrete the appropriate digestive enzymes, like chitinase, that would have broken

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ACCEPTED MANUSCRIPT down the chitin in the apatitic shells. On the other hand, the quantity necessary for the observed coprolites would have had to be considerable, plus allowed to act on the

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valves for probably an unrealistically lengthy period in order for them to be corroded.

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Hyolithid conchs with attached operculum and articulated brachiopod valves are present in some specimens of the priapulid Ottoia prolifica Walcott, 1911 from the Burgess Shale (Vannier, 2012). The gut diameter of O. prolifica ranges from 0.8 to 1.5

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mm, which is comparable to the size of the Duyun coprolites, and may be evidence

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that the Duyun producer was a priapulid worm.

The guts of specimens of O. prolifica contain various undigested invertebrate

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remains, suggesting these worms fed randomly at the sediment–water interface

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(Vannier et al., 2010; Vannier, 2012). Similarly, the monospecific bioclasts in the

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Duyun coprolites may merely reflect what was available at the particular time food was consumed.

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Similarly in the coprolites composed of palaeoscolecid fragments, all button-like sclerites were indigestible, either because they were thicker or partly biomineralized, such as by apatite. That some of these are connected by partially surviving cuticle suggests that it too was more resistant to digestion than the interior tissues. Taphonomic barriers aside, other elements of the biota in the Duyun fauna are not found in coprolites. For example, none consists of eodiscoid trilobites, even though phosphatized sclerotes are common in the limestones. Perhaps these arthropods were too agile to be captured, or spent most of their time above the sea floor and beyond reach. In other situations, however, eodiscoids did serve as a prey in the Cambrian

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ACCEPTED MANUSCRIPT ecosystem (Zhu et al., 2004). 5.2 Comparison to other examples.

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Relatively few examples in the fossil record are known of invertebrate coprolites

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that are well preserved by secondary mineralization, such as by apatite replacement. Muddy ellipsoids, rods and strings are filled with fine-grained material that consisted originally of either or both organic matter and lime mud. The bioclastic rods

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composed of packed brachiopod valves or worm cuticles are somewhat comparable to

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‘morphotype 7—rod-like coprolites’ of Eriksson et al. (2011)—but the latter are larger in size and contain either delicate fragments (Edwards et al., 2012) or no visible

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inclusions (Eriksson et al., 2011). By contrast, some of muddy coils may be

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comparable to ‘morphotype 5—amphipolar coprolites’ (Eriksson et al., 2011).

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However, the seven coprolite morphotypes described by Eriksson et al. (2011) are from the Cretaceous shallow marine strata and are related to a diverse vertebrate

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fauna, while those described by Edwards et al. (2012) are from a terrestrial setting of Devonian age. Thus, this shows that similar morphotypes are produced by a wide variety of animals. On the other hand, this also attests to some similarities in the manner of digestion and extrusion. An inevitable problem with faecal pellets is that it is usually impossible to identify their likely producers. Only in sporadic cases are specimens directed associated with the body fossils or trace fossils belonging to their producers, such as some occurrences of Tomaculum problematicum Groom, 1902 (e.g., Podhalańska, 2007; Weber et al., 2012). Commonly a wide range of possible producers can be entertained,

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ACCEPTED MANUSCRIPT and even in early Cambrian examples the co-existing fauna may be quite diverse, including some primitive chordates (e.g. Chen et al., 1995; Shu et al., 1999).

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Certain faecal pellets in the Ordovician of Bohemia, also assigned to Tomaculum

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problematicum are associated with particular body fossils and the sedimentary matrix around them (Bruthansová and Kraft, 2003). The variation in size and shape of these faecal pellets suggests that they came from different producers or from producers at

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different growth stages (Bruthansová and Kraft, 2003). Similarly the size ranges of

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the clusters of muddy ellipsoidal and rod-shaped coprolites reported here may indicate that they were excreted either by both juvenile and adult forms of a larger producer.

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On the other hand, the uniformity of the pellets in the large aggregates suggests more

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likely a different kind of animal. The lack of much larger coprolites may indicate the

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absence of a corresponding large producer, but it could also be due to a taphonomic bias. The latter possibility may be supported by the nature of the phosphatization

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process which seems to have permitted preservation of only small-sized carcasses and bioclasts.

The contents of faecal pellets are proof of what the animals consumed (e.g. Köster et al., 2011; Zatoń and Rakociński, 2014), and may provide evidence for evaluating the feeding strategy (Wedmann and Richter, 2007). The coprolites consisting solely of brachiopod valves, bradoriid carapaces or palaeoscolecid cuticles suggest that the Duyun predators either reacted to prey windfalls, or exhibited prey selectivity because they belong to different taxa. A wide array of predators is considered to have existed already in early and middle Cambrian time (e.g. Pratt, 1998; Budd, 2001; Vannier and

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ACCEPTED MANUSCRIPT Chen, 2005; Haug et al., 2011; Vannier, 2012), and selective predators are inferred to have existed in benthic communities such as those represented by the Kaili fauna

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(Zhu et al., 2004), the Chengjiang fauna (Chen, 2004) and middle Cambrian Alum

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Shale of Sweden (Eriksson and Terfelt, 2007).

Zooplankton faecal pellets are major components of ‘marine snow’ and marine sediments and their flux plays a critical role in transporting and recycling of organic

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matter (Turner, 2002). With the evolution of both phytoplankton and planktic

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arthropods in the Cambrian in tandem with the macroevolution of metazoans (Lipps and Culver, 2002; Butterfield, 2007), the manner by which marine organic matter was

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recycled changed dramatically from the Proterozoic. The faecal pellets of extant

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zooplankton vary and include ellipsoidal and rod shapes (e.g. Wilson et al., 2008;

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Köster et al., 2011). However, these tend to be isolated objects, not clustered. The more or less uniform orientation of the pellets in the clusters suggests they have

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passed through a gut en masse and are more likely from deposit-feeding or herbivory on the seafloor.

5.3 Taphonomic considerations Coprolites are regarded as trace fossils, but unlike conventional trace fossils, such as trackways and burrows, they are only rarely found in situ. For example faecal pellets on the seafloor may have been released by animals living in the water column; transport by ocean currents is possible if they stayed suspended. There are examples of faecal pellets that remain in situ because they are preserved inside burrow tubes in plants (Taylor et al., 2009), inside arthropod carapaces and close by in the surrounding

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ACCEPTED MANUSCRIPT sediment (Zhang et al., 2007), and in burrows made by deposit-feeders (e.g., Weber et al., 2012; Izumi, 2013). In the Duyun coprolite assemblage there is no direct evidence

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for most coprolites to indicate whether they remained in situ or not, but the faecal

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strings and loosely packed faecal pellets were probably not exposed to strong currents and not transported far as otherwise they would have disaggregated, possibly as the binding mucus decayed.

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Orsten-type fossil Lagerstätten exhibiting preservation of soft tissues with high

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fidelity have become a major focus of study, particularly with regard to their arthropod fauna. The understanding of the taphonomic pathways associated with this

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exceptional preservation is still elusive (e.g. Maas et al., 2003; Shen et al., 2013b).

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Because phosphatocopine arthropods with soft-parts preserved were found together

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with faecal pellets in the Alum Shale Formation of southern Sweden, Maeda et al. (2011) considered that the faecal pellets themselves were responsible for increasing

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the phosphorus level in the sediment during early diagenesis, leading to the formation of orsten-type preservation. Similarly, the trilobite gut was assumed by Lerosey-Aubril et al. (2012) to form a microenvironment enriched in phosphorus that led to detailed preservation. Neither of these mechanisms can be demonstrated for the Duyun fauna, which includes both replaced hard parts and soft tissues (including embryos), extracted individually from limestones. It is possible that in these epeiric seas there was a significant loading of phosphorus from the adjacent land surface and because of restricted circulation it remained in the seawater for a sufficient amount of time before being diluted (Sato et al., in press).

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6. Conclusions

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Relatively few examples in the fossil record are known of invertebrate coprolites

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that are well preserved by secondary mineralization in the form of apatite replacement. Four morphotypes of coprolites (muddy ellipsoids, rods, and strings, and bioclastic rods) are recognized from the phosphatized fossil assemblage in the middle Cambrian

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(Stage 5) Gaotai Formation of South China. According to their size, morphology and

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inclusions they are presumed to be produced by several taxa of small-sized invertebrate animals, possibly including juvenile versions. Muddy ellipsoids, muddy

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rods and muddy strings are filled with fine-grained material that consisted originally

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of either or both organic matter and lime mud. These were produced mostly by

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deposit-feeders but small pellets clusters might have been produced by filter-feeders. Coprolites consisting of either brachiopod valves or palaeoscolecid cuticles probably

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indicate the presence of prey selectivity. Although their affinities remain unknown, these coprolites and co-existing rare orsten-type soft-bodied fossils and numerous phosphatized invertebrate skeletons and shells point to an elaborate trophic structure in this middle Cambrian, low-energy marine ecosystem. Acknowledgements This study was supported by the National Natural Science Foundation of China (41272027, 41302012) and Ministry of Education of China (20115301110001). We thank T. Lan and J.-B. Hou for help in field work, and H.-Q. Zhang and M. Tian for sample preparation, and the two referees for critical comments.

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Bruthansová, J., Kraft, P., 2003. Pellets independent of or associated with Bohemian

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ACCEPTED MANUSCRIPT Table 1. Basic characteristics of the Duyun coprolites.

clusters of

ellipsoids

small spheroids

Muddy

coiled or

strings

meandering

Muddy

clustered and

rods

isolated

Length

L/W

specimens

(mm)

ratio

30

1.0– 2.3

about

0.8–2.1

1.4– 8.1

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0.8–2.1

2.5– 5.9

cylindrical

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1.2– 2.0

2.5–3.0

traces smooth

absent

Figures 2A–H

±wrinkles

2I–K

possibly

smooth,

2L–P

organism-rich

with

deposit

shallow concentric grooves

worm cuticles ,

granular

3A–I, 4A–J

bradoriid carapaces or brachiopod valves

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rods

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cylinders

Bioclastic

absent

2.5 13

Surface

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Muddy

Number of

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Type

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ACCEPTED MANUSCRIPT Figure Captions Fig. 1. Location and stratigraphic occurrence of Cambrian Stage 5 coprolites found

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near Duyun, southern China.

Fig. 2. Phosphatized coprolites from the lower Gaotai Formation. (A–H) clusters of muddy ellipsoids with faecal pellets varying in size and number: (A) YKLP 12091,

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small cluster with most pellets parallel to its long axis; (B) YKLP 12092, large

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cluster with many pellets roughly oriented in right angles to its long axis; (C) YKLP 12093, cluster of pellets oriented obliquely at various angles; (D) YKLP

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12094, loosely packed pellets oriented obliquely at various angles. (E–H) clusters

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with a few relatively larger pellets with cylindrical shape: (E) YKLP 12095, seven

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pellets oriented subparallel to the long axis; (F) YKLP 12096, larger pellets oriented almost subparallel to the long axis; (G) YKLP 12097, three various-sized

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pellets; (H) YKLP 12098, two large pellets. (I–K) muddy strings: (I) YKLP 12099, tightly coiled specimen; (J, K) YKLP 12100, 12101, meandering specimens with transverse striae (arrowed). (L–P) muddy rods comprising large, elongated cylinders with transverse to oblique concentric shallow grooves on the outer surface: (L) YKLP 12102, irregularly curving cylinder; (M) YKLP 12103, short straight cylinder; (N) YKLP 12104, irregularly curving cylinder; (O) YKLP 12105, elongate curving cylinder; (P) YKLP 12106, elongated, slightly curving cylinder. Scale bar same for all.

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ACCEPTED MANUSCRIPT Fig. 3. Phosphatized bradoriid, palaeoscolecid cuticle and coprolites (bioclastic rods). (A–F) coprolites composed of small button-like sclerites belonging to

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palaeoscolecid worms: (A) YKLP 12107, slightly curving cylinder; (B) YKLP

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12108, straight cylinder; (C) detail of (B) showing each sclerites ornamented with a ring of pointed protuberances and one located centrally; (D) YKLP 12109, irregular cylinder containing muddy material along with sclerites; (E) detail of (D);

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(F) YKLP 12110, curving form in between elongate ellipsoid to cylinder in shape.

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(G–I) coprolites composed of compressed bradoriid (Bradoria duyunensis Zhang, 2007) carapace: (G) YKLP 12111, irregular cylinder dominated by muddy

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material and exhibiting fine pits. (H) cylindrical shaped, showing fine pits; (I)

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detail of (H) showing fine pits and narrow marginal rim (arrowed). (J) articulated

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valves of B. duyunensis with fine pits and narrow marginal rim (arrowed), (K) detail of fine pits. Specimens (A–K) were collected from Cambrian Stage 5 the

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lower Gaotai Formation in Duyun, Guizhou. (L) Cuticle of palaeoscolecid worms collected from Cambrian Stage 3 Yu'anshan Formation in Yongshan, Yunnan; (M) detail of (L) showing fine protuberances.

Fig. 4. Phosphatized brachiopods and coprolites (bioclastic rods) composed of brachiopods and variable amounts of muddy material from the lower Gaotai Formation in Duyun, Guizhou. (A) YKLP 12112, irregular short cylinder; (B) detail of (A); (C) YKLP 12113, short cylinder; (D) detail of (C); (E) YKLP 12114, irregular cylinder containing valves with broken and worn surfaces (arrowed); (F)

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ACCEPTED MANUSCRIPT YKLP 12115, irregular cylinder consisting of a cluster of valves (mostly larval); (G) detail of L, showing articulated valves; (H) YKLP 12116, irregular cylinder; (I)

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YKLP 12117, short cylinder with valve exhibiting two elevated nodes; (J) detail

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of (I) showing the two prominent nodes and finely pitted ornament. (K–M) ligulate brachiopods: (K) Opisthotreta? sp.; (L) Lingulepis sp.; (M) Botsfordia sp.

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500 µm scale bar same for A, C, E, F, H, I; l, 200 µm scale bar for B, D, G, J–M.

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Fig. 5. Rose diagrams showing the orientational frequency of the long axis of each ellipsoidal muddy pellet against the long axis of the elongate cluster (taken as

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horizontal). Cluster orientation is held such that the vector mean of pellet

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orientation dips to the right. Orientations are of the pellets visible on the cluster

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exterior and measured from SEM photomicrographs; petal length is normalized to percentage. (A–D) plot of illustrated specimens Fig. 2A–D respectively; YKLP

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12091–12094. (E–F) plot of non-illustrated specimen (YKLP 12118, 12119).

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ACCEPTED MANUSCRIPT Highlights of four bullet points

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Cambrian (500 Myr old) coprolites found from China display diversified morphotypes

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They provide evidence for evaluation of the predator–prey and scavenger

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relationships

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A complex trophic structure may have already been present in the benthic community

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The survival of these coprolites seems to involve some specialized burial conditions

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