Residues from the Upper Permian carnivore ...

Palaeogeography, Palaeoclimatology, Palaeoecology 482 (2017) 70–82

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Residues from the Upper Permian carnivore coprolites from Vyazniki in Russia - key questions in reconstruction of feeding habits Piotr Bajdek a, Krzysztof Owocki b, Andrey G. Sennikov c,d, Valeriy K. Golubev c,d, Grzegorz Niedźwiedzki e,⁎ a

Aleja Najświętszej Maryi Panny 20/20A, 42-200 Częstochowa, Poland Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, 00-818 Warsaw, Poland Borissiak Paleontological Institute, Russian Academy of Sciences, Profsoyuznaya 123, Moscow 117997, Russia d Kazan Federal University, Kremlyovskaya 18, 420008 Kazan, Russia e Department of Organismal Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18A, 752 36 Uppsala, Sweden b c

a r t i c l e

i n f o

Article history: Received 24 January 2017 Received in revised form 17 May 2017 Available online 31 May 2017 Keywords: Fossil feces Acid dissolution Undigested remains Microbial fossils Palaeoecology

a b s t r a c t Residues of twenty-five coprolite fragments collected from the Upper Permian of Vyazniki (European Russia) were studied in detail. The phosphatic composition, general shape and size, and bone inclusions of these specimens indicate that medium to large-sized carnivores, such as therocephalian therapsids or early archosauriforms, were the most likely coprolite producers. The contents of the examined fossils (i.e. scale, bone and tooth fragments, mineral grains, and microbial structures) do not differ significantly among the samples, implying fairly comparable feeding habits of their producers. Fragments of large tooth crowns in two of the analyzed samples imply that either (1) the coprolite producer swallowed the cranial elements of its prey or (2) the coprolite producer broke and swallowed its own tooth while feeding (such tooth damage is known in archosaurs that have tooth replacement, e.g. crocodiles and dinosaurs). Indeed, the most complete tooth fragment in these fossils is serrated, most likely belonging to an early archosauriform known from skeletal records from the Late Permian of Vyazniki. Another coprolite fragment contains the etched tooth of a lungfish, while putative actinopterygian fish remains (scales and small fragments of bones) are abundant in some samples. Mineral particles (mostly quartz grains, feldspars and mica) may have been swallowed accidentally. The preserved microbial colonies (mineralized fossil fungi and bacteria or their pseudomorphs), manifested in the coprolites as Fe-rich mineral structures, seem to have developed on the expelled feces rather than on the items before they were swallowed. © 2017 Elsevier B.V. All rights reserved.

1. Introduction Coprolites (fossil feces) are of great interest and increasing importance in the study of food chains in ancient ecosystems (Thulborn, 1991; Chin et al., 2008; Wood et al., 2012; Zatoń and Rakociński, 2014; Schwimmer et al., 2015; Niedźwiedzki et al., 2016a, 2016b; Silva et al., 2017). Such study is possible due to incompletely digested food components and other inclusions which these fossils often contain (Rodríguez-de la Rosa et al., 1998; Northwood, 2005; Yates et al., 2012; Zatoń et al., 2015, 2017; Bajdek et al., 2016; Hansen et al., 2016; Qvarnström et al., 2016). Recently, coprolite studies have become increasingly multi-disciplinary (e.g. palaeobotany, palaeozoology, chemical analyses, biomarker analyses; see Zatoń et al., 2015), allowing us to obtain a greater amount of novel data. Coprolite content is often described on the basis of thin sections (Chin, 2002, 2007a), but these are usually non-serial and made on a small number of specimens, rarely more than dozen thin sections in ⁎ Corresponding author. E-mail address: [email protected] (G. Niedźwiedzki).

http://dx.doi.org/10.1016/j.palaeo.2017.05.033 0031-0182/© 2017 Elsevier B.V. All rights reserved.

total (Chin and Kirkland, 1998; Chin, 2007b; Smith and Botha-Brink, 2011; Fiorelli et al., 2013; Bajdek et al., 2016). Such methods allow us to visualize details of even very delicate inclusions (Dentzien-Dias et al., 2013; Bajdek et al., 2016), yet any conclusions regarding the feeding habits of the coprolite producers are tenuous because of the small amount of material sampled. Coprolite studies based on an alternative method, chemical maceration (acid dissolution), are still rare and usually return a paucity of quantitative data (e.g. Kar et al., 2004; Vijaya and Singh, 2009; Khosla et al., 2015, 2016; Robin et al., 2016; Vajda et al., 2016). These two methods are destructive (Chin, 2002; Wood and Wilmshurst, 2016), and therefore the analyses should be well-planned and consider the most suitable methods, and the material should be properly documented, in order to maximize the amount of information that can be obtained. Two non-destructive alternatives, namely computed tomography (Milàn et al., 2012a; Anagnostakis, 2013; Fiorelli et al., 2013; Bravo-Cuevas et al., 2017; Segesdi et al., 2017) and synchrotron microtomography (Qvarnström et al., 2017; Zatoń et al., 2017), can give detailed identification of inclusion material. Qvarnström et al. (2017) demonstrate that propagation phase-contrast synchrotron

P. Bajdek et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 482 (2017) 70–82

microtomography (PPC-SRμCT) permits high-quality virtual 3D-reconstruction, and that this can be a powerful method when applied to coprolites. In this paper, we present the results of a detailed examination of residues obtained via controlled acid dissolution of a set of 25 phosphatic coprolite fragments collected from the Upper Permian of Vyazniki, Central Russia (Fig. 1). These specimens represent two morphotypes interpreted as produced by large carnivores (Owocki et al., 2012; Bajdek et al., 2016; Niedźwiedzki et al., 2016a). Detailed observations on thin sections of these two coprolite morphotypes (A and B sensu Owocki et al., 2012) have been recently presented (Bajdek et al., 2016), and the importance of the entire set of nine coprolite morphotypes (A–I) collected in Vyazniki from the Permian and Triassic deposits has also been recently discussed (Niedźwiedzki et al., 2016a). However, the results of the acid dissolutions presented here greatly expand our understanding of the coprolite composition and palaeoecology of the top carnivores from these Late Permian ecosystems. Additionally, using multiple analytical techniques (thin section, acid dissolution, and scanning electron microscope) of the coprolite material from Vyazniki allows us to compare the results obtained from distinct analysis methods. This study examines the totality of inorganic and organic inclusions extracted via the dissolution method from two coprolite morphotypes from a single stratigraphic level, allowing us to reconsider the palaeobiological implications presented in our previous studies (Owocki et al., 2012; Bajdek et al., 2016; Niedźwiedzki et al., 2016a). These observations may be generally applicable to future coprolite research. In addition, some aspects of diet interpretation based on the coprolite content and mineral composition are discussed. In the future, we plan to perform additional non-destructive research (CT-scans and synchrotron microtomography) on this information-rich material from Vyazniki.

2. Geological setting The studied coprolites were collected from an artificial outcrop (sand pit) at the Bykovka Quarry (56.256350N; 42.100183E) at Vyazniki, Russia (Fig. 1A, B). The Upper Permian rocks exposed at Vyazniki represent the record of a large fluvial distributary system

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developed to the west of the Ural Mountains (Sennikov and Golubev, 2006, 2012; Newell et al., 2010). At the Bykovka Quarry, an approximately 7-m-thick section is visible, comprising thin intervals of interlaminated greenish and red mudstone, siltstone and fine-grained sandstone with locally conglomeratic intraclasts (Fig. 1C; see Owocki et al., 2012: Fig. 3; Niedźwiedzki et al., 2016a: Fig. 4C, D). This section represents the upper part of the Upper Permian (Zhukovian Regional Stage; Obnora Formation) deposits and consists predominantly of lacustrine claystones and limestones as well as floodplain claystones, siltstones, sandstones and locally fluvial sandstones. The deposits of the Zhukovian Regional Stage are characterized by a pre-extinction and still diverse terrestrial flora and fauna (e.g. Afonin, 2005; Sennikov and Golubev, 2006, 2012; Krassilov and Karasev, 2009; Golubev et al., 2012). This part of the Permo-Triassic Vyazniki section also has a rich record of vertebrate coprolites (Niedźwiedzki et al., 2016a). All material studied here was collected from the same stratigraphic interval, that is, the upper coprolite-bearing interval (Fig. 1C), rich in morphotypes and specimens. Coprolites were photographed in situ and in some cases preserved in local accumulations (see Owocki et al., 2012: Fig. 3A, B, D) in mudstone, siltstone and sandstone beds, well-exposed in the lower and uppermost part of the section (Newell et al., 2010; Owocki et al., 2012; Bajdek et al., 2016; Niedźwiedzki et al., 2016a). The uppermost Permian strata from Vyazniki have yielded numerous vertebrate body fossils, a rich material of fish teeth, bones and scales (Minikh and Minikh, 1998; Pindakiewicz et al., 2015), and rare and slightly abraded bones of small to large tetrapods (Sennikov and Golubev, 2006, 2012; Newell et al., 2010).

3. Materials and methods The aim of the study was to extract all the hard elements (mineral and organic) that were preserved in the phosphatic coprolite matrix. In total, about 40 coprolites from morphotypes A and B (as designated by Owocki et al., 2012: see Fig. 4) were collected from the Bykovka Quarry for this study. Twenty-five well preserved, dried and surface cleaned fragments, 9 of morphotype A and 16 of morphotype B (samples 1–25, each weighing approximately 20 g), were selected from this collection (Table 1, Fig. 2A–D) and dissolved in a mixture of

Fig. 1. Maps of the Eastern Europe (A), the area around the town Vyazniki (B) and the Bykovka Quarry section (C) showing the latitude and longitude and lithostratigraphical location of coprolite-bearing fossil site (positions are in decimal degrees; datum: WGS 1984; BY – Belarus, LV – Latvia; EST – Estonia; LT – Lithuania). Modified from Newell et al. (2010) and Owocki et al. (2012).

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Table 1 The list of coprolite fragments examined in this study with details about food residues. Sample Morphotype Mineral grains

Bones

Fish bones

Ganoine

1 2 3

A A A

Rounded quartz Abundant fragments, mostly angular; b1 mm None identified Present Rounded quartz, feldspars Abundant fragments, rounded and angular; b1 mm None identified Present Rounded quartz, feldspars and mica Abundant fragments, rounded and angular; b1.4 mm Present Present

4

B

Rounded quartz, feldspars, mica

5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

A B B B A B B B A B B B B B B A A B B A B

Rounded quartz, feldspars, mica Rounded quartz Rounded quartz Rounded quartz, feldspars, mica Rounded quartz Rounded quartz, feldspars, mica Rounded quartz Rounded quartz, feldspars, mica Rounded quartz Rounded quartz Rounded quartz, mica Rounded quartz, mica Rounded quartz Rounded quartz Rounded quartz Rounded quartz Rounded quartz Rounded quartz, feldspars, mica Rounded quartz Rounded quartz Rounded quartz, feldspars

Abundant fragments, rounded and angular; rounded bone 8.5 × 5 mm Abundant fragments, rounded and angular; b 4 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm Abundant fragments, rounded and angular; b1 mm

buffered formic acid (3–5%) and acetic acid (2–3%). The solutions with immersed coprolites were heated several times to around 50 °C to accelerate dissolution (approximately 2 h total). The process lasted 2– 3 weeks until the mineralized coprolite mass was completely disintegrated. The samples were then washed with distilled water to carry the mineral suspension away. Finally, the samples were put into a sieve (0.1 mm mesh openings) and washed with a mixture of distilled water and 95% ethanol. The residues were then dried and placed in sterile sample tubes. The extracted material was analyzed in two stages. First, all samples were examined under stereo and optical microscopes under reflected and transmitted illumination via unpolarized, plane-polarized and cross-polarized light methods. Selected items were then studied under SEM equipped with EDS. All residue samples and selected sample elements (e.g. scales, bones, tooth fragments) are preserved in plastic tubes at the research collection at the Institute of Paleobiology, Polish Academy of Sciences, Warsaw (Poland). 4. Coprolite descriptions 4.1. Morphotype A Narrow and elongated, cylindrical in shape, fairly straight coprolite, with rounded or slightly tapered extremities (see Owocki et al., 2012: Fig. 4A–C; Bajdek et al., 2016: Fig. 2A–C; Niedźwiedzki et al., 2016a: Fig. 6A–D). This morphotype is characterized by numerous skeletal remains (teeth, bones, scales), (see Owocki et al., 2012; Bajdek et al., 2016; Niedźwiedzki et al., 2016a, this study). A carnivorous therocephalian therapsid was suggested as producing these coprolites (Owocki et al., 2012; Niedźwiedzki et al., 2016a). The presence of fragments of bones in this morphotype suggests their producers had a fast metabolism (Chin et al., 1998, 2003; Owocki et al., 2012). Owocki et al. (2012) suggested that the specimens of morphotype A had been produced by a carnivorous therapsid, as well as Smith and Botha-Brink (2011) who attributed some Upper Permian bone-rich coprolites/ cololites most likely to therapsids. The large diameter and volume of these specimens would point out large therocephalians Moschowhaitsia

Teeth

None identified None identified

None identified None identified 1 possible fish tooth (0.17 × 0.10 mm) None identified

None identified Present None identified Present Present Present None identified None identified None identified None identified Present None identified None identified None identified None identified None identified Present Possible None identified None identified Possible

None identified None identified None identified None identified None identified None identified None identified Tooth None identified Tooth None identified None identified None identified None identified Dipnoan tooth None identified None identified None identified None identified None identified None identified

Present Possible rounded Present Present Present Present Present Present Present Present Present Present Present Present Present Present Present Present Present Present Present

vjuschkovi or Megawhaitsia patrichae known from the Vyazniki assemblage as the most probable producers (Owocki et al., 2012). Moreover, the presence of well-vascularized therapsid (possibly dicynodont) bones in the coprolites might tentatively suggest that they have been produced by a top predator (Owocki et al., 2012; Bajdek et al., 2016). 4.2. Morphotype B Thick and elongated, cylindrical in shape, straight or slightly curved coprolite which is usually composed of several segments and have rather rounded extremities (see Owocki et al., 2012: Fig. 4D–F; Bajdek et al., 2016: Fig. 3D–F; Niedźwiedzki et al., 2016a: Fig. 6: E–H). Poorly preserved bone and tooth fragments were identified in this morphotype (see Owocki et al., 2012; Bajdek et al., 2016; Niedźwiedzki et al., 2016a, this study). A carnivorous archosauromorph or archosauriform was suggested as a supposed producer (Owocki et al., 2012; Niedźwiedzki et al., 2016a). Owocki et al. (2012) attributed the specimens of morphotype B to a carnivore producer with slow metabolism due to the fact that bone inclusions are rare and highly degraded. Generally, such bonepoor feces characterize those produced by animals with extensive digestion and strong gastric acids, like for instance in certain extant taxa like crocodiles (Fisher, 1981a, 1981b; Milàn, 2012) and snakes (Secor, 2008). On the other hand, bones might have been regurgitated rather than expelled in feces or just swallowed in small amounts (see Silva et al., 2017). The large size of the specimens, as well as fragments of serrated teeth being included (observation based on this study), suggests the producer is a medium- to large-sized archosauriform. The osteological material of Archosaurus rossicus is known from Vyazniki, so this oldest proterosuchid is the most probable producer of segmented and bonepoor coprolites from the site (Owocki et al., 2012; Niedźwiedzki et al., 2016a). 5. Results The residues are composed of mineral grains (quartz, feldspar, mica; Fig. 4) and secondarily of bone fragments (including fragments of scales and teeth; Figs. 5 and 6) and mineralized aggregates of microbial origin.


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Fig. 2. Examples of studied coprolite fragments (A – morphotype A; B–D – morphotype B; sensu Owocki et al., 2012) collected from the same Upper Permian upper coprolite-bearing interval exposed at the Bykovka Quarry (see Owocki et al., 2012; Bajdek et al., 2016). Highly weathered coprolite fragments (E–F) observed in situ in the upper part of the Bykovka Quarry section (red arrows point to bone fragments). Red square inserts are enlargement of elements that are identified as bone remains. Scale bar: 1 cm.

Some fragments of the coprolite matrix have not completely dissolved and are permineralized by iron oxides, microbial matter (Fig. 7), manganese minerals and also some elements are slightly silicified (EDS observations). The results of stereo microscope observations are summarized in the Table 1. Comparison of types of inclusions found within the coprolites from Vyazniki (morphotypes A and B) via different analytical methods (thin sections, acid dissolution, scanning electron microscope) in this and our previous studies is presented in the Table 2. 5.1. Mineral grains Mineral grains found in the samples are represented primarily by quartz and also feldspars or mica (Fig. 4), but N 50% of the grains are quartz in all studied samples. The quartz grains are usually rounded, mostly finely grained and rarely exceeds 0.25 mm in diameter, but can be up to 0.75 mm in diameter. In spite of some diversity, no substantial differences in either abundance or size of the quartz grains between the samples were noticed (Fig. 8). The mineral clasts normally constitute most of the residues and they are generally of smaller dimensions than bone elements. The quartz grains can be most easily distinguished from rounded bones and minute fragments of incompletely dissolved coprolite matrix under cross-polarized light. 5.2. Bones and scales All of the dissolved coprolite samples revealed the presence of minute rounded and angular bone fragments (e.g. Figs. 3E and 5F). Since the thin sections reveal that some bone fragments are fractured (Bajdek et al., 2016), the angular bone elements in part may be fragments of larger bones partially disintegrated during the process of dissolution and maceration. However, some of them have well-preserved external bone surfaces, which suggest that they have been poorly etched by stomach acids. This is especially the case of dark glassy bone elements found in 24 of the 25 coprolite samples, which are often angular and sometimes have patterns like those of fish scales, and therefore are interpreted as ganoine (Figs. 3C–D and 5C–D). Moreover, other angular minute bones, probably of actinopterygian fish, were found in some of the

samples and were apparently also poorly digested too. One of the samples (no. 1) contains mostly angular bone fragments, though in the other samples both rounded and angular ones are abundant. 5.3. Teeth fragments The nearly-complete serrated tooth crown (12.1 × 5.5 mm) of an archosauriform was found in sample no. 12 (Figs. 3G and 6G–J). Another crown, smaller but comparable in morphology, was found in sample no. 14 (Fig. 6C–F). The distal parts of both teeth show clear signs of abrasion by masticatory wear (e.g. Fig. 6C–I). Some fragments of the enamel and dentin are broken off; the broken surfaces are angular and neither tooth shows evident signs of acid etching or decalcification. However, the etched tooth (11.3 × 7.4 mm) of a lungfish was found in sample no. 19 (Figs. 3H and 6A–B). 5.4. Biofilms Phosphatized aggregates and in part Fe-rich mineralized microbial biofilms of thread-like structures were found under SEM. The filaments range from 0.5 μm to 3 μm in width (Fig. 7A–B, D–F). The hyphae are most likely either fungal in origin or possibly represent bacteria, for example Actinobacteria. Also, spherical bacterial cells were found in these mineral aggregates (Fig. 7C), which have previously been described and discussed in the material from the same locality (Owocki et al., 2012; Bajdek et al., 2016). 6. Discussion 6.1. Comparison of analytical methods In this and our previous studies (Owocki et al., 2012; Bajdek et al., 2016) three different analytical methods (thin sections, scanning electron microscopy, and acid dissolution), in addition to macroscopic observations, were used for detailed study of organic remains and other inclusions in the coprolite material from the Upper Permian of Vyazniki, Russia. The results of the analyses of the two different morphotypes (A

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Fig. 3. Photos of some elements found in the residues. (A–B) View of two samples (no. 19, morphotype B and no. 9, morphotype A); note that the largest elements are mostly undissolved coprolite matrix, but fragments of fish scales are also present (red arrows). (C) Marginal fragment of serrated tooth of an archosauriform (sample no. 12, morphotype B). (D) Fish remain (samples no. 10, morphotype B). (E) Bone fragment (sample no. 10, morphotype B). (F) Close-up view of the mineral grains (sample no. 6, morphotype B). (G) Serrated tooth of an archosauriform (sample no. 12, morphotype B). (H) Etched lungfish tooth (sample no. 19, morphotype B). Scale bar: A, B = 5 mm; C–H = 1 mm.

and B sensu Owocki et al., 2012; see also Niedźwiedzki et al., 2016a) are summarized in the Table 2. Results varied depending on the method. The acid dissolution allowed detection of the largest amount of hard remains, such as bones and the only teeth found in the coprolite material from Vyazniki. Bone remains found using this method are also the most easily identifiable, because the method recovers such details as fish scale surface patterns. Yet, bones tend to be highly fragmented after acid dissolution due to numerous fractures seen in thin sections. Remarkably, the acid dissolution allowed us to find a large amount of mineral grains (mainly clastic quartz), which has gone unnoticed in studies using thin sections and SEM. Some details of bone preservation are more easily studied by the use of thin section (Bajdek et al., 2016; Zatoń et al., 2015). Thin sections also allowed us to detect numerous, very delicate and minute remains, such as bacteria, cyanobacteria, protists, fungi, invertebrate eggs, arthropod exoskeletons, possible worms and burrows, hairs, plant cuticles, all of which were lost during the acid dissolution and maceration (Bajdek et al., 2016; see also Dentzien-Dias et al., 2013). Scanning electron microscopy was effective for studying details of some large elements, such as bones and other items detected in thin sections and non-microscopic observations (this study; Owocki et al., 2012). SEM was also very useful in the study of pseudomorphs after bacteria in the coprolite matrix. Noteably, the study of the coprolite

matrix under SEM allowed us to largely expand our knowledge about microbial biofilms, such as fungal hyphae, in the coprolite material from Vyazniki (see also Dentzien-Dias et al., 2016). Still, some details of the organization of microbial colonies are best visible in thin sections (Bajdek et al., 2016). In sum, acid dissolution was the most effective method for studying the diet of the coprolite producers from Vyazniki, despite some kinds of swallowed remains (e.g. hairs and possibly arthropods) not being detected. Much valuable paleobiological information, such as evidence for parasitism, was also (and exclusively) obtained through thin sections. SEM equipped with EDS was an important supplementary method allowing us to study different aspects of the material in more detail. 6.2. Palaeobiological interpretations Although coprolites are a valuable source of information about the diet of their producers (e.g. Chin et al., 2008; Wood et al., 2012; Schwimmer et al., 2015; Bajdek et al., 2016), several factors may easily mislead the researcher when the coprolite content is analyzed and interpretations of coprolite contents can be problematic. Potentially complicating factors include (1) prey species differences in hard skeletal element content; (2) dietary component differences in resistance to dissolution in the gastrointestinal tract and also in their fossilization potential; (3) diversified diets or diets that are changeable seasonally or


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Fig. 4. SEM images of selected mineral grains (A–F) from the coprolite residues and results of the EDS analysis of their surfaces (G–I). (A–C) Angular grains (A, B – sample no. 8, morphotype B; C – sample no. 19, morphotype B). (D–F) Rounded grains (D – sample no. 12, morphotype B; E – sample no. 21, morphotype A; F – sample no. 19, morphotype B).

ontogenetically; (4) carnivores consuming other species' gastrointestinal tracts and/or (5) swallowing their own body elements (like teeth or hairs); (6) feces can be exploited by other organisms (like fungi and invertebrates) or can be (7) consumed by other vertebrates. Additionally, (8) carnivore/omnivore coprolites are usually, but not necessarily, phosphatic, which complicates analysis of non-phosphatic specimens. These issues will now be addressed in turn. 6.2.1. Selective preservation of remains Different prey species will have different amounts of hard skeletal elements. For example, Zatoń and Rakociński (2014) described Upper Devonian fish coprolites/cololites with abundant arthropod cuticle fragments, followed by fish scales and teeth and (least abundant) conodont and scolecodont elements. They concluded that the predominance of arthropods and fish remains within the coprolites clearly suggests that the predators preferred those food items. However, some arthropods are entirely armored with chitinous exoskeletons, fishes have bones and scales, and the bodies of conodonts and numerous types of invertebrates are nearly entirely soft. The skeletal elements and other diet components differ in resistance to dissolution in the gastrointestinal tract as well as in their fossilization potential. Stomach contents of marine reptiles contain chitinous belemnite hooklets and calcitic rostra, other calcitic shells, but less-resistant to digestive processes aragonitic elements are missing (Kear, 2006; Lomax, 2010). Bajdek (2013) described an Upper Cretaceous coprolite

containing fragmented calcitic inoceramid shells, but no other remains were present. It seems obvious that its producer fed on inoceramid bivalves but, as emphasized by Bajdek (2013), its complete diet remains unknown. Moreover, some vertebrates, as crocodiles, used to completely decalcify ingested bones (Milàn, 2012). Chin and Kirkland (1998) presented different states of preservation of plant remains in Upper Jurassic herbivorous dinosaur coprolites depending on the mineral composition of the coprolite specimens. 6.2.2. Resistance to dissolution Phosphatic elements found in the coprolites from Vyazniki seem mostly well-resistant to dissolution by stomach acids (Fig. 8). There are such elements as fish scales (composed of ganoine), teeth, or cortical (compact) bone. Some of the bone elements are rounded from putative acid etching, although other angular elements also are found. No cancellous (spongy) bones were recognized in the material. It seems that cartilaginous and cancellous bone elements were completely digested by coprolite producers. Also in the thin sections bone elements with cancellous tissue are poorly preserved or lacking (Bajdek et al., 2016). In addition, Owocki et al. (2012) described in detail A and B morphotypes of carnivore coprolites from Vyazniki, but only one on them is abundant with bone fragments, and the other nearly boneless. It was suggested that the coprolite producers differed in physiology, as e.g. in the food retention time in the gastrointestinal tract (Owocki et al., 2012; Bajdek et al., 2016). It cannot be also ruled out that the

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Fig. 5. SEM images of selected phosphatic elements from coprolites. (A) Fragment of compact bone (probably it is fragment of long bone of small tetrapod) from sample no. 1 (morphotype A). (B, E) Fragments of dermal bones with characteristic and well-layered internal organization (B – sample no. 9, morphotype B; E – sample no. 8, morphotype B). (C, D) Fragments of bones with characteristic ridges (r) from specimen no. 18 (morphotype B). (F) Fragment of rib of small tetrapod from specimen no. 10 (morphotype B).

producers had distinct prey preferences or that the same coprolite morphotype was produced by different taxa. A carnivore feeding on small tetrapod prey or those having poorly mineralized skeleton (e.g. small amphibians) would not be expected to excrete feces rich in hard undigested elements. 6.2.3. Diversified diet The diet of some animals is quite diversified or changeable seasonally, as e.g. in coyotes (Seamster et al., 2014). The diet also shifts during ontogeny, as exemplified by crocodiles (Wallace, 2006). The content of the analyzed samples is however fairy homogeneous and rather no substantial differences between the 25 samples were noticed. It might be related to the ecological conditions and behavior or to physiology of the coprolite producers (e.g. both producers were top predators in the Late Permian ecosystem from Vyazniki and hunted mainly large animals). It's possible that the studied material does not include scats of juvenile individuals. Fishes constituted a constant element of diet of carnivores that produced the morphotypes A and B. However, their diet was implemented with tetrapod prey (see Owocki et al., 2012; Bajdek et al., 2016). 6.2.4. Complex food chains Carnivores consume other species' gastrointestinal tracts, including those of herbivores. Prasad et al. (2005) described phytoliths (silicified plant tissues) preserved in Upper Cretaceous coprolites from India linking them to various plant taxa, including putative grasses. The

phytoliths were extracted from four coprolite morphotypes (A, B, Ba, and C) that were all ascribed to titanosaur sauropods, although only the type A coprolites were ascribed to titanosaurs by Ghosh et al. (2003) and Sharma et al. (2005) cited by Prasad et al. (2005). However, at least the Type A and Type B coprolites are phosphatic (Ghosh et al., 2003; Khosla et al., 2015) that points out that the diet of their producers included meat. Ghosh et al. (2003) in fact notes the phosphatic composition of the specimens and then ignore this part of their own results suggesting herbivory based on the δ15N isotopic analyses of the Type A coprolites. Khosla et al. (2015) concluded that the combination of a phosphatic composition with plant and microfossil dietary residues in the Type A coprolites suggests that their producers were intentional or inadvertent omnivores. They noted that extant crocodilians are known to ingest considerable plant material (N 7% by weight or volume; Platt et al., 1990) either through feeding in aquatic environments with abundant plant debris or possibly through consumption of the gut contents of herbivorous prey (Khosla et al., 2015; see also Keenan et al., 2013). Similarly, Northwood (2005) noted that some of the silicified coprolites containing abundant plant material described by Rodríguez-de la Rosa et al. (1998) from the Upper Cretaceous of Mexico might have been produced by crocodilians. Crocodilians decalcify bones so that typically no bone remains are found in their feces (Milàn, 2012). RuizOmeñaca et al. (1997) described nine morphotypes of phosphatic coprolites lacking bone elements and containing possible plant seeds and green algae from the Upper Cretaceous of Spain. Erroneously, all these coprolites were ascribed to herbivores and ornithopod dinosaurs were


77

Fig. 6. SEM observations of phosphatic elements from coprolites. (A–B) Etched lungfish tooth (sample no. 19, morphotype B). Archosauromorph teeth fragments from the sample no. 14, morphotype B (C–F) and the sample no. 12, morphotype B (G–J).

pointed out as the most likely producers (Ruiz-Omeñaca et al., 1997). Zatoń et al. (2015) and Segesdi et al. (2017) described plant cuticles in phosphatic coprolites that might have been produced by carnivores or omnivores. It seems that plant remains are not rare in phosphatic and bone-bearing coprolites. In the coprolite material from Vyazniki, some plant tissues were described from thin sections by Bajdek et al. (2016). However, we have found no plant cuticles in the residues after dissolution of coprolite fragments in the present study. Some minute material could possibly get lost when washed through the sieve (0.1 mm mesh openings), but it seems that relatively few plant cuticles have been preserved in the analyzed material. Either plant tissues were not swallowed by coprolite producers in big amount or they were destroyed during diagenesis

(e.g. via oxidation, see Owocki et al., 2012). On the other hand, the residues after dissolution contain considerable amounts of clastic grains (mainly quartz) which are uncommon in thin sections. We conclude that different analytic methods favor detection of different types of inclusions (Table 2). Mineral clasts with a diameter larger than 0.063 mm that had been formerly retained in the digestive tract are classified as gastroliths (Wings, 2007). Such grains, as e.g. quartz, can be excreted with feces and have already been described in coprolites (Wings, 2012; Bajdek et al., 2014). Dimensions of the mineral grains found in the examined Upper Permian coprolite samples from Vyazniki do not exceed those of grains of the host sediment (Newell et al., 2010). The grains might have been easily consumed accidentally, e.g. while feeding in the

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Fig. 7. SEM observations on studied incompletely dissolved fragments of the coprolite matrix with microbial fossils. (A, B, D–F) Details of microbial thread-like structures representing fungi or bacteria (A, B, F – sample no. 4, morphotype B; D, E – sample no. 10, morphotype B). (C) Spherical bacterial cells (sample no. 4, morphotype B). (G, H) Results of the EDS analysis of their surfaces suggesting Fe-rich mineral composition of these structures.

aquatic environment on fish. Also, they might come from ingested gastrointestinal tracts of herbivores, which often consume considerable amounts of sediments (Beyer et al., 1994; Bajdek et al., 2014). Because quartz grains are well-resistant to digestive processes (see Wings, 2007), they are expected to accumulate in feces of top predators, coming from different trophic levels of the food chain.

6.2.5. Ingestion of the producer's own body elements Some animals swallow their own body's elements as e.g. teeth or hairs. Bajdek et al. (2016) described hair-like structures from a coprolite of the morphotype A from Vyazniki. It seems probable that the ingested hairs derive from prey. Well-vascularized, probably therapsid bone fragments are indeed found in the morphotype A (Owocki et al.,

Table 2 Comparison of types of inclusions detected within coprolites via different analytical methods in this and previous studies. Inclusions

Thin sections

Acid dissolution

Scanning electron microscope

References

Bones or bone fragments

+

+

+

Fish scales or their fragments

+

+

–

Arthropod exoskeletons fungi bacteria

+

+

+

Large fragments of tooth Supposed hairs, plant cuticle, cyanobacterial cells, protists, invertebrate eggs, possible nematode burrows (trace fossils) Mineral grains

– +

+ –

– –

Owocki et al. (2012) Bajdek et al. (2016) this study Bajdek et al. (2016) this study Owocki et al. (2012) Bajdek et al. (2016) this study this study Bajdek et al. (2016)

–

+

–

this study


79

Fig. 8. Pie charts (selected 7 examples) showing a relative percentage of the main element groups (samples no. 3, 5, 13 – morphotype A; samples no. 12, 15, 23 – morphotype B).

2012). Nevertheless, because the morphotype A was ascribed to a therapsid carnivore as well (Owocki et al., 2012), the hairs might belong to the coprolite producer if swallowed e.g. while fur cleaning. The lungfish tooth found in a coprolite fragment in the present study must have come from prey. However, it's more problematical to interpret the broken archosauriform teeth found in the examined samples. If teeth fragments found in the sample no. 12 and 14 derive from prey, the rest of its skeletal elements were nearly completely digested. Indeed, teeth are very resistant to dissolution by gastric fluids and may be better-preserved in bromalites than other skeletal elements (Silva et al., 2017), although it should be noted that extant crocodiles normally decalcify ingested teeth (Fisher, 1981a, 1981b). Interestingly, it would also point that the coprolite producers swallowed the entire prey with at least some cranial elements. Modern reptiles often swallow the entire prey, as exemplified by snakes (Secor, 2008), although in crocodiles a very large prey item needs to be initially dismembered (Grigg and Gans, 1993; Webb and Manolis, 2009). This can be done through mechanical action or through decomposition of a carcass, as in modern crocodiles that may consume carrion and also hide large prey items until they rot (Webb and Manolis, 2009). Early Permian mesosaurids probably also consumed carrion (Silva et al., 2017). Either of these possibilities would be expected to demonstrate bone-crushing of the remains (see Chin et al., 1998). Alternately, the coprolite producers may have swallowed their own teeth which were broken while feeding. Such tooth damage is known to occur in numerous archosauriforms and archosaurs, which are often characterized by relatively fast tooth replacement (Grigg and Gans, 1993). Here, the distal parts of both teeth show clear signs of mechanical abrasion (Fig. 6C–I). A large bone-rich phosphatic mass interpreted as a coprolite from the Upper Jurassic Morrison Formation, described in an abstract by Stone et al. (2000), contained a broken distal end of an Allosaurus tooth. The authors suggested that during mastication the tooth was broken and ingested by the theropod, which chewed its meal and broke the bones into smaller portions (Stone et al., 2000). It is possible that the Upper Permian material from Vyazniki represents the oldest known record of a comparable mechanism in archosauriforms. Moreover, mesosaurid teeth are found in coprolites, gut contents and regurgitalites of mesosaurids from the Early Permian and either represent broken teeth of the bromalite producers or derive from abundantly consumed mesosaurid carrion (Silva et al., 2017). 6.2.6. Exploitation of feces Feces may be exploited by invertebrate organisms, including obligate or opportunistic invertebrate coprophagies (Galante and Marcos-García, 1997; Chin and Gill, 1996; Wahl et al., 1998; Milàn et

al., 2012b; Chin and Bishop, 2007). Chin et al. (2009) described at least seven different taxa of snails found on or within coprolites of herbivorous dinosaurs from the Upper Cretaceous of Montana. However, the snails exploited the feces rather than have been consumed with forage (Chin et al., 2009). The hyphae found in the samples from Vyazniki are interpreted as most likely fungal in origin or representing Actinobacteria. Actinobacteria are present but constitute a rather minor group of bacteria in human and alligator feces (Keenan et al., 2013). However, Cano et al. (2014) found larger proportions of Actinobacteria in cortices of human coprolites due to environmental contamination by soil microbes. Similarly, the fungal hyphae would have developed after excretion of the fecal matter (see Badal and Atienza, 2005). It should be noticed that based exclusively on thin sections, such structures may be easy to misinterpret for coming from the gastrointestinal tract. The problem of origin of bacterial and fungal structures in coprolites was also discussed by Bajdek et al. (2016). 6.2.7. Ingestion of feces by herbivores Some vertebrates consume their own or other individuals' feces, as exemplified by woolly mammoths (van Geel et al., 2011), and herbivore feces might be mistaken for carnivore/omnivore feces too. Some herbivorous animals are known to ingest bones, perhaps for supplementation of minerals, as for example tortoises (Esque and Peters, 1994). In such a case, the bulk of the coprolite material would be from a herbivore, which would obviously influence the interpretation. 6.2.8. Mineral composition of coprolites Carnivore coprolites have been thought to be necessarily phosphatic in contrast to herbivore coprolites (Chin, 2002). However, this has been shown to not always be the case. Fecal matter rich in shell fragments of a coprolite specimen from deep-marine turbidite sediments of the Cretaceous of Poland was replaced by fine clastic material (Bajdek, 2013). Also, Retallack and Krull (1997) described spiral coprolites/cololites consisting of sandstone fragments from the Permian of Antarctica. Gilmore (1992) described non-phosphatic argillaeous spiral coprolites/cololites from the Silurian of Ireland. A taphonomic scenario leading to such a form of preservation has not yet been described. Distinct forms of preservation of feces might have to do with differences in the role of bacteria in this process (see Hollocher and Hollocher, 2012; Bajdek et al., 2016; Qvarnström et al., 2016), among other taphonomic factors. Bacteria allow the preservation of the phosphatic matrix of feces even in environments of a very low sedimentation rate (Hu et al., 2010; Silva et al., 2017).

80


Burmeister (2000) briefly described calcitic coprolites containing fish bones and scales from the Upper Triassic of Madagascar. Nevertheless, most of calcitic coprolites known from the fossil record were produced by herbivores (e.g. Chin and Kirkland, 1998; Chin, 2007b; Fiorelli et al., 2013). Enigmatic excrement or intestine-shaped sideritic and limonitic structures are known from various formations, including the Upper Permian of China, the Upper Cretaceous of Saskatchewan and Madagascar, the Upper Miocene of the state of Washington, USA, as well as the Paleocene of North Dakota (Broughton et al., 1978; Seilacher et al., 2001; Broughton, 2016). Their origins have been variously interpreted as coprolites or pseudofossils (see Mustoe, 2001). Seilacher et al. (2001) suggested that they are cololites (intestinal casts) and that the absence of bone remains and phosphate could be explained by the action of roll-fronts of oxidized groundwater that destroyed phosphatic bones, but favored siderite precipitation. Some propose that the sideritic/limonitic material might be a post-void filling (cast of molds after fecal matter) rather than a fossilized early replacement of organic material of feces and intestines of giant worms (Broughton, 2016). Nevertheless, due to the atypical morphology of those specimens, nonphosphatic composition and the lack of organic remains, their fecal origin is doubtful. On the other hand, several morphotypes of secondarily sideritic coprolites, some of them containing plant remains, are known from the lowermost Jurassic of Poland (Niedźwiedzki, 2011). Nonphosphatic coprolite specimens may be hard to assign to herbivorous, carnivorous or omnivorous producers. Bajdek et al. (2014) performed δ13C and δ15N isotopic analyses to confirm the coprolitic interpretation of non-phosphatic specimens from the Upper Triassic of Poland ascribed to dicynodonts and the herbivorous diet of their producers. 7. Conclusions Although analyses of fossil feces may yield potentially valuable data about food chains in ancient ecosystems, caution is advised because the results can be easily misinterpreted. Single feces samples may accumulate remains from different trophic levels, and the diagenetic processes and ingested food components should also be carefully considered. As demonstrated in the material from the Upper Permian of Vyazniki, different analytical methods (thin sections, acid dissolution, and scanning electron microscope) favor detection of different types of inclusions, a fact that should also be taken in consideration. Fishes constituted a constant element of the diet of the carnivores that produced coprolites of morphotypes A and B from the Vyazniki site. Their diets were however supplemented with tetrapod prey, as evidenced by small and large bone fragments in the coprolites. Fragments of large tooth crowns that were found in two coprolites suggest that either the producers swallowed the cranial elements of their prey items, or that they swallowed their own teeth while feeding. After excretion, the fecal matter comprising the coprolites was exploited by microorganisms and highly colonized by bacteria and fungi from the environment. Acknowledgments The coprolite-bearing deposits at Bykovka were examined in the field in 2008, 2010 and 2013 during trips organized by the Institute of Paleobiology, Polish Academy of Sciences, Poland, the Faculty of Biology, University of Warsaw, Poland and the Borissiak Paleontological Institute, Russian Academy of Sciences. The field studies were supported by grants from the Polish Ministry of Science and Higher Education (no. 7986/B/2011/40 to Tomasz Sulej). The research was also supported by the Evolutionary Biology Center, Uppsala University and the Institute of Paleobiology, Polish Academy of Sciences. G.N. is currently funded by a Wallenberg scholarship grant awarded to Per Erik Ahlberg (Uppsala University). A.G.S. and V.K.G. are funded according to the Russian Government Program of Competitive Growth of Kazan Federal University,

by the Program of Basic Research of the Presidium of the RAS No. 30 ‘The evolution of the organic world and planetary processes’ and by RFBR project No. 17-04-00410. Thanks to Paula Dentzien-Dias and two anonymous reviewers whose comments improved the paper. We are grateful to Isabel Montañez (PPP, Editor-in-Chief) and Jennifer Ast (Ast Clear Text, Uppsala) whose comments largely improved the final version of the manuscript. References Afonin, S.A., 2005. Latest Permian palynological assemblage from Vyazniki, European Russia: stratigraphic and palaeoecological significance in relation to the Permo-Triassic boundary. NMMNH Bull. 30, 5–8. Anagnostakis, S., 2013. Upper Cretaceous Coprolites from the Münster Basin (northwestern Germany) – a glimpse into the diet of extinct animals. Dissertations in Geology at Lund University (Msc. Thesis, no 357, p. 30). Badal, E., Atienza, V., 2005. Análisis microscópico de coprolitos de herbívoros hallados en contextos arqueológicos. 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