1Department of Biology, Emory University, Atlanta, GA 30322.
Coprolites occur in the Petrified Forest Member in association with a bone bed known in PEFO as "The Dying Grounds;" the environment is interpreted as a perennial swamp or watering hole. Coprolites are primarily ellipsoidal and cylindrical; specimens examined have an average of 1.4 + 0.4 cm diameter (n = 45) and lengths range from 1-6 cm, although most specimens are incomplete. Digestive tract morphology of tracemakers is revealed by coprolite size, surface markings (vertical parallel and horizontal heteropolar striations), and pinched or tapered ends. Bone fragments and concentrations of calcium and phosphorus, evident in some samples through macroscopic and SEM examinations, reflect a carnivorous feeding habit for at least some tracemakers. Likely candidates for tracemakers, estimated through the vertebrate body fossil record for this region, are aetosaurs, metoposaurs, phytosaurs, rauisuchians, or theropods.
About a third of examined coprolites have minute-diameter holes (0.7 + 0.3 mm; n = 16, measured through SEM), some of which show interconnections through tunnels parallel to coprolite surfaces. We interpret these features as coprophagy traces made by insects, such as dipteran larvae, which may be among the oldest reported such traces in the geologic record. These traces demonstrate cycling of organic material from vertebrate feces occurred soon after fecal formation and represent time preceding early diagenesis, exhumation, transportation, and final burial of feces.
Figure 1Location of coprolite samples in Petrified Forest
Member, Chinle Formation, Petrified Forest National Park,
Arizona; "D.G." indicates "Dying Grounds."
Although coprolites (fossilized feces) have gained some popular recognition in recent years, particularly as related to dinosaurs (Hunt et al., 1994; Wright, 1996), they remain comparatively less studied than trace fossils such as tracks, trails, and burrows. Although unpopular, coprolites are nevertheless valuable trace fossils because of their direct relation to paleodiet. These trace fossils can be used to determine the existence of certain food types, such as plants or animals, during the time of fecal formation (Walderman and Hopkins, 1970; Sohn and Chatterjee, 1979; Chin 1990; Chin et al., 1991a,b) and digestive tract morphology (Thulborn, 1991). Traces within coprolites, such as burrows by organisms consuming organic material in the original feces, are also instructive for understanding nutrient cycling in the context of the tracemakers' environments (Chin and Gill, 1996).
Trace fossils in strata of the Chinle Formation (Late
Triassic) of Petrified Forest National Park (PEFO) are very
common, interpreted as originating from both invertebrate
and vertebrate tracemakers in a variety of continental
settings (Dubiel and Hasiotis, 1995; Hasiotis and Dubiel,
1993a,b, 1995; Martin et al., 1997). Although Late Triassic
coprolites in nearby New Mexico were investigated by Ash (1978)
and Weber and Lawler (1978), vertebrate coprolites in the
Chinle of PEFO have not been thoroughly described or interpreted
in terms of their taphonomic and paleoecologic significance.
we provide a preliminary description of vertebrate coprolites and their accompanying trace fossils. The latter may be the oldest interpreted evidence of feeding on vertebrate fecal remains (coprophagy) in the geologic record.
Study Area and Stratigraphy
The 45 specimens in this study were collected in PEFO from a smectitic purple-gray mudstone in the Petrified Forest Member of the Late Triassic Chinle Formation (Figure 1). The bone bed containing the coprolites is referred to as the "Dying Grounds" by some workers in this region because of its abundance of skeletal material. This area was formed mainly through deposition in low-sinuosity streams (Kraus and Middleton, 1987), as represented by channel sandstones, floodplain-paleosol mudstones, and locally evident organics-rich pond and bog mudstones (Parrish, 1989). The depositional environment for final coprolite burial is interpreted as a pond or floodplain.
The 45 specimens were initially assessed through qualitative and quantitative analysis. Each specimen was examined for specific morphology. The samples exhibited most standard morphological characteristics for coprolites, as outlined by Thulborn (1991) and Hunt et al. (1994), and thus proved capable of categorization. Sizes were assessed through measurement and calculation of circumference, diameter, radius, and length. Circumferences were taken from the three thickest zones on coprolites and averaged to give the approximate circumference. Diameter and radii were then calculated from circumference data. Length was incomplete in nearly all specimens but measurements were taken for the sake of comparison.
About one-third of specimens showed regularly shaped holes and connections between holes, hence scanning electron microscopy (SEM) was employed to better describe and measure these features. Samples for SEM investigation were washed with acetone, then vacuum-pumped dry and gold coated with a Denton Vacuum DESK II Cold Sputter/Etch Unit. Once samples were coated with gold, they were placed on the mounting stage in the SEM. The SEM, a Zeiss DSM-962, was furnished by Fernbank Natural History Museum in Atlanta, Georgia, for this portion of the study. The SEM allowed examination of microstructures and accurate measurements of diameters of the suspected burrows within the coprolites. Carbon-coated coprolites were also examined for elemental analysis on the same unit.
Amphipolar = 0% Bend = 26% Heteropolar = 0% Radial = 0% Cylindrical = 93.3% Concentric = 42% Pellet = 0% Parallel Striations = 28% Pinched End = 24% Regular Pits = 13% Tapered End = 55% Irregular Pits = 35% Constriction = 22%
Coprolite morphological terms include 15 types commonly used in the coprolite literature. Neumayer (1904) coined the terms amphipolar and heteropolar; Thulborn (1991) subsequently initiated the use of isopolar and anisopolar as descriptive terms for coprolite morphology. Of these 15 descriptive terms, at least one of nine could be applied to the examined Chinle specimens (Table 1). Most of the samples are incomplete and broken on one end, which makes some of the morphological types difficult to distinguish. For example, determination of isopolar and anisopolar requires two complete ends, but because the entire length of the coprolites did not always remain intact, these types could not be interpreted. Weathering also may have broken down surface morphology, therefore this feature also could not be documented in some samples.
Coprolite sizes varied to some degree (Table 2) but with more sampling a normal distribution might become more apparent. Because the coprolites were mostly ellipsoidal and cylindrical, circumference, diameter, radius, and length were the most useful measurements to quantify. Specimens examined have an average of 1.4 + 0.4 cm diameter, and lengths range from 1-6 cm, although because most specimens are incomplete, these lengths represent minimum values.
Regularly-sized holes and connections between holes on some coprolites, examined through SEM, showed evidence of probable coprophagy traces. Sample PEFO-14 (Figure 2a-b) proved to be the best sample for the study of these regularly shaped holes. With the SEM, 16 well-defined holes were measured and analyzed. From these measurements diameters ranged from 0.28 to 1.32 mm, with a mean of 0.7 + 0.3 mm. Proportionately, 38% of the holes are in the 0.7 mm range, which demonstrates a regularity in size that is probably attributable to a similar-sized tracemaker. Analysis of the holes with the SEM also showed tunneling and interconnections parallel to the coprolite surface, which suggest a trace made by a living organism, as opposed to gas bubbles that might be associated with decay of fecal material.
Range Mean Standard deviation Circumference 2.4-8.27 4.4 1.3 Diameter 0.76-2.63 1.4 0.4 Radius 0.4-1.3 0.7 0.2 Length 1.0-6.1 2.7 1.2
Taphonomic and Paleoecologic Significance of Chinle Coprolites
Figure 2Coprolite sample PEFO-14. Top, Macroscopic view, showing overall cylindrical morphology of coprolite and burrows in coprolite; millimeter scale. Bottom, Composite SEM image of coprolite with view of numerous holes and tunnels between holes, representing burrows (coprophagy traces) in sample.
Because fossilization occurred in a wetland environment, the tracemakers were probably carnivores or omnivores because digestion of animals with skeletons would leave bone residues in the fecal matter (Thulborn, 1991). Bone matrix is very useful in fossilization because it provides minerals and structure from which apatite can form. Herbivore scat tends to contain larger quantities of undigested plant matter which will decay instead of fossilize (Chin et al., 1996), hence most coprolites are likely from carnivore tracemakers. Bone fragments in Chinle coprolites are evident, as well as localized high concentrations of calcium and phosphorus (indicated by elemental analysis on the SEM), which also indicates a carnivorous diet for most tracemakers. Furthermore, cylindrical morphology, observed in 93% of Chinle specimens, is also suggestive of meat-eating tracemakers. In modern terrestrial vertebrates, pellet-shaped scat is typically formed by herbivores, whereas cylindrical scat is more commonly left by carnivores (Halfpenny and Biesot, 1986).
End morphology can also suggest other aspects of digestion, such as how the anal sphincter of an animal may have worked. Feces with pinched ends may have been excreted from an animal with a stronger or faster-closing sphincter muscle than those that produce feces with tapered ends. Constrictions and bends could be incurred after exiting the body but otherwise they suggest periodicity of peristalsis of the large intestine. Parallel striations also characterize the large intestine but they imply striations on the internal surface of the intestine. Because none of the coprolites exhibit heteropolar striations, they can not be attributed to fish (Thulborn, 1991). Irregular pits, as opposed to regularly shaped holes attributable to coprophagy, may be a product of transportation of coprolitic material before final burial or holes produced when bone fragments dislodged from the exterior of the coprolite.
Coprophagy traces have been rarely evaluated. Grooves discovered in an Eocene coprolite might be attributed to dung beetles (Bradley, 1946). Chin and Gill (1996) evaluated coprophagy traces from Late Cretaceous coprolites and attributed them to dung beetles, but no coprophagy traces of any kind have been reported from coprolites as old as Late Triassic. Dung beetles are clearly too large as possible tracemakers for burrows in the Chinle coprolites, but possible tracemakers may have been dipteran larvae, such as those exemplified by modern dung-eating flies (Petersen and Wiegert, 1982; Nilsson, 1983; Iwasa, 1984; Stevenson and Dindal, 1987; Zhemchuzhina and Zvereva, 1989; Stoffolano et al., 1995). Fungal microrhizae are an alternative hypothesis for the traces, but the regularity in size and interconnectiveness of the traces are contrary to the size variation and randomness exhibited by microrhizal structures.
Coprolite makers most likely would have been represented by any or all of four possible carnivorous tracemakers, indicated by body fossils found in PEFO: phytosaurs, metoposaurs, theropods, and rauisuchians (Parrish, 1989). An absence of flattening that normally occurs with impact upon the open-air ground suggests that these coprolites were probably excreted into water (Waldman and Hopkins, 1970), favoring an aquatic habitat for the trace makers. The floodplain region could have accommodated each of these inhabitants; metoposaurs and phytosaurs were especially likely candidates because of their aquatic life habits and the presumed deposition of fecal material in water (interpreted from the nonflattened specimens). Aetosaurs or other herbivore tracemakers may have been responsible for the 7% of non-cylindrical coprolites, but no other evidence other than shape reflects a herbivore origin.
From this study we show that it is possible to classify the PEFO coprolites into descriptive categories. Specifically, because the coprolites in this study showed many similar and consistent morphological attributes, they were possibly left by similar types of animals. The overwhelming percentage of cylindrical coprolites at least suggests similar intestinal workings and diet, and other evidence, such as bone fragments and high concentrations of calcium and phosphorus in some specimens, reflect carnivorous tracemakers. None of the examined coprolites was left by fish because none of them have heteropolar markings, typical of fish feces; correlation with known body fossils in PEFO thus points toward theropods, rauisuchians, metoposaurs and phytosaurs as possible tracemakers, with herbivorous aetosaurs as less likely candidates. Further study of Chinle coprolites in PEFO should better define tracemakers.
Evidence of coprophagy in Chinle coprolites is reasonably conclusive because of the overall morphology and regularity of holes and tunnels evident in some specimens. More research is necessary to better delineate possible tracemakers but insects, such as dipteran larvae, are a possibility. Fungal coprophages, which would be evident through microrhizae, represent an alternative explanation for tracemakers but the regularity and size of the traces argue against this interpretation. If these traces are more persuasively shown as related to insect activity in vertebrate feces, they would be the oldest reported such traces in the geologic record.
We thank the PEFO personnel, who all deserve praise for their cooperation and helpfulness during our visits to the park. SEM analyses were conducted at Fernbank Museum of Natural History in Atlanta, Georgia, under the knowledgeable guidance of Christine Bean, an enthusiastic participant in our "paleo-poop" research. We thank the three anonymous reviewers for their reading the manuscript and their positive feedback regarding the work. Lastly, we very much appreciate the encouragement of Vincent Santucci, who helped the final publication of this paper to become a reality.
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Zhemchuzhina, A. A., and E. L. Zvereva. 1989. Dependence of larval development of coprophagous flies (Diptera) on some properties of the substrate. Entomology Review 68:28-38. Figure 2Coprolite sample PEFO-14. Top, Macroscopic view, showing overall cylindrical morphology of coprolite and burrows in coprolite; millimeter scale. Bottom, Composite SEM image of coprolite with view of numerous holes and tunnels between holes, representing burrows (coprophagy traces) in sample.