The ichnology of vertebrate consumption: dentalites, gastroliths and bromalites

There is a long tradition of indirectly inferring feeding in fossil and Recent vertebrates from the functional morphology of bones and teeth. However, some trace fossils provide direct evidence of feeding, and the study of the ichnology of feeding dates to the 1820s–1830s. Trace fossils that document vertebrate consumption in all of its phases are dentalites (“tooth marks”), gastroliths and bromalites (includes coprolites, consumulites and regurgitalites, among others), and these trace fossils are key to understanding the evolution of nutrient acquisition and food processing in the evolutionary history of vertebrates. We review the fossil record and significance of these ichnofossils as they relate to feeding, which is to say we review the ichnology of vertebrate consumption. Beyond a review, we also indicate areas for further research, which are many, on dentalites, gastroliths and bromalites. Finally, we analyze our knowledge of the history of these trace fossils to identify critical biotic events and turning points in the evolutionary history of vertebrate consumption. There is an extensive fossil record of vertebrate dentalites (“tooth marks”), principally on bony substrates, but also on invertebrate hard parts, coprolites, plants, lithic substrates and others, reviewed here for the first time. Two centuries of studies of dentalites show strong biases towards archeology, and towards dinosaurs as a result of the Taxophile Effect. This record merits more synthetic study in an ichnotaxonomic framework and the development of criteria for establishing inferences about behavior. Indeed, dentalites are of diverse paleoethological significance, including: (1) predation, including hunting strategies; (2) bite method and force; (3) dietary selection; (4) feeding; (5) scavenging strategies; (6) methodologies of bone accumulation; (7) trophic patterns; (8) intraspecific (agonistic) interactions; (9) tooth sharpening; and (10) bone and rock utilization for other purposes, including mineral extraction. What is now needed is a dentalite ichnology beginning with diverse documentation of the dentalite ichnofossil record, compilation and synthesis of the entire record, rigorous ichnotaxonomy and determination of analytical criteria for establishing inferences about the behaviors archived by tooth-mark ichnofossils. Bromalites include regurgitalites, consumulites, coprolites, pabulites and digestilites. Regurgitalites are the least studied bromalites, the most difficult to identify, and their fossil record is strongly controlled by taxonomic and taphonomic factors. Bromalite pellets can represent coprolites or regurgitalites, and two-dimensional examples could be taphonomic artifacts (decayed specimens or physical concentrations). Many identified vertebrate regurgitalites were produced by fish or birds and are preserved in a limited range of environmental settings (e. g., aquatic low energy). Regurgitalites have diverse utility, including: (1) providing evidence of the evolution of predation and digestion; (2) analysis of taphonomy and sedimentary environments; (3) proxies for the presence of biotaxa; (4) loci for exceptional preservation; (5) biogeographic studies; (6) evaluating digestive processes of producers; and (7) evidence of the evolution of durophagy. There are numerous descriptions of consumulites, reviewed for the first time here, but they are usually concealed within publications with a different focus. Consumulites give the most unambiguous dietary attributions of any bromalites and provide direct evidence of the nature of digestion and the structure of the digestive tract. However, the study of consumulites is in an early stage of development, though they also have great potential to provide direct evidence of aspects of patterns of digestion, such as: (1) assessing the chemistry of digestive systems by examining the etching and erosion of consumulite materials; (2) studying the evolution of the components of the digestive system; (3) analyzing dietary changes through ontogeny; (4) evaluating the evolution of diets within clades; and (5) identifying environmental tolerances. Consumulites may preserve a wide range of organic elements with a poor fossil record and thus can be Lagerstätten. In addition, consumulites can also preserve tissues of the gastrointestinal tract. The systematic study of consumulites will undoubtedly yield significant records of contained fossils, as has the recent focus on the contents of coprolites. The term gastrolith refers to sand and/or gravel swallowed by an animal and retained in the digestive tract. Wings recently grouped objects with different origins under the single term gastrolith, so he proposed to add prefixes to the word gastrolith to create terms that identified their different origins: “bio-gastrolith” for the calcareous concretions formed in the bodies of some crustaceans; “patho-gastrolith” for concretions formed in the stomach pathologically; and “geo-gastroliths” for swallowed rock particles. These terms are unnecessary if gastrolith is restricted to the meaning we advocate, which is the same as Wing’s “geo-gastrolith.” Wings also advocated using the term 2 “exolith” for “stones” that might be gastroliths but that lack a convincing skeletal association. This term, however, enshrines the widespread misconception that highly polished “stones” are gastroliths, regardless of any skeletal association. It also lacks specificity, as any polished “stone” anywhere could be called an exolith. Thus, we do not use the term exolith. The distribution of gastroliths is very irregular in extant vertebrates and is often related to the presence of a muscular gizzard. Nevertheless, swallowing or not swallowing sand/gravel can be specific to some individuals within a species. A variety of functions have been suggested for gastroliths, only two of which are of significance: use in digestion to grind, pulverize and/or disintegrate food or use as ballast for buoyancy control. It seems likely that some crocodiles and marine mammals use/used gastroliths for buoyancy control, but all other gastrolith-bearing vertebrates appear to have used them in digestion. Identification of fossil gastroliths is only certain when the sand/gravel is found as a concentrated mass in an anatomically plausible position within the abdominal region of a fossil skeleton. There are various ways to polish stones, notably by the wind to make them ventifacts. Polished clasts identified as gastroliths are siliceous, mostly quartz or chert. These clasts could have been polished by wind and/or water, both before ingestion by an animal and/or after excretion or other removal from an animal’s digestive tract. Furthermore, how a stomach or gizzard would polish siliceous clasts (which are very hard) is also unclear, and such polishing does not occur in extant birds. Only a small minority of bona fide gastroliths, particularly those of plesiosaurs, are highly polished. There is thus an inability to establish when and where the clasts were polished, and inferring that they acquired their polish while gastroliths is not supported by actualistic studies of gastroliths. The idea that any highly polished clast is a gastrolith needs to be abandoned. Most records of gastroliths are from plesiosaurs, birds and some dinosaurs. Gastroliths are trace fossils in need of ichnotaxonomy that provide important insights into various behaviors. Gastroliths clearly are the work of an animal. Unlike eggs, for example, the sand/gravel that comprise gastroliths (our definition) is not made by animals–it is swallowed by, concentrated by, transported by and, in some cases, altered by animals. So, the trace-fossil status of gastroliths is unimpeachable. We advocate development of an ichnotaxonomy for gastroliths. Ichnotaxonomic names, however, should not be assigned to individual grains/clasts of sand/gravel of fossil gastroliths. We favor naming the entire gastrolith mass from a single abdominal cavity. Ichnotaxobases could be the number of gastroliths in the mass, their general petrographic composition, and their overall size, shape, surface texture and other shared morphological features. This likely would produce a workable ichnotaxonomy that recognizes ichnotaxa that are readily distinguished by morphological differences that are a direct reflection of varied behavior. Gastroliths provide important insights into various behaviors, notably diet, digestion, buoyancy control and habitat preferences. After footprints, coprolites are the most studied vertebrate trace fossils, and they are the subject of an extensive and rapidly growing literature. Coprolites have an extensive fossil record that has proven potential to address a broad range of paleontological issues: (1) coprolites as proxy for biotaxa have utility in biochronology, biogeography and faunal turnover; (2) coprolites as trace fossils can delimit a hierarchy of ichnocoensoes and ichnofacies; (3) coprolites as end products of the gastrointestinal tract can provide evidence of digestive processes; and (4) internally, coprolites can be Lagerstätten that preserve a wide range of organisms with an otherwise poor fossil record. Other bromalites are digestilites, pabulites and micturalites. Digestilites is a new term for materials derived from the digestive tract. They are subject to chemical and physical processes that result in characteristic damage that can be recognized in regurgitated or defecated material. Digestilites composed of invertebrate debris provide a particularly important insight into the evolution of durophagous fish and also constitute a significant sediment source, particularly in the Cenozoic. Many late Cenozoic (and some earlier) microvertebrate accumulations consist of digestilites, and this large topic deserves substantial study. Pabulites are fossilized food that never entered the digestive tract. Footprints, some nests and other traces also can record evidence of vertebrate predation and consumption. Mololite is a new term for tooth wear, which is a type of trace fossil. There are taphonomic megabiases in the trace fossil record of vertebrate consumption. The bromalite and dentalite records are heavily skewed towards carnivores. There are also significant size-related biases, for example that small and large coprolites and regurgitalites are rare, as are small dentalites. Certain time periods demonstrate strong, geologically-based biases. For example, the continental flooding of the Late Cretaceous resulted in extensive trace (and body) fossils preserved in the Western Interior Basin of North America, not only in the sedimentary deposits of the seaways but also in the rocks that formed on the associated coastal plains. The first large sample of vertebrate ichnofossils related to feeding is from the Devonian, but the largest acme is in the Late Cretaceous, which resulted from taphonomy (continental flooding), the evolution of predators (e.g., sharks, mosasaurs, large theropods) and the Taxophile Effect. The fossil record of trace fossils provides substantial information about the evolution of vertebrate feeding. In addition, relevant vertebrate and invertebrate ichnofossils provide significant insight into major evolutionary events. The earliest evidence of predation is from terminal Neoproterozoic trace fossils. The earliest definitive vertebrate feeding traces are spiral coprolites and regurgitalites from the Late Ordovician, but earlier bromalites could pertain to vertebrates. The oldest dentalite is from the Middle Silurian. Consumulites occur in Middle Silurian fish, but the first recognizable contents are from the Early Devonian. Bromalites and dentalites provide evidence for major evolutionary events including the Great Ordovician Biodiversification Event, Middle Paleozoic Marine Revolution, and Mesozoic Marine Revolution, as well as various proposed mass extinctions, real and imagined. 3 Consumulites are important in understanding the evolution of the avian digestive Bauplan. We also introduce the following terms: (1) cropalite for preserved contents of the crop, (2) proventrilite for contents of the proventriculus; (3) aspirationalite (from the medical term for food in the airway) for consumulites that preserve prey in the oral cavity with a significant portion extending exteriorly; (4) dislocational evisceralite for a portion of the gastrointestinal tract is physically removed from a carcass; and (5) preservational evisceralite for preferential fossilization of the gastrointestinal tract. There is an almost 200-year history of naming vertebrate tracks, but there is an unjustified reluctance to apply a binominal ichotaxonomy to traces related to feeding that impedes the development of their study.