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First bone-cracking dog coprolites provide new insight into bone consumption in Borophagus and their unique ecological niche


Borophagine canids have long been hypothesized to be North American ecological ‘avatars’ of living hyenas in Africa and Asia, but direct fossil evidence of hyena-like bone consumption is hitherto unknown. We report rare coprolites (fossilized feces) of Borophagus parvus from the late Miocene of California and, for the first time, describe unambiguous evidence that these predatory canids ingested large amounts of bone. Surface morphology, micro-CT analyses, and contextual information reveal (1) droppings in concentrations signifying scent-marking behavior, similar to latrines used by living social carnivorans; (2) routine consumption of skeletons; (3) undissolved bones inside coprolites indicating gastrointestinal similarity to modern striped and brown hyenas; (4) B. parvus body weight of ~24 kg, reaching sizes of obligatory large-prey hunters; and (5) prey size ranging ~35– kg. This combination of traits suggests that bone-crushing Borophagus potentially hunted in collaborative social groups and occupied a niche no longer present in North American ecosystems.

eLife digest

Living hyenas are infamous for crushing the bones of their prey to extract the nutritious marrow inside. This feeding ability is rare today, and African and Asian hyenas, particularly the spotted hyena, are the only true ‘bone-crackers’ in our modern ecosystems. Yet, between 16 to 2 million years ago, the common, but now extinct North American dogs also crushed bone. Their skeletal features – such as highly robust skulls and jaws, teeth to withstand high stress, and large muscle-attachment areas for a powerful bite –share many similarities with the spotted hyena. It is therefore likely that these extinct North American dogs played a similar role in the ecosystem as living hyenas do now.

The last of these bone-cracking dogs, Borophagus, vanished approximately 2 million years ago. In a recent study in , researchers discovered fossilized feces, also known as coprolites, which presumably belong to Borophagus parvus that lived in central California between 5 to 6 million years. These coprolites preserve ingested bone and so provide more evidence of what this species of dogs ate. Now, Wang et al. – including some of the researchers involved in the previous study – analyzed the fossil coprolites and their ingredients in great detail using computer tomography, measurements and comparisons with living predators and their prey.

The results show that Borophagus parvus weighed around 24 kg and hunted large prey of 35 kg up to kg: the size of a living mule deer. Its skull structure was similar to the spotted hyena, but its digestive system resembled that of striped and brown hyenas. Spotted hyenas have chalk white feces containing digested bone matter, presumably due to a highly acidic digestive system, but the coprolites of Borophagus contained undissolved bones (which they ate regularly). Wang et al. also discovered that these dogs dropped feces in clusters, which is how the spotted hyena and wolves mark territory. This suggests that Borophagus were also social animals.

Bone-crackers (modern and extinct) act as apex predators and providers of free organic material needed for decomposition, which are essential roles for maintaining a healthy ecosystem. The extinction of Borophagus likely modified the dynamics of the food web over the past few million years. It remains unclear why this way of feeding is absent in all living animals of North America. Future studies could investigate how the disappearance of Borophagus may have influenced the establishment of modern environments, eventually setting the scene for human habitation of the continent.


Several lineages of dogs (family Canidae) and hyenas (family Hyaenidae) have independently evolved striking bone-crushing adaptations, such as highly robust skulls, jaws, teeth, and large attachment areas for powerful masticatory muscles. These highly specialized bone-cracking morphologies are likely associated with social hunting (Van Valkenburgh and Koepfli, ; Van Valkenburgh et al., ), as best exemplified by the living spotted hyena (Kruuk, ). Spotted hyenas hunt and feed in groups, have a gastrointestinal system that is able to break down large quantities of bone consumed, and discharge feces with high-carbonate content (Macdonald, ; Estes, ; Hulsman et al., ). Whether extinct hyena-like canids consumed a comparable quantity of bone—and, if so, how those bones are processed inside their gastrointestinal system—both remain questions that have been unanswerable for lack of fossil evidence. These questions are directly addressed in this study with the first discovery of coprolites (fossilized feces) from one of the archetypal bone-eating dogs, Borophagus. Borophagines are a group of carnivorans with highly specialized craniodental morphological traits indicative of bone-cracking adaptation, and have long been recognized to be a terminal member of the subfamily Borophaginae that went extinct just before the beginning of the Ice Ages in North America (Wang et al., ). Therefore, understanding the paleoecology of these top predators has important implications for reconstructing community dynamics on the continent before megafaunal extinction and human habitation.

We analyzed a new sample of coprolites recently discovered from the Mehrten Formation (latest Miocene, – Ma) in Stanislaus County, California. Numerous bone fragments on the external surface and inside the coprolites strongly suggest that they were produced by Borophagus, which is amply represented by body fossils at the same fossil-producing area, thereby affording a rare opportunity to directly examine the diet of an extinct bone-crushing top predator. Despite improvements in our understanding of the biomechanics of the functional convergence of craniodental adaptations between Eurasian-African hyaenids and North American borophagine canids (Werdelin, ; Tseng and Wang, ; Tseng and Wang, ), dietary inferences were previously made only from the fossilized bones of these predators. The discovery of coprolites thus offers the first glimpse into the food ingested and excreted by these ‘hyaenoid dogs’ (Simpson, ), as well as several traits related to their territorial behavior, social hunting, and bone digestion that were previously unapproachable. This study examines 14 coprolites recovered from two localities in the Turlock Lake area, as well as their presumed producer, Borophagus parvus. Our findings provide new insights into the paleoecology of this group of top predators and refine their position in the food web at the end of the Miocene Epoch in North America.

Institutional abbreviations

F:AM Frick Collection of the American Museum of Natural History, New York, New York; FMNH, Field Museum of Natural History, Chicago, Illinois; LACM, Natural History Museum of Los Angeles County, Los Angeles, California; UCMP, Museum of Paleontology at University of California, Berkeley, California.

Results and discussion

Producer of Mehrten coprolites

The large number of bones inside most Mehrten coprolites rules out herbivores as their producers. The size of the coprolites further indicates large carnivorans as their original makers. For medium to large carnivorans from the Mehrten Formation, Wagner (, ) listed a bone-crushing dog Borophagus secundus (=Osteoborus cyonoides), a small coyote-sized Eucyon davisi, an ancestral badger Pliotaxidea garberi, an early wolverine Plesiogulo marshalli, and an ancestral cat Pseudaelurus near P. hibbardi. Most recently, Balisi et al. () added a fox, Vulpes stenognathus, to the list. Of the above, Vulpes, Eucyon, Pliotaxidea, and Plesiogulo can be ruled out as being too small to produce scats of the size of the Mehrten coprolites, whereas the true nature of Mehrten felids is poorly known.

Of the large Mehrten canids, Balisi et al. () recognized two bone-crushing canids, B. secundus and B. parvus, which are the only wolf-sized taxa large enough to be the producers of the Mehrten coprolites. Of these two species, B. secundus is rare, represented by two fragmentary jaws and teeth plus 1–2 questionably referred teeth, whereas B. parvus is far better represented by 27 specimens. At the main coprolite-producing locality (see Materials and methods), LACM locality (=Dennis Garber T locality), an isolated P2 or P3 (UCMP ) is questionably referred to B. secundus (Balisi et al., ), whereas in LACM locality , no identifiable carnivoran is found (Figure 9).

The Mehrten coprolites are comparable in size (Table 1) to scats from extant wolves and are generally larger than those from living coyotes, despite significant overlap between scat diameters of the wolves (average 27 mm, range 13–47 mm) and the coyotes (average 21 mm, range 7–34 mm) (Weaver and Fritts, ; Reid, ). In extant African carnivores, Harrison () documented scat diameters of 20–35 mm from African hunting dogs, Lycaon pictus, and striped hyena, Hyaena hyaena. Therefore, with a maximum diameter of mm, the Mehrten coprolites are more likely produced by a wolf-sized Borophagus than a coyote- to fox-sized Eucyon. Of the two species of Mehrten Borophagus, B. parvus was the more likely producers of Mehrten coprolites based on their body size and far better representation of body fossils, although the possibility of B. secundus cannot be excluded.

Coprolite morphology

We adopt a modified scheme for characterizing hyaenid coprolite aggregate pellets introduced by Diedrich (), but we use different terminologies for orientations (Figure 1A). Although scat morphology of extant wolves and hyenas may be somewhat different—depending on length of retention in digestive tract, fiber and water content of feces, and hardness of ground on which scats were dropped—our Mehrten coprolites (Figures 2 and 3) appear to share substantial similarities to those of living hyenas (Figure 1B). Of the 14 individually catalogued coprolites, five probably are a first dropping due to their bluntly constricted terminal on at least one of their ends and their relatively greater diameter (LACM , , , , and ). However, only one, LACM , has the typical shape of a conical pellet (Figure 1A), although LACM represents a variation of the conical-disk pellet combination that failed to separate after dropping. LACM has tapering on both ends, suggesting that the modern hyena pellet terminology by Diedrich () does not completely apply to the Mehrten canids. The rest of the nine pieces are all incomplete pellets, and their exact position within the scat string is difficult to determine.

If the above assessment is correct, the Mehrten coprolite sample probably consists of individual pellets from multiple dropping events possibly by multiple individuals. This is also suggested by different degrees of desiccation among different coprolite pellets (Figure 5E), that is, they were not defecated at the same time. If this is the case, and assuming that the coprolites have not been transported (there is no sign for transportation), the LACM locality may have been an ancient ‘latrine’ ground for social defecating and scent-marking for territorial boundaries. Such locations have been well documented in extant spotted hyenas (Kruuk, ), coyotes (Gese and Ruff, ), and wolves (Asa et al., ; Harrington and Asa, ). While such behavior is common among social carnivorans, it has not been documented in extinct carnivorans.

Mehrten coprolites maintain nearly perfectly rounded cross sections, showing no sign of post-defecation settling or flattening, nor is there any sign of deformation during the initial impact of dropping. This suggests that the original feces were able to maintain their integrity either because of a relatively hard, moisture-free matrix, and/or because the bones inside plus the high-calcareous contents of the matrix resulted in relatively rigid feces at defecation. Nor do the coprolites show major signs of post-defecation alteration, suggesting fast burial after dropping. Bones are abundant in all coprolites, consisting of 5% of total volume of all coprolites (range 2–25%; see Table 1 for individual volume estimates). As examples, we describe two complete coprolites below.

LACM (Figure 2, Video 1)

This is a nearly perfectly preserved coprolite and also one of the largest, measuring mm in maximum diameter. The bluntly tapered end suggests a terminal pellet (first dropping, Figure 1A). This coprolite is composed of two unseparated pellets, as delineated by a visible groove. The proximal (last dropping) end has a flat surface, representing a clean separation from the next pellet. A single bone is visible on the external surface, with at least 14 bone fragments recognizable in CT image (Figure 2D), although all are unidentifiable small pieces.

LACM (Figure 3, Video 2 )

This is another of the most complete coprolite pellets. The cross-section is nearly perfectly rounded, although there is a distinct flattening on one side, indicating dropping on hard ground during defecation. This coprolite also contains the largest piece of bone, a fragment of a rib shaft measuring 29 mm long × mm wide × mm thick, that nearly spans the length of the pellet (Figure 3C,D). The terminal end of this rib also protrudes outside the coprolite on the tapered end, leaving a sharp tip, 3 mm long, projecting at an angle into the lateral wall of the intestine and showing modest polishing on its surface (red arrows in Figure 3). Another piece of bone (enclosed by red dashed line in Figure 3) has a rounded external surface with a thin cortex filled entirely by cancellous bone, suggesting an articular joint. The size of this bone is consistent with a rib head for the shaft, although we cannot positively identify this as such without physical preparation. Two other smaller pieces of bones are also identified from microCT-scanned images. Total bone volume is 13% of coprolite matrix for LACM , among the highest of all coprolites (Table 1).

Bones inside coprolites

The majority of bones inside the coprolites, even when fully exposed, are too small and too fragmentary to be identified to a particular element or to a particular taxon beyond mammals or even vertebrates. Such difficulty can also be compounded by digitally segmented microCT reconstructions. These digitally separated bones are often an inexact replication of the actual shapes, mostly due to high similarity in X-ray opacity between bones and surrounding matrix. With the exception of a single rib fragment in LACM , all other virtually segmented bones lack sufficient morphological detail to be unambiguously identified.

Generally, there is a lack of clear orientation relative to the long axis of each coprolite (Figure 4). This randomness may be a result of several factors. With the exception of the rib fragment—which, because of its length, must be aligned along the long axis of the coprolite (Figure 3C,D)—most bones are relatively small, and intestine diameter is not a limiting factor in their orientation. Lack of a longitudinal orientation may also be due to a relatively viscous (low water content) matrix and compaction during the last (dehydration) journey of feces through the large intestine.

Surface modifications on bones include rounding of corners, polishing of surface, and acid etching. The external surface of a small bone (red dashed line in Figure 3B) exposed to the intestine wall has experienced visible polishing; this polished surface was also stained a darker color than the unpolished parts. Polishing is known to occur in 80% of bones in extant wolf scat ([Esteban-Nadal et al.,

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