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 2018, 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 100 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, 1993; Van Valkenburgh et al., 2003), as best exemplified by the living spotted hyena (Kruuk, 1972). 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, 1978; Estes, 1991; Hulsman et al., 2010). 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., 1999). 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, 5.3–6.4 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, 1989; Tseng and Wang, 2010; Tseng and Wang, 2011), 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, 1945), 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.

All fossil coprolites and associated vertebrate fossils studied from the Mehrten Formation are housed in the Natural History Museum of Los Angeles County (LACM). Additional fossil collections from the Mehrten Formation housed in the Museum of Paleontology at University of California (UCMP) were also studied. Body size estimates are mostly based on comparisons in the Mammalogy collection of the LACM.

Twelve fossil coprolites were scanned in a Skyscan1172 microCT scanner at a pixel resolution of 26.98 micrometers. The resulting basis images were reconstructed and the resulting dataset imported into Fiji (v. 2.0). In Fiji, the image brightness and contrast were optimized, the images were converted from 16 to 8 bits, and the pixels were binned by a factor of two in all planes. This processed image dataset was then imported into Avizo Lite 9.0.1 for analysis. To aid in detecting bone fragments within the coprolite matrix, each image dataset separately was smoothed by applying a 3D median filter to the images using neighborhood values of 6, 18 and 26 pixels. Cross-sectional images were examined using each of the smoothing levels, as well as the original unsmoothed images. Structures identified as bone were marked using the brush tool with the limited range option to most accurately define the bone/matrix edges. Where there were multiple bone fragments in a coprolite, each was marked separately. Each segmented bone fragment included both the cortical and cancellous portions where present (except in the case of a large rib fragment). The Avizo Materials Statistics module was used to determine the volume of each bone fragment and the surrounding matrix. Avizo measurement tools were used to determine the maximum length and width of each bone fragment as well as the orientation of each fragment’s long axis with respect to the long axis of the coprolite.

Fauna, flora, age relationship, depositional setting, and paleoclimate

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VanderHoof (1933) was first to report a fossil horse, Pliohippus tantalus, from near Oakdale in Stanislaus County, California. Although the Oakdale locality has produced only a few fossils since then, it signaled the potential for discovery of vertebrate fossils in the Mehrten Formation, as well as associated plants (VanderHoof, 1933; Axelrod, 1944). A partial skull of Megalonyx mathisi was described subsequently from Black Rascal Creek in ‘Upper Mehrten Formation’ (Hirschfeld and Webb, 1968). Systematic collecting of fossils in the Turlock Lake area, mostly by one of us (DG), was carried out in as early as the 1950 s. In an unpublished Ph.D. dissertation, Wagner (1981) reviewed the geologic setting and laid out a biostratigraphic framework of the Mehrten Formation as related to the vertebrate fossils. More recently, Sankey et al. (2015) reinvestigated the Turlock Lake fossil sites and began a process of integrating the Mehrten fossils in a modern geologic context (stratigraphic information archived in LACM and UCMP) (see also [Sankey and Biewer, 2017]).

The vertebrate fauna from the Modesto Reservoir Member of Mehrten Formation (as defined in [Wagner, 1981]) was poorly disseminated and with adequate descriptions of only a few forms: a new ‘saber-toothed’ salmonid fish Smilodonichthys rastrosus (Cavender and Miller, 1972; Sankey et al., 2016), a bony fish Orthodon microlepidotus (Casteel and Hutchison, 1973), an extinct New World badger Pliotaxidea garberi (Wagner, 1976), two plethodontid salamanders Aneides lugubris and Batrachoseps sp. (Clark, 1985), and most recently, a giant tortoise Hesperotestudo orthopygia (Biewer et al., 2014; Biewer et al., 2015; Biewer et al., 2016). Wang et al., 1999 and Tedford et al., 2009 listed selected borophagine and canine canids from the Mehrten Formation without description or illustration. A systematic revision of Mehrten canids was completed by Balisi et al. (2018) that recognized four species: Borophagus parvus, B. secundus, Vulpes stenognathus, and Eucyon davisi. See Wagner (1981) for a preliminary faunal list of the rest of the unpublished mammals.

The above four canids are all known in the Hemphillian North American Land Mammal age (Wang et al., 1999; Tedford et al., 2009). Borophagus parvus, however, is the most restrictive both in geographic (southwestern United States) and chronologic (late Hemphillian) ranges, offering the best potential for age assessment. Wang et al. (1999) commented on the slightly more derived dental characteristic of the Mehrten B. parvus, as compared to the topotype materials from the Redington Local Fauna in the lower member of the Quiburis Formation in Pima County, southeastern Arizona, which has been magnetically constrained within Chron 3An.2n (6.436–6.733 Ma) (Lindsay et al., 1984; Hilgen et al., 2012). If those characters are the result of a chronocline, the Mehrten B. parvus may be slightly younger than their Arizona counterpart. Wagner (1981) considered the Modesto Reservoir Local Fauna equivalent in age to Pinole Local Fauna in the San Francisco Bay area, which is overlain by a dated tuff (5.3 ± 0.1 Ma) within Pinole Formation and placed in the latest Hemphillian (Hh4) (Tedford et al., 2004). If the above comparisons are correct, the Modesto Reservoir Local Fauna should fall in the latest Hemphillian (Hh4), possibly within 5.3–6.4 Ma.

From two localities, T-14 (LACM locality 3917, Cement Goose Pit Island = UCMP V6878=V90008) and T-20 (LACM locality 3923, Leaf Island), on two small islands in the western part of Turlock Lake (the former shown in Figure 9A), Axelrod (1980) listed 25 species of fossil plants from what he called Turlock Late Flora consisting of 8 trees (including one conifer), 13 shrubs, 3 herbaceous perennials, and 1 or 2 vines. In particular, aquatic taxa, such as Cyperus (flatsedges), Juncus (rushes), and Typha (cattails), are known to live along the margins of streams, lakes, and ponds, and the fossil plant localities were proposed to be lacustrine deposits ‘some distance from the shore’ (Axelrod, 1980). This flora was characterized as an oak woodland-savanna and a floodplain assemblage, and comparisons to modern vegetation from nearby regions suggested a paleoclimate of slightly cooler (mean annual temperature 15.5°C) and considerably wetter (precipitation 635 mm) than the present-day Turlock Lake area (17.5°C and 335 mm for corresponding measurements). This shift toward a more continental climate in modern day Turlock Lake was suggested to be brought about by the uplift of the Coastal Range and its rain shadow effects during the Pleistocene (Axelrod, 1980).

The majority of the coprolites complete enough to be assigned a Dennis Garber field number are produced from a single locality, LACM locality 3937 (=UCMP locality V68134, Dennis Garber T-34 locality), whereas only one coprolite is from LACM locality 3935 (=Dennis Garber T-32 locality) (Figure 9A). Both are located on the northwestern corner of Turlock Lake; they are within 300 m of each other and are from approximately the same stratigraphic horizon. T-32 was later subsumed within T-34 as a single locality. Fossil-producing exposures are in a large area forming an elbow shape. At the north end, there are two layers of white volcanic ash sandwiching a brown silty clay (Figure 9B). This ash exposure continues to the eastern end of the area, which has a similar lithology to those to the west, although there seems to be a higher ratio of clay to silt and the contact between the ash and clay seems sharper. ([Retallack, 1997]:color photo 24) remarked that carnivore coprolites are common in sequences of well-drained soils because of their phosphatic composition and enclosed bones.

Figure 9

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Estimation of predator body size

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Several regression equations relate skeletal or dental measurements to body mass in extant canids and other carnivorans (Van Valkenburgh, 1990; Anyonge, 1993; Anyonge and Roman, 2006), enabling prediction of the body mass of extinct canids based on measurements of isolated elements. Body mass proxies and their reliability differ slightly, with measures of cross-sectional area of proximal weight-bearing limb bones generating more accurate estimates than dental predictors do. Dental predictors are still useful, however, because teeth tend to be more abundantly preserved than postcrania.

Using the equation of Van Valkenburgh (1990), we generated a distribution of body masses from the lengths of 76 lower first molars (carnassials) of B. parvus compiled by Wang et al. (1999) and Balisi et al. (2018). We also measured two well preserved B. parvus humeri (F:AM 75903-B, F:AM 67955) and one femur (F:AM 63008-A) at the American Museum of Natural History, using the canid equations from Anyonge (1993) to calculate body mass from humeral circumference, cortical cross-sectional area, and second moments of area.

Based on lengths of lower first molars, B. parvus has a median body mass of 18.9 ± 1.6 kg (Figure 10). The Arizona population, with a median mass of 19.2 ± 1.6 kg, tends to be larger in body size than the California population, with a median mass of 18.1 ± 2.0 kg.

Figure 10

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Equations using measurements of the humerus and femur, all specimens from the Arizona population, generated higher estimates than dental estimates of both Arizona and California populations. For F:AM 75903-B, a distal humerus, we calculated body mass using an approximation of the circumference (22.8 kg), cortical area (25.829 kg), second moment of area in the anteroposterior plane (20.898 kg), and second moment of area in the mediolateral plane (29.33 kg); these four estimates produced a median measurement of 24.315 ± 3.656 kg. For F:AM 67955, a complete humerus, we obtained a body-size estimate of 32.4 kg using an approximation of the circumference. For F:AM 63008-A, a proximal femur, we estimated 20.2 kg.

These dental and postcranial estimates of body mass place B. parvus in the same size class as the dingo Canis lupus dingo (20 kg), maned wolf Chrysocyon brachyurus (23 kg), African wild dog Lycaon pictus (24 kg), red wolf Canis rufus (30 kg), and striped hyena Hyaena hyaena (35 kg) (Nowak, 1999; Macdonald, 2006). These extant species (except the omnivorous Chrysocyon) are carnivorous to hypercarnivorous.

Estimation of prey body size

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Several species of fossil ungulates have been recorded at Turlock Lake (Wagner, 1981), providing a pool of potential prey taxa and a starting point for our analysis. We assembled a comparative rib collection of 14 ungulate individuals belonging to 12 extant species at the LACM, spanning as much as possible the familial diversity preserved at Turlock Lake (Table 2). Each specimen comprised a full complement of ribs on at least one side of the body. We attempted to sample the ungulate families recorded by Wagner (1981) or, if extinct, the most closely related extant family (e.g. extant Cervidae as proxy for Palaeomerycidae). Extant perissodactyls were not sampled because the perissodactyls at Turlock Lake tend to be either prehistoric equids smaller than modern equids, for which smaller extant artiodactyls could serve as a proxy, or the rhinocerotid Teleoceras, which is likely too large to generate the rib fragment preserved in the coprolite.

The coprolite rib fragment has an anteroposterior width of 9.1 mm and mediolateral thickness of 5.2 mm. Using Mitutoyo calipers to the nearest 0.01 mm, we recorded two measurements on each of 13 ribs per species: (1) the mediolateral thickness at the point where it measured 9.1 mm anteroposteriorly, and (2) the anteroposterior width at the point where it measured 5.2 mm mediolaterally (Figure 11). The 13 rib measurements per species were visualized using line plots. Species represented by lines intersecting the horizontal line that marked the corresponding coprolite rib measurement were interpreted to be close in size to the prey animal represented by the rib. Because the specimens lacked metadata including body mass, we obtained species body mass estimates from the literature.

Figure 11

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Figure 12 tracks the anteroposterior width or mediolateral thickness of each rib among the extant taxa in comparison to the corresponding measurements in the coprolite rib fragment. Gaps in the data indicate ribs that were either wider or narrower for much of their length than the two fixed measurements, and so were not measured.

Figure 12

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Given its relatively flat morphology, the coprolite rib fragment is unlikely to have come from ribs 1 or 2, which tend to be round in cross-section, despite lines representing these ribs in Figure 12 intersecting the black line marking the fragment. In general, the ribs examined begin to flatten around rib 3 or 4, and become roughly square around rib 7 to rib 10 before narrowing and rounding again into rib 11 to the end. Therefore, we focused on the species lines that intersect the fragment line only around rib 7 to rib 10.

Given the points of intersection of the species lines with the fragment line, the three ungulate species closest in size to the animal whose rib is preserved in the coprolite are the mule deer Odocoileus hemionus (45 to 150 kg), vicuna Vicugna vicugna (35 to 65 kg), and guanaco Lama guanicoe (90 to 140 kg) (Nowak, 1999; Macdonald, 2006).

All data are published either in the main manuscript or within Supplementary Information. There is no additional data.

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Author details

1. Xiaoming Wang

   1. Department of Vertebrate Paleontology, Natural History Museum of Los Angeles County, Los Angeles, United States
   2. Department of Vertebrate Paleontology, American Museum of Natural History, New York, United States
   3. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Supervision, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   xwang@nhm.org

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1610-3840

2. Stuart C White

   School of Dentistry, University of California, Los Angeles, United States

   Contribution

   Resources, Data curation, Software, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

3. Mairin Balisi

   1. Department of Vertebrate Paleontology, Natural History Museum of Los Angeles County, Los Angeles, United States
   2. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, United States

   Contribution

   Resources, Data curation, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-6633-1222

4. Jacob Biewer

   1. Department of Geological Sciences, California State University, Fullerton, United States
   2. Department of Geology, California State University Stanislaus, Turlock, United States

   Contribution

   Resources, Data curation, Validation, Visualization

   Competing interests

   No competing interests declared

5. Julia Sankey

   Department of Geology, California State University Stanislaus, Turlock, United States

   Contribution

   Resources, Data curation, Supervision, Funding acquisition, Validation, Investigation, Visualization, Writing—original draft

   Competing interests

   No competing interests declared

6. Dennis Garber

   Department of Vertebrate Paleontology, Natural History Museum of Los Angeles County, Los Angeles, United States

   Contribution

   Resources, Data curation, Funding acquisition, Validation, Visualization

   Competing interests

   No competing interests declared

7. Z Jack Tseng

   1. Department of Vertebrate Paleontology, Natural History Museum of Los Angeles County, Los Angeles, United States
   2. Department of Vertebrate Paleontology, American Museum of Natural History, New York, United States
   3. Department of Pathology and Anatomical Sciences, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, Buffalo, United States

   Contribution

   Resources, Data curation, Software, Formal analysis, Supervision, Validation, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

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