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

  1. Xiaoming Wang  Is a corresponding author
  2. Stuart C White
  3. Mairin Balisi
  4. Jacob Biewer
  5. Julia Sankey
  6. Dennis Garber
  7. Z Jack Tseng
  1. Natural History Museum of Los Angeles County, United States
  2. American Museum of Natural History, United States
  3. University of California, United States
  4. California State University, United States
  5. California State University Stanislaus, United States
  6. Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, United States
Research Article
Cite as: eLife 2018;7:e34773 doi: 10.7554/eLife.34773
12 figures, 2 videos, 2 tables and 2 additional files

Figures

(A) morphology of individual pellets in a complete assemblage of feces from a single dropping event by the extant spotted hyena, Crocuta crocuta. Adapted from ([Diedrich, 2012]:Figure 4), except for the orientation (Diedrich’s anterior/posterior orientation is counter to traditional sense of anatomy). (B) scats of extant spotted hyena (still image reproduced from a Smithsonian magazine video, available at http://www.smithsonianmag.com/videos/category/weird-science/weird-science-hyena-poop/?no128ist). (C) scats of extant grey wolf; note preservation of bone fragments and hairs (photo by Xiaoming Wang on September 21, 2016 in Xorkol Basin in southern Xinjiang Uygur Autonomous Region, China).

https://doi.org/10.7554/eLife.34773.003
LACM 158707, a complete coprolite from LACM locality 3937 (=Turlock Lake 34), Mehrten Formation, Stanislaus County, California, collected by Dennis Garber.

(A) Lateral view, top is toward distal (first dropping) end; (B) another lateral view about 90° from A; (C) another lateral view about 90° of further rotation from B; (D) 14 bone fragments (in various colors) digitally segmented within the coprolite (light grey) in the same orientation as in A; (E) close-up of an exposed bone fragment (unidentified) on C showing acid etching (flaking) on external surface. See also Video 1 to show three dimensional relationships of individual bones within this coprolite.

https://doi.org/10.7554/eLife.34773.004
LACM 158708, a complete coprolite and bones contained within, from LACM locality 3937, Mehrten Formation, Stanislaus County, California, collected by Dennis Garber.

(A) Lateral view, top is toward distal (first dropping) end; (B) another lateral view about 90° from A; (C) digitally separated individual bones (in different colors) within coprolite matrix (light grey), identical view as that of B; (D) a rotated view of a rib fragment seen in C, showing the convex (external) side, yellow and dark green shapes representing internal (toward chest cavity) and external cortical bone respectively, and yellowish brown sandwiched between the cortical bones being cancellous bone. Red arrows indicate the same protruded tip of rib fragment, and red dashed lines define the exposed outlines of a flat bone (mostly buried within coprolite matrix; dark blue piece in C shows the full extent of this bone within the coprolite). With the exception of the rib, all other bone fragments are unidentifiable. See also Video 2 and original Avizo segmentation file (web link) to show three dimensional relationships of individual bones within this coprolite.

https://doi.org/10.7554/eLife.34773.005
Rose diagram of bone orientations inside the coprolites.

Only coprolite pellets with at least eight bone fragments inside and a clear long axis are presented. (In the case of LACM 158709, see Figure 3A: although its axial dimension is similar to its diameter, its constricted distal end gives unambiguous orientation of its long axis.) Angles (0–90°) are between the long axis of the coprolite and the long axis of bone fragments in three-dimensional space (see Figure 3C for a definition of the angles). Data from Table 1.

https://doi.org/10.7554/eLife.34773.006

(A) LACM 158709 with three visible bone fragments (a1, a2, a3); (B) LACM 158710; (C) LACM 158711 with four visible bone fragments partially prepared (c1–c4); (D) LACM 158712 with two visible bone fragments partially exposed (d1, d2); (E) LACM 158713, surface cracks suggesting desiccation before burial; (F) LACM 158716 with one bone fragment partially exposed (f1); (G) left jaw of extant Eucastor tortus, compared to the fragment of coronoid process of the mandible (red arrows) of d1 in D (FMNH 64966; photo courtesy of Joshua Samuels); (H) digitally reconstructed bone (colored yellow; light grey background is coprolite matrix) of f1 in F, tentatively identified as the ventral aspect of the foramen ovale in the basisphenoid of a medium-sized mammal. Dashed red lines indicate exposed outlines of bones. All scales for coprolites are 10 mm.

https://doi.org/10.7554/eLife.34773.007
Comparison of craniodental functional morphology in Canis, Borophagus, and  Crocuta.

(A) Lower dentition homology and positions of functionally analogous bone-cracking teeth. Jaws are scaled to the same length. (B) Macrowear data from lower first molar samples of Crocuta crocuta (Sub-Saharan Africa) (data from [DeSantis et al., 2017]), Borophagus parvus (new data based on AMNH specimens from (1) Quibiris Formation, Arizona and (2) Big Sandy Formation, Arizona), and Canis lupus (new data based on AMNH specimens from Alberta, Canada). (C) Hunter-Schreger Band (HSB) enamel microstructure patterns in the upper and lower dentitions of the three carnivorans; darker shades indicate higher degree of zig-zag HSB specialization (modified from Figure 2 from [Tseng, 2011]). (D) Morphospace of relative warp (RW) axes from a geometric morphometric analysis of fossil (shaded symbols) and extant (black symbols) canid and hyaenid cranial shape, and (E) Phylogenetic relationships of borophagine canids (top) and hyaenids (bottom) plotted onto morphometric data, with Canis indicated by black triangle. Both (D) and (E) are modified from Figure 5 from Tseng and Wang (2011). (F) von Mises stress distributions in the crania during right fourth premolar bite simulations using 3-D finite element analysis, with warmer colors indicating higher stress. Crania are scaled to the same length (modified from Figure 7 from [Tseng, 2013]).

https://doi.org/10.7554/eLife.34773.012
Cranial and dental morphology of Borophagus secundus (F:AM 61640 from Edson Quarry, Marshall Ranch, Sherman County, Kansas, late Hemphillian).

A suite of features is commonly associated with bone-crushing adaptations, such as a highly vaulted forehead, shortened rostrum and associated imbrication of premolars, thickened lower jaws, broadened palate, laterally flared lower cheek teeth, differentially enlarged P4 relative to P3 and p4 relative to p3, and anterior premolars (P1-3 and p1-3) reduced to small pegs that are no longer functioning in occlusion. (A) right lateral view of skull and mandible; (B) occlusal view of upper teeth; and (C) occlusal view of lower teeth.

https://doi.org/10.7554/eLife.34773.013
Artist conception of feeding by a pack of bone-crushing dogs of the species Borophagus secundus, sister taxon of Borophagus parvus, by Mauricio Antón.

Competitive group feeding does not permit leisurely picking and choosing of meat for quiet consumption and may have been a driving force for complete utilization of carcasses. Adapted from Wang et al., 2008: figure 5.4 and with permission for reproduction by Mauricio Antón.

https://doi.org/10.7554/eLife.34773.014
Map and photo of coprolite locality.

(A) satellite image of Turlock Lake area (37°36–37'N 120°34–36'W) from Google Earth Pro, image date March 31, 2015 (Google Earth Pro (Version 7.1.5.1557), [Google Inc, 2015]); red star is approximate position of LACM locality 3937 (=Dennis Garber T-34 locality) and of LACM locality 3935 (=Dennis Garber T-32 locality). (B) LACM locality 3937, looking to the south; black ovals are approximate positions of fossil-producing horizons and that to the left is the location for coprolites; photograph by Jacob Biewer on September 5, 2015.

https://doi.org/10.7554/eLife.34773.015
Distribution of B. parvus body mass estimated from lengths of the lower first molar (carnassial) using the equation from Van Valkenburgh (1990).

The Arizona population tends to be larger in body size than the California population, which largely comprises Turlock Lake individuals.

https://doi.org/10.7554/eLife.34773.016
Rib measurement methods illustrated on half of a ribcage of Eld’s deer (Cervus eldi).

Anterior ribs are to the right; posterior, to the left. For this set of measurements, the colored tags mark where each rib measures 9.1 mm in anteroposterior width. The corresponding mediolateral thickness at the marked points were then recorded. Ribs without a colored tag were either wider or narrower for much of its length than the two fixed measurements of coprolite width and thickness.

https://doi.org/10.7554/eLife.34773.017
Rib measurements per species.

The horizontal black line in both plots indicates the corresponding measurement for the coprolite rib fragment. (A) Anteroposterior width of the rib where it has a mediolateral thickness of 5.2 mm, the rib fragment thickness. (B) Mediolateral thickness of the rib where it has an anteroposterior width of 9.1 mm, the rib fragment width.

https://doi.org/10.7554/eLife.34773.018

Videos

Video 1
LACM 158707 movie: A video of microCT scan of LACM 158707 with variously colored bones digitally segmented within the coprolite.

Video in Avizo Lite 9.2 by Stuart C. White.

https://doi.org/10.7554/eLife.34773.009
Video 2
LACM 158708 movie: A video of microCT scan of LACM 158708 with variously colored bones digitally segmented within the coprolite.

Video in Avizo Lite 9.2 by Stuart C. White.

https://doi.org/10.7554/eLife.34773.010

Tables

Table 1
Measurements of coprolites and their included bones.

Maximum diameter and length of coprolites are measured by digital calipers, and the rest are calculated by Avizo software. ‘*' in coprolite diameter and length indicates incomplete dimensions due to damage.

https://doi.org/10.7554/eLife.34773.008
Coprolite dimensionsBone dimensions
LACM catalogue numberMaximum diameter × length (mm)Coprolite volume (mm3)Matrix volume (mm3)Matrix fractionBone fragments containedBone max length (mm)Bone max width (mm)Bone orientation (degrees)Bone volume (mm3)Bone fraction/coprolite
15870624.6* × 31.9*58715871100%None
15870731.2 × 47.2185081782396%Bone_18.16.670155
Bone_216.55.12456
Bone_310.67.88207
Bone_46.15.17023
Bone_54.64.66326
Bone_67.97.21043
Bone_73.62.43211
Bone_811.44.71245
Bone_95.51.7853
Bone_104.72.8405
Bone_1111.02.2688
Bone_128.54.84378
Bone_135.03.95810
Bone_146.13.63714
Total bone6854%
15870824.9 × 44.610184881487%Bone_13.02.1213
Bone_211.14.41525
Bone_316.110.014344
Bone_45.63.43911
Bone_5 Cortex8.37.76114
Bone_5 Marrow9.76.861104
Bone_65.13.44911
Bone_74.32.1706
Bone_8 Rib long31.07.046156
Bone_8 Rib Marrow30.18.246574
Bone_8 Rib short29.48.746122
Total bone137013%
15870927.1 × 23.46556634197%Bone_112.52.36521
Bone_27.94.58045
Bone_312.64.42453
Bone_46.62.34510
Bone_55.02.25410
Bone_63.61.9725
Bone_76.14.51128
Bone_810.64.98142
Total bone2143%
15871021.3 × 26.640664066100%None
15871129.1* × 31.2*117411125196%Bone_116.97.1197
Bone_218.76.393
Bone_36.83.013
Bone_413.17.1169
Bone_56.53.718
Total bone4904%
15871229.4 × 27.5*8284801297%Bone_121.312.337234
Bone_213.23.16718
Bone_37.12.527
Bone_43.41.9182
Bone_58.62.87512
Total2723%
15871327.5 × 25.6*8694845497%Bone_115.26.526107
Bone_210.48.744114
Bone_34.71.9665
Bone_44.92.77214
Total bone2403%
15871417.7* × 20.9*1570150896%Bone_18.25.229624%
15871518.0* × 24.0*2481244398%Bone_171392%
15871620.5* × 14.9*1245119796%Bone_110.29.070484%
15871718.7* × 19.6*1424107175%Bone 118.912.71435325%
Total76851Total37735%
Table 2
Postcranial specimens used to approximate prey body size based on dimensions of the coprolite rib fragment.
https://doi.org/10.7554/eLife.34773.011
FamilyGenusSpeciesSpecimen number
AntilocapridaeAntilocapraamericanaLACM 30482
TayassuidaeTayassupecariLACM 86904
CamelidaeLamaguanacoeLACM 31328
CamelidaeVicugnavicugnaLACM 54706
CervidaeCervusaxisLACM 529
CervidaeCervusdamaLACM 30452
CervidaeCervusdamaLACM 30876
CervidaeCervuseldiLACM 86095
CervidaeCervusnipponLACM 31069
CervidaeCervusporcinusLACM 85966
CervidaeCervustimorensisLACM 86012
CervidaeOdocoileushemionusLACM 307
CervidaeOdocoileushemionusLACM 30903
CervidaeOdocoileusvirginianusLACM 52442

Data availability

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

Additional files

Supplementary file 1

158708 bin=4 Avizo file (plus data folder): Segmentation file for LACM 158708 in Avizo software (ThermoFisher Scientific).

Voxel size has been downgraded to 108 micrometers on a side to reduce file size. Segmentation in Avizo Lite 9.2 by Stuart C. White.

https://doi.org/10.7554/eLife.34773.019
Transparent reporting form
https://doi.org/10.7554/eLife.34773.020

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