NIMRAVIDAE, Cope, 1880

Therrien, François, 2005, Feeding behaviour and bite force of sabretoothed predators, Zoological Journal of the Linnean Society 145 (3), pp. 393-426 : 403-406

NIMRAVIDAE , CARNIVORA

Nimravids had a Holarctic distribution and are found in deposits dating from the late Eocene to the earliest Miocene ( Fig. 1 ) ( Martin, 1989, 1998a; Bryant, 1996b; Peigné et al., 2000; Peigné, 2003). Until recently nimravids were considered to include two distinct, monophyletic lineages, the Paleogene Nimravinae and the Miocene Barbourofelinae, even though the chronostratigraphic range of the two taxa did not overlap ( Bryant, 1991; Peigné, 2003). However, new discoveries have revealed that ‘barbourofelines’ are more closely related to felids than to other nimravids ( Morales et al., 2001; Peigné & Bonis, 2003; Morlo, Peigné & Nagel, 2004; see below). Nimravids consist of a paraphyletic assemblage of scimitar-toothed ecomorphs ( Dinictis felina , Pogonodon platycopis and Nimravus brachyops are studied) and the monophyletic dirk-toothed Hoplophoneini ( Hoplophoneus primaevus , H. occidentalis , H. dakotensis and Eusmilus cerebralis are studied) ( Bryant, 1996b; Peigné, 2003). Although its upper canine morphology qualifies it as scimitar-toothed, N. brachyops has relatively shorter upper canines, stouter lower canines and exhibits only incipient sabretooth adaptations (e.g. Toohey, 1959; Scott, 1962); its position, along with the sole conical-toothed nimravid Dinaelurus , as the sister taxon to all other nimravids suggests that it may be close to the ancestral (i.e. basal) nimravid condition ( Bryant, 1996b; Peigné, 2003).

Mandibular force profiles

Among nimravids, two distinct patterns, corresponding to the scimitar-toothed and dirk-toothed ecomorphs, emerge from the dorsoventral and labiolingual mandibular force profiles ( Figs 6, 7 ). Although members of both ecomorphs exhibit a decrease in dorsoventral and labiolingual force values between post-M 1 and P 3 P 4, they differ mainly by their mandibular crosssectional properties at the canine. Dirk-toothed nimravids are characterized by a symphyseal region slightly stronger dorsoventrally than the corpus at the carnassial, the symphysis being much stronger than at the premolars (P 3 P 4; Fig. 6). Labiolingually, the symphyseal region is still stronger than at the premolars but is weaker than at the carnassial, except in Eusmilus cerebralis . In contrast, the symphyseal region of scimitar-toothed nimravids is much weaker, both dorsoventrally and labiolingually, than the corpus at the carnassial ( Fig. 7 ). The symphysis is only slightly stronger than at the premolars (P 3 P 4), a condition reminiscent of that observed in extant canids ( Fig. 4) (Therrien, 2005). A smaller, presumably less mature Dinictis felina individual (YPM 13587; see Bryant, 1996b) is characterized by a symphyseal region weaker than the corpus at P 3 P 4. Finally, N. brachyops differs from other scimitar-toothed sabretooths in having higher postcarnassial Zx / L and Zy / L -values and a labiolingually stronger symphyseal region.

The ecomorph dichotomy among nimravids is also recognizable in the relative mandibular force profiles (Zx / Zy, Figs 6, 7 ). Whereas the shape of the mandibular ramus tends to remain the same among scimitar-toothed nimravids (Zx / Zy = 2.00), it deepens anteriorly in dirk-toothed nimravids, as indicated by the increasing Zx / Zy values. Although the symphyseal region in both ecomorphs is strongly buttressed against dorsoventral loads, having minimal Zx / Zy canine values of 2.37 (excluding N. brachyops ), dirk-toothed nimravids have significantly higher Zx / Zy canine values than scimitar-toothed nimravids (P <0.006, P <0.04 without Nimravus ). The mandibular force profile of N. brachyops is generally similar to that of other scimitar-toothed nimravids, but it differs markedly in having a symphyseal region much better adapted towards labiolingual and torsional loads (Zx / Zy canine = 1.89), similar to the condition observed in the extant Neofelis nebulosa ( Fig. 4) (Therrien, 2005).

Interpretation

Again assuming similarity of cortical bone thickness and of safety factors, nimravids are shown to have been able to generate bite forces equal to or even greater than felids of similar mandibular length ( Table 1). For example, at the carnassial (P 4 M 1 interdental gap), Pogonodon platycopis had a maximum bite force 10% superior to Panthera pardus and the bite of Hoplophoneus primaevus was 66% more powerful than that of Acinonyx jubatus .

The difference in mandibular force profiles between ecomorphs indicates that dirk-toothed and scimitartoothed nimravids killed their prey differently. The dorsoventrally and labiolingually stronger mandibular symphysis of dirk-toothed nimravids demonstrate that greater loads were exerted on the anterior extremity of the mandible than in scimitar-toothed nimravids, suggesting that the former may have emphasized the canine bite as a means to subdue their prey. With their elongate sabres and inferred ambush predatory style, dirk-toothed nimravids may have delivered powerful canine bites, driving the sabres deep into their prey to kill it quickly. Consequently, the symphysis had to be reinforced dorsoventrally and labiolingually to sustain the localized stresses generated during the bite. In contrast, the close similarity of the mandibular force profiles of scimitar-toothed nimravids to those of canids suggests they may not have relied on a single, powerful canine bite to kill their prey. Instead, these cursorial sabretoothed predators probably pursued their prey and delivered slashing canine bites to weaken it, their short, coarsely serrated sabres proving ideal for that purpose (e.g. Martin, 1980). The weaker symphyseal region of the smaller D. felina individual suggests that it may have hunted slightly smaller prey than its larger and older conspecifics.

The relatively uniform Zx / Zy profile near the cheek teeth in scimitar-toothed nimravids ( Fig. 7 ) indicates that the shape of the mandibular ramus remains constant throughout its length. The constancy of the Zx / Zy ratio reflects a feeding behaviour in which the ramus was not adapted for high-load applications, such as bone-cracking, but for the unique purpose of slicing flesh as seen in conical-toothed felids (see Therrien, 2005). The anteriorly increasing Zx / Zy values along the mandibular ramus in dirk-toothed nimravids ( Hoplophoneini ; Fig. 11 ) indicate that the ramus becomes relatively deeper towards the symphysis and, thus, that dorsoventral stresses become increasingly more important.

All nimravids, except for N. brachyops , have strongly dorsoventrally buttressed mandibular symphyses compared to conical-toothed felids, with minimum Zx / Zy canine values of 2.37 for Eusmilus cerebralis and maximum values of 4.15 in Hoplophoneus dakotensis . This adaptation suggests that torsional stresses and the unpredictability of load orientation, such as those produced by struggling prey, must have been greatly reduced when sabretoothed nimravids delivered canine bites. In other words, prey must have been restrained and offered relatively little resistance when the sabretooths employed their sabres or else the symphysis would have been better adapted to withstand labiolingual and torsional stresses.

Dorsoventral force Labiolingual force Relative force (Log Zx/L) (Log Zy/L) (Zx/Zy)

Interestingly, the Zx / Zy canine values of hoplophoneines are significantly higher than those of scimitartoothed nimravids, suggesting that the former may have been better at immobilizing their prey. Given that dirk-toothed sabretooths had limbs as robust as those of bears while scimitar-toothed nimravids had less robust limbs more typical of cursorial predators ( Anyonge, 1996), mandibular stresses may not have been as well constrained within the sagittal plane during bite in scimitar-toothed nimravids, thus requiring

Dorsoventral force Labiolingual force Relative force (Log Zx/L) (Log Zy/L) (Zx/Zy)

1.04 1.46

Dinictis felina (L = 11.21 cm)

Dinictis felina (subadult; L = 9.54 cm)

Pogonodon platycopis (L = 14.65 cm)

Nimravus brachyops (L = 14.69 cm) a mandibular symphysis adapted for this possibility. Nevertheless, the Zx / Zy canine values of scimitar-toothed nimravids are much higher than in conical-toothed felids, indicating that labiolingual and torsional stresses were still significantly lower. As in cheetahs ( Eaton, 1970; Schaller, 1972), scimitar-toothed nimravids could have destabilized and restrained sufficiently their prey, especially with the aid of their robust incisor battery (Biknevicius et al., 1996), in order to greatly reduce torsional stresses for the sabres to be used safely.

Nimravus brachyops , the scimitar-toothed nimravid with incipient sabretooth morphology, differs from other nimravids in having a significantly rounder mandibular symphysis (Zx / Zy canine = 1.89, P <0.01 from all nimravids, P <0.09 from scimitar-toothed nimravids). These lower Zx / Zy canine values reveal that torsional loads induced by struggling prey were relatively more important during canine bite, but not to the extent observed in most modern felids. This suggests that N. brachyops killed in a fashion intermediate between that of conical-toothed carnivorans and full-fledged sabretooths. In fact, the Zx / Zy profile of N. brachyops is very similar to that of Neofelis nebulosa and, to a lesser degree, machaeroidines ( Figs 4, 5 ). Although the details of their dorsoventral and labiolingual force profiles reflect differences in hunting behaviour and possibly phylogeny, the intermediate Zx / Zy canine values of these taxa suggest that their killing behaviour may have been similar: a canine bite delivered on a partially immobilized prey of larger size than the predator (see Discussion).

Figures

Figure 1. Phylogeny and temporal range of sabretooth genera studied. Ischyrosmilus gracilis (sensu Churcher, 1984) is included in the Smilodon lineage (probably equivalent to S. gracilis). Although this taxon was not studied, Megantereon is presented to complete the Smilodontini tribe. Based on Goin & Pascual (1987), Bryant (1996b), Turner & Antón (1997), Gunnell (1998), Peigné (2003), and Morlo et al. (2004).

Figure 5. A, mandibular force profiles of machaeroidines. Values are presented for the canine, P3P4, and M1M2 interdental gaps. Zx/L-values at the canine are higher than those at M1M2, suggesting a powerful canine killing bite. B, comparison of bending strengths (section moduli Zx and Zy) in Machaeroides eothen and M. simpsoni. The missing segments of M. eothen (USNM 361372) and M. simpsoni are reconstructed on the basis of M. eothen (USNM 17059). The symphyseal region of all specimens is much stronger than the ramus. The Zx/Zycanine values of machaeroidines are similar to those of felids with special killing techniques.

Figure 7. Mandibular force profiles of scimitar-toothed nimravids. Values are presented for the canine, P3P4, and post-M1 interdental gaps. Zx/L-values at the canine are lower than those at post-M1, suggesting shallower bites than dirk-toothed nimravids. No increase in dorsoventral buttressing occurs in the vicinity of the cheek teeth, indicating that the mandibular ramus is adapted for slicing meat exclusively. The Zx/Zycanine values of scimitar-toothed nimravids, to the exception of Nimravus brachyops, are much higher than those of extant felids, suggesting that prey was restrained prior to the sabre bite. The Zx/Zycanine values of N. brachyops are relatively lower, being similar to those of the extant felid Neofelis nebulosa.

Figure 11. Mandibular force profiles of thylacosmilines. Values are presented for the canine, P3P4, M1M2, and post-M4 interdental gaps. Zx/L-values at the canine are higher than those at post-M4, suggesting a powerful canine killing bite. No increase in dorsoventral buttressing occurs in the vicinity of the cheek teeth, indicating that the mandibular ramus is adapted for slicing meat exclusively. The Zx/Zycanine values are much higher than those of extant felids, suggesting that prey was restrained prior to the sabre bite. The higher Zx/Zycanine values of the juvenile relative to the adult are reminiscent of the situation observed in juvenile Panthera leo. Consequently, it is possible that young thylacosmilines underwent an extended period of parental care.