Chewing, dentition and tooth wear in Hippopotamidae (Hippopotamus amphibius and Choeropsis liberiensis)

Among mammals, hippopotamids (‘hippos’) have been described as the species with the lowest chewing efficacy despite elaborate enamel folds on the occlusal surface or their cheek teeth, which was hypothesized to result from the lack of a grinding chewing motion. We investigated the chewing and dentition of the two extant hippo species, the common hippo (Hippopotamus amphibius) and the pygmy hippo (Choeropsis liberiensis), making (video) observations of live animals and gathering data on museum specimens (n = 86 H. amphibius and 26 C. liberiensis skulls). Hippos have a low degree of anisodonty (differences in width between maxillary and mandibular cheek teeth) and anisognathy (difference in width between the upper and the lower jaw), corresponding to a mainly orthal (up-and-down) chewing motion. The two hippo species differ slightly, but distinctively, in their anterior dental morphology and chewing mode. In both species, the canines do not completely prevent a lateral jaw movement but would, in theory, permit this movement until the mandibular canines get into contact with the maxillary protruding snout. This movement is only realized, to a small extent, in pygmy hippos, leaving distinct wear traces on their incisors and creating relatively wider wear facets on the maxillary canines. In common hippos, the interlocking upper and lower incisors prevent lateral jaw movement. Corresponding contact wear facets are evident on the medial aspect of the upper, and on the lateral aspect of the lower incisors–unless museal reconstructions mispositioned these teeth. If these facets are interpreted as an indication for a relic of a lateral jaw movement that was probably more prominent in hippo ancestors, i.e. if we assume that hippos evolved orthal chewing secondarily, several other characteristics of hippos can be explained, such as a low degree of hypsodonty (in the absence of distinct attrition due to a grinding chewing movement), a secondary loss of complexity in their enamel schmelzmuster, a secondary evolution of a wide mouth gape, a reduction in anisodonty compared to their ancestors, and the evolution of a bilaterally symmetrical (‘trifoliate’) enamel folding pattern on the molar occlusal surface from an ancestral bunoselenodont condition. As an underlying driving force, selection for intraspecific combat with canines and incisors, necessitating a wide gape and a rigid jaw, has been suggested.


Supplementary text: age dependence, cranium and mandible width, eruption sequences
With age, the length of the skull and the mandible increased (Fig. S23-S24).Both measures were tightly related to each other, but in the relationship with age, there was a dichotomy in common hippos (Fig. S23-S24).This dimorphism was also evident in the length of the incisors (Fig. S25) and the canines (Fig. S26).While it is tempting to ascribe this to sexual dimorphism, the few specimens of known sex do not unambiguously support this notion, in line with the general observation that sexual dimorphism, though present, is not very pronounced in common hippos [1].Rather, the results support the notion that growth in hippos is very variable, as was reported for their canines by Matthes [2].
When comparing maxilla or mandible width to the width of anterior teeth or the space between the anterior teeth, most scaling relationships for the cranium included linearity within common hippos and across the two species, whereas for the mandible, the sum of anterior tooth width increased more-than-linearly with mandible width in common hippos whereas the space between the anterior teeth nearly stayed constant across body sizes; across both species, the tooth width scaling did not exclude linearity, but that of the interdental spaces was below linearity (Fig. S27).This indicates that in common hippos, the lower first incisors and/or canines increase with positive allometry with mandible width.
The dental anatomy of the deciduous teeth and the eruption pattern of the permanent teeth in the common hippo have been published for the lower jaw [3,4].More recently, the full eruption sequence for common and pygmy hippos have been published in the supplementary material of Gomes Rodrigues et al. [5].

Choreopsis liberiensis
Upper jaw: dc Here, we describe our observations regarding the upper jaw for the common hippo.We noticed that the dp 4 is replaced later by the permanent tooth than the dp4.While the dp 4 was still present, the P4 was already in place.While the dp4 has three cusps and is therefore longer than its single-cusped successor, the dp 4 has only two cusps and resembles the molar teeth.In Fig. S30, the transition of the deciduous to the permanent dentition of the upper fourth premolar is visible.
The same pattern of an accelerated tooth replacement in the lower jaw could be observed in the eruption pattern of the second and third molar.They usually appear first in the lower jaw and only later in the maxilla.In conclusion, odontogenesis seems to be accelerated in the lower jaw.
Combining molar occlusal area with the dental age categories, it is evident that younger individuals of the common hippo that are still undergoing odontogenesis exhibit an overall smaller molar area, because the second and the third molar tooth erupt with a more advanced age (Fig. 16).

Supplementary text: deciduous dentition
The dental formula for the milk teeth in the common hippo is: di 2/2, dc 1/1, dp 4/4.The deciduous first incisors and canines are usually erupted at birth, in contrast to the premolars [3,4].The deciduous canines and incisors are similar regarding their dental anatomy, having a peg-like shape and rounded tips.They reach a length of about a centimeter.The canines are shed at around 14 months.Around the time the deciduous canine sheds, the surrounding bone is being suppressed and the permanent tooth erupts slightly behind its predecessor [4].The first and second incisors are lost at around 1 1/3 and 2 1/2 years of age, respectively.
At around five months the first three deciduous premolars have erupted in both jaws.The fourth premolar follows shortly after, first in the mandible, then in the maxilla (see above).The deciduous premolars, except the first one, are each replaced by a permanent tooth.The first one is not present in every individual and only persists for a varying amount of time [3].
The first premolar usually has only one root, but two may occur [6], and a single cusp.The second deciduous premolar also only has one cusp.The third deciduous mandibular premolar has one main cusp and a pair of smaller cusps behind the former (Fig. S31).In the maxilla, it consists of two single cusps with a pair of cusps following, which results in an increased tooth width in the posterior direction (Fig. S32).
In the mandible, the deciduous fourth premolar dp4 shows three pairs of cusps behind each other, and the outer cusp of the second pair is the most prominent one [4] (Fig. S33).The cusp width increases in the posterior cusps (Fig. S16), which gives the tooth a slight triangular shape (Fig. S33).In the permanent dentition the number of cusps is reduced to one (Fig. S34).
In the maxilla, the deciduous fourth premolar dp 4 consists of one small, sometimes missing, anterior cusp with two pairs of cusps following, the most outstanding one being the antero-external cusp [4] (Fig. S35).The permanent P 4 consists of only one cusp (Fig. S36).
The pygmy hippo has a very similar dentition regarding the dental anatomy, but only one pair of the lower milk incisors are replaced by permanent teeth (Fig. S37-S38).
Table S1.Summary of the different age categories correlating with the different teeth patterns in the Hippopotamus amphibius defined by Laws [3]."Exposed" means protruding above gum level."Open" means that the tooth is visible in its alveolus, but not protruding above bone level.D is used for a deciduous tooth, I = Incisor, C = Canine, P = Premolar, M = Molar [7] Figure S1 Ventrodorsal view of an upper skull of an adult common hippo (Hippopotamus amphibius).The orange arrow marks the measured distance between the Processus palatinus ossis incisivi and the Os occipitale, the green arrow illustrates the measured distance between the Processus palatinus ossis incisivi and the Os palatinum.Photo: Annika Avedik.

Figure S23
Comparison of the upper skull length and the age category from Laws [3] in hippos (Hippopotamus amphibius, Choeropsis liberiensis).

Figure S24
Comparison of the mandible length and the age category from Laws [3] Figure S2 (A) Lateral view of an adult common hippo (Hippopotamus amphibius) skull.We determined the length of the mandible by measuring the length between the Ramus mandibulae and the cranial margin of the Corpus mandibulae (yellow arrow).(B) Frontal view of an adult Hippopotamus amphibius skull.We measured the distance between the upper (blue arrow) and lower canines (green arrow).Photos: Michelle Aimée Oesch.

Figure S3 Figure S4
Figure S3Dorsal view of the lower incisors of a common hippo (Hippopotamus amphibius).We measured the length from the tooth alveolus to the tip of the tooth on the lingual (light blue arrow) and the mesial (dashed dark blue arrow) side of the tooth.The width of the incisors was determined at the base of the tooth (purple arrow).We determined the length between the tooth alveolus and the wear facet (light green arrow).The length (pink arrow) and the width (yellow arrow) of the wear facet was measured, as well as the distances between the incisors.Photo: Annika Avedik.

Figure S5
Figure S5 Dorsoventral view of the lower anterior dentition of a common hippo (Hippopotamus amphibius).We measured the basal tooth width (dark blue arrow), the lingual tooth length (dark green arrow), the facet width (yellow arrow) and length (pink arrow).Photo: Annika Avedik.

Figure S7 .Figure S8
Figure S7.Macrowear scoring table designed to quantify tooth wear of the premolar and molar teeth in the common hippo (Hippopotamus amphibius).Based on the drawings of Laws[3], with some modified or added wear stages.

Figure S9
Figure S9Fronto-lateral view of a semi-opened skull of a common hippo (Hippopotamus amphibius).The canines are not fully positioned in their alveoli (possibly to create a more impressive display), preventing the closing of the skull.Note the abnormally growing right I 2 , and the typical wear facets on the I 1 and I1.Photo: Michelle Aimée Oesch.

Figure S10
Figure S10 Dorsoventral view of the lower incisors of a common hippo (Hippopotamus amphibius).The wear facets of both lower incisor pairs are facing the wrong direction due to museal mispositioning.Photo: Annika Avedik.

Figure S11 Figure S12 Figure S13 Figure S14 Figure S15
Figure S11 Frontal view of live of a common hippo (Hippopotamus amphibius), showing the position of the wear facets of the lower and upper incisors.Photo: Brian Stefanski.

Figure S16 Figure S17 Figure S18 Figure S19 Figure S20 Figure S21
Figure S16Comparison of cusp width in the common hippo (Hippopotamus amphibius) maxillary and mandibular deciduous p4.The line denotes y = x.

Figure S22
Figure S22Comparison of the mandible and maxilla width, measured at the level of the canines in hippos (Hippopotamus amphibius, Choeropsis liberiensis).The line denotes y = x.

Figure S30
Figure S30Deciduous tooth replacement of the upper fourth premolar in a common hippo (Hippopotamus amphibius).On the left side, the single-cusped permanent P 4 is visible, while on the right side the permanent P 4 has erupted halfway, while the p 4 is still present.Photo: Annika Avedik.

Figure S31
Figure S31The mandible of a juvenile Hippopotamus amphibius.The deciduous second incisors and first three premolars are present, while the first incisors and canines have already been replaced by the permanent teeth.On both sides, the first molars are protruding just above the bone level.Photo: Annika Avedik.

Figure S32
Figure S32 Maxilla of a juvenile Hippopotamus amphibius.The milk dentition of the left incisors and first four premolars is visible.The incisors on the right side and both the canines are already replaced by the permanent dentition.The first molars are visible below the bone level, not yet protruding.Photo: Annika Avedik.

Figure S33
Figure S33 Mandible of a juvenile Hippopotamus amphibius, with a partial milk dentition.Photo: Annika Avedik.