Tarsal morphology of ischyromyid rodents from the middle Eocene of China gives an insight into the group’s diversity in Central Asia

Systematic paleontology

Order Rodentia Bowdich, 1821³¹

Family Ischyromyidae Alston, 1876³²

Genus Asiomys Qi, 1987³³

Asiomys dawsoni Qi, 1987³³

Figure 3A–E

Material. Fragment of right calcaneus (IVPP V24417), early Middle Eocene, Huheboerhe, Irdin Manha Formation, Erlian Basin, China.

Description. The bone is damaged and most probably that of a juvenile as it shows loss of the tissue in the extremities of the bone such as the calcaneal tuber and calcaneal eminence, which are usually less calcified in juveniles. The bone is relatively large (Table 1), with an elongated calcaneal tuber and a relatively short body (Fig. 3A–D). The sustentaculum tali is partly damaged; it has a subcircular articulation facet, which was probably more extended craniocaudally than mediolaterally. The caudal margin of the sustentaculum tali is inclined cranially, similar to the condition seen in species A and more than in species B (Fig. 3A). The sustentacular facet overlaps about one-half of the craniocaudal reach of the ectal facet. The groove for the ‘spring ligament’ (sensu Szalay and Decker³⁴), which runs along the medial edge of the sustentaculum tali, is poorly pronounced. Likewise, the calcaneal groove for the tendon of the flexor fibularis muscle is shallow and poorly marked, most probably due to poor preservation. The ectal facet is relatively wide and similarly shaped as in species B (below). The peroneal process is completely damaged.

The calcaneal tuber is strongly compressed, but it resembles in shape those of species A and B. A long groove for the calcaneofibular ligament is impressed on its lateral side.

The anterior plantar tubercle is large and swollen, similar to that in species A, and touches the brim of the calcaneocuboid surface. The latter, only slightly damaged laterally, is round in outline, without a distinct pit, and inclined about 20–30°.

Systematic remark: The fossil was associated with Asiomys dentition found in the same spot. We attribute specimen IVPP V24417 to Asiomys dawsoni, based on this fact and its distinctive size (Asiomys being the largest rodent in the assemblage). Asiomys is the only ischyromyid rodent known from the basal strata of the Irdin Manha Formation of Huheboerhe.

Genus indet.

Species A

Figure 3F–K

Material. Right calcaneus (IVPP V24416), early Middle Eocene, Irdin Manha Escarpment, Irdin Manha Formation, Erlian Basin, China.

Description. The right almost complete calcaneus of an adult specimen is relatively large (Table 1), comparable in length to the calcaneus of a coypu (Myocastor coypus) or Asiatic brush-tailed porcupine (Atherurus macrourus). The bone has a characteristically elongated calcaneal tuber and rather short body (Fig. 3F–I). The calcaneal tuber is quite slender in comparison with the structure found in the coypu and porcupines. The shape of the bone resembles most closely the calcaneus of Paramys wortmani (see³⁵: Fig. 12B), although in Paramys the calcaneal tuber is more compressed mediolaterally.

The sustentaculum tali is large and eminent, reaching far medially and tapering, although its medial end forms a blunt edge parallel to the long axis of the bone. This medial edge also bears a well-marked but not deep groove of the calcaneonavicular (or ‘spring’) ligament (Fig. 3G). The sustentacular facet (facies articularis talaris media in Fostowicz-Frelik³⁶: Fig. 12B2) is round, with only slight anteroposterior compression. It occupies almost the whole dorsal surface of the sustentaculum, encroaching slightly onto the calcaneal body. In that it differs from Notoparamys and Paramys wortmani, which both have a much more medially placed sustentacular facet, which does not encroach on the calcaneal body. The range of the sustentacular facet overlaps less than one-third of the ectal facet (posterior facies articularis talaris in Fostowicz-Frelik³⁶: Fig. 12B2) on its anterior and medial sides. The calcaneal eminence is slightly longer than that in Marmota and Sciurus, in proportions closer to that of porcupines and of similar size as in Paramys wortmani. The ectal facet is wide, long, and has a distinctly helical course, even more strongly marked than in North American ischyromyids (see Rose and Chinnery³⁵: Fig. 12A). It is, however, inclined more strongly mediolaterally than in Notoparamys and Paramys, and faces strongly medially. On the dorsal side of the calcaneal eminence, posterolateral to the ectal facet, there is a flattened rough area (finely pitted), marking the place of attachment of the lateral collateral ligaments binding the distal fibula and the astragalus with the calcaneus and stabilizing the astragalocalcaneal joint.

A calcaneal body is short and stocky with poorly marked tendon ridges at the dorsal surface. A large peroneal process is partly damaged at its lateral margin. The process is placed closer to the cuboid surface than the sustentaculum tali. The position of the sustentaculum tali and the proportions of the calcaneal body of specimen IVPP V24416 resemble rather closely the calcaneus of Paramys wortmani (see³⁵).

The calcaneal tuber is not ‘pinched’ at its dorsal side but moderately compressed, thus there is no coracoid ridge posterior to the ectal facet. At the lateral side of the tuber, there is a long groove for the calcaneofibular ligament running askew, towards the dorsal surface of the calcaneal tuber. The groove for the calcaneofibular ligament is more weakly expressed than in the North American paramyines and arboreal sciurids, but similar to that of Marmota.

The caudal surface of the calcaneal tuber is subcircular (only slightly more extended dorsoplantarly than mediolaterally, see Fig. 3 and Table 1). The groove for the calcaneal tendon (= Achilles tendon) is deep and placed asymmetrically at the surface (Fig. 3J). Also, the medial process of the calcaneal tuber is much better developed and extending medially.

The plantar surface of the bone is almost straight with a delicate flexure cranially to a well-developed plantar heel process (Fig. 3G). The anterior plantar tubercle is relatively large, swollen, but shifted medially, towards the sustentaculum tali. It is placed very close to the cuboid surface, almost touching its margin; such location and the medial shifting resembles the condition in some ground squirrels, e.g., Cynomys (see Fostowicz-Frelik et al.⁸: Fig. 3D–F). The anterior plantar tubercle is also somewhat flattened and inclined medially and forms a well-marked calcaneal groove for the tendon of the flexor fibularis muscle.

The calcaneocuboid articular surface is semicircular, slightly wider mediolaterally than long dorsoplantarly, which distinguishes species A from Marmota and paramyines (see³⁵). It is almost transversally positioned, not inclined, as in most of the rodent taxa (coypu and porcupines included), and gently concave; it is also confluent and level with the cuboid pit, forming one round surface at the cranial end of the bone.

Genus indet.

Species B

Figure 3L–Q

Material Right calcaneus (IVPP V24418), early Middle Eocene, Daoteyin Obo, Irdin Manha Formation, Erlian Basin, China.

Description The bone is complete, slightly larger than in species A (Table 1), matching in length the calcaneus of the coypu. Its overall structure is very similar to the calcaneus of Paramys (either P. wortmani or P. taurus, see Rose and Chinnery³⁵: Fig. 12B, C). It has a long and strong calcaneal tuber and a relatively strong but short calcaneal body (Fig. 3L). The tuber is more compressed mediolaterally than in species A; thus, the caudal surface of the tuber is extended more dorsoplantarly than mediolaterally (Fig. 3P). The attachment for the calcaneal tendon forms a rounded concavity at the caudal side of the tuber, and is more horizontally and symmetrically located at the surface than in species A. The lateral surface of the calcaneal tuber bears a marked scar from the calcaneofibular ligament, although the scar is convex, not concave as in species A and in other compared taxa (e.g., Cynomys).

The sustentaculum tali is large and round; it is located relatively close to the calcaneal body, not extending as far medially as in the North American paramyines (see³⁵). It is slightly longer anteroposteriorly and located more caudally (closer to the ectal facet) than in species A. Thus, the sustentacular surface overlaps ca. one-half of the cranial part of the ectal facet. The medial edge of the sustentacular shelf bears a deep groove for the ‘spring ligament’.

The ectal facet is large, equally wide throughout its length, long and helical, although its course is straighter along the proximodistal direction than in species A. The ectal surface faces mediodorsally, with a slightly weaker medial component than in species A. The dorsal surface of the tuber, just caudal to the ectal facet, is not typically ‘pinched’ into a sagittally oriented crest, but it is, nevertheless, more mediolaterally compressed than in the species A, similar to Marmota.

The calcaneal body forms about one-third of the bone length. Its dorsal surface is carved by deep longitudinal marks indicating the position of the extensor digitorum brevis muscle (Fig. 3). A middle-size peroneal process is located cranially at the calcaneal body. It is strong and long anteroposteriorly, reaching almost the edge of the calcaneocuboid surface. Its lateral edge shows a deep groove for the tendon of the peroneus longus muscle, while its dorsal surface forms a groove for the peroneus brevis muscle tendon (Fig. 3). Species B differs from the ground squirrels in the shape and location of the peroneal process, which is less extended laterally in species B than e.g., in marmots, although it is relatively much larger than in the coypu and porcupines.

The anterior plantar tubercle looks less swollen than in species A; it is located at the very margin of the calcaneocuboid surface and as in species A is shifted medially (Fig. 3O, Q). The calcaneocuboid surface is slightly inclined (ca. 25°) anteromedially, which distinguishes the bone from species A, Marmota, and Notoparamys, which all have the calcaneocuboid facet almost transversal and perpendicular to the long axis of the calcaneus. In this respect, the calcaneocuboid surface resembles more closely the calcaneus of Paramys taurus (Rose and Chinnery³⁵: Fig. 12C). The calcaneocuboid surface is almost round, slightly wider mediolaterally, resembling that of species A. A relatively small calcaneal pit (extending only to a half of the anterior plantar tubercle base, see Fig. 3Q), smaller but deeper than in species A, forms a shallow sink at the medial side of the surface, cranially to the sustentaculum tali.

PCA analysis

A Principal Component Analysis (PCA) was performed based on 14 measurements of the calcaneus. The analysis included the calcaneal measurements of five ischyromyid species (two described here as species A and B, and three comparative species from North America) and 16 extant large rodent species (Supplementary Table S1). The extant taxa represent six basic types of locomotor adaptations found in rodents: ambulatorial (terrestrial generalists), amphibious (swimming), arboreal (tree climbing), cursorial (four-pedal runners), ricochetal (bipedal jumpers), and semi-fossorial (burrowing).

Principal Components 1 and 2 (PC1 and PC2) represent 87.48% and 5.75% of the variance, respectively, whereas Principal Components 3–4 represent further 4% of the variance (Supplementary Table S2). All the variables are positively correlated with PC1 and their loadings are very balanced (Fig. 4). Thus, it implies that the PC1 represents a proxy for the size of the bone. PC2 is most strongly correlated with the length of the calcaneal body, BL (-0.86) and more weakly correlated with the width of the cuboid facet (CCW) and anterior width of the ectal facet (AEW), 0.31 and 0.21, respectively (Fig. 4). The correlation with the length of the calcaneal body is an especially important factor for estimating an animal’s vertical jumping ability; the species with elongated calcaneal bodies are generally better jumpers (see^8,36). The strong negative correlation of the length of the calcaneal body in the second component is illustrated by grouping the species with a strong jumping locomotor repertoire (e.g., squirrels and chinchillas) towards the left side of the plot (Fig. 4). Incidentally, this phenomenon does not concern the calcanei of ricochetal species (see the position of Pedetes versus that of Sciurus and Chinchilla: Fig. 4), where the mechanics of a jump are differently realized, and the stabilisation and relative stiffness of the ankle joint plays the most important role (thus, the calcaneal body and calcaneal tuber are more similar in size).

In the plot of PC1 against PC2, ischyromyids do not cluster together. Instead, the PCA morphospace is divided into two (or even three) broad groups of ischyromyid locomotor adaptations: the ambulatorial species and those with more pronounced jumping or cursorial ability. Chinese taxa fall among typically large ambulatorial rodents, such as the coypu (Myocastor) and porcupines (Atherurus and Hystrix). Closest to them there is the North American ischyromyid Quadratomus, which is somewhat shifted towards the cursorial species and can be thus distinguished as differently specialized (more cursorial). Two other North American ischyromyids, Ischyromys and Reithroparamys, are grouped with Chinchilla and Ondatra, respectively, which may imply some jumping and slightly scansorial locomotor adaptations for Ischyromys and those of typical agile generalist species for Reithroparamys.

Although the sample is limited, the results of the PCA analysis point to general differences in the structure of the calcaneus, and thus, locomotor specialisation, between Asian and North American ischyromyid species. Moreover, Asian species seem to differ less from each other than the North American ones do, reflecting the overall greater species diversity and coverage of a wider niche spectrum of the North American ischyromyids.

Functional and paleoecological implications

The studied calcanei add to our knowledge on the functional aspects of locomotion of ischyromyid rodents. Proximal tarsal morphology has been recently used to interpret the locomotor behavior of some extinct rodents (see e.g.,^8,37,38,39). In the scheme of locomotor categories of Samuels and Van Valkenburgh⁴⁰, attributions proposed for early ischyromyids fit into generally terrestrial⁴¹, arboreal⁴² or a mixture of those two³⁵.

A relatively short calcaneal body, widely spread sustentaculum tali, and a large peroneal process observed in most ischyromyid species (including these studied herein) indicate rather poor cursoriality. Instead, their ankle joint structure allows for a large freedom of foot movements in different planes. A medially extended sustentaculum tali together with a long and helically twisted ectal facet indicate a large degree of sliding between the calcaneus and astragalus along their articular facets, which makes possible a great degree of foot torsion resulting in foot eversion and inversion. This effect is further enhanced by an extended calcaneocuboid facet that is gently concave and oriented perpendicularly to the long axis of the calcaneus in species A.

Such adaptations are helpful for both clinging to branches and adjusting to uneven or inclined substrate during climbing. A great degree of freedom of movement may be helpful also during burrowing, when the hind legs are used to push forward loose soil out of a burrow or an animal is forced to maintain a crouched posture, when it digs with its forelegs and head. Nevertheless, as much as the calcaneal structure may suggest some burrowing ability in ischyromyids (see Rose and Chinnery³⁵), the rest of the postcranial skeleton known from the more complete specimens of North American representatives⁴¹ does not support fossorial adaptations. In particular, a long tail in the pre-Oligocene North American (see e.g., Paramys or Reithroparamys in Wood⁴¹: figs. 8 and 44, respectively) suggests some arboreal adaptations or at least occasional climbing, as such a tail greatly enhances balancing on uneven terrain. In contrast, typically fossorial mammals have reduced tails⁴³.

The overall morphology of dental and mandibular remains^16,18 of Asian ischyromyids is similar to that of their North American counterparts^16,19. As complete or even partial postcranial skeletons are unknown for the Asian ischyromyids, we can surmise their general locomotor adaptations based on calcaneal morphology which, although not in striking contrast with their North American counterparts, shows some differences.

Overall, the calcaneal morphology of Chinese ischyromyids is closest to that of ground squirrels and especially porcupines (both Atherurus and Hystrix) and the coypu; the similarity to the last one is supported also by the PCA analysis. The calcaneal morphology and proportions may therefore reflect their locomotion behavior as generalized terrestrials, with a somewhat limited ability to climb (a rare but observed behavior in Hystrix) and to dig burrows (as does Atherurus⁴³). A transverse and gently concave calcaneocuboid facet of species A facilitates foot rotation along the long axis, useful on an uneven, rocky terrain or while traversing branches, when an animal needs a flexible foot for a better grip (see Chester et al.⁴⁴). On the other hand, the lack of both a characteristically bent calcaneal tuber and posteriorly located peroneal process in all ischyromyids (except for Notoparamys, see Rose and Chinnery³⁵) argues against the arboreal adaptations characteristic of tree squirrels.

Source: Ecology - nature.com