Our analyses of the trabecular structure in the talus of small to medium-sized living primates indicate that the number, thickness, three-dimensional distribution, and arrangement of the trabeculae in this tarsal bone are primarily linked to the types and magnitudes of loads associated with the postures and motions of the foot. Body mass seems to only affect the number and robustness (thin vs. thick) of the trabeculae, but seemingly not their orientation and elongation. In addition to the external functional anatomy, the study of the trabecular structure of this bone is therefore particularly interesting for extinct taxa, as it can contribute to better understanding their potential locomotor behavior. Here, we have quantified the three-dimensional architecture of the trabecular bone in the tali of three late Eocene primates from Southern of France (Quercy phosphorites): two Adapiformes (Leptadapis and Adapis) and one Omomyiformes (Necrolemur). For this study, we have analyzed two tali referred to Leptadapis magnus [Quercy Old Collections (locality unknown)], four tali referred to Adapis parisiensis [localities: Escamps (MP19) and Rosières 2 (MP19)], and ten tali referred to Necrolemur antiquus [locality: La Bouffie (MP17a)]. These fossils are housed in the Paleontological collections of the University Montpellier 2. The locomotor behavior of these taxa has been analyzed previously using various postcranial skeletal elements (e.g., Dagosto, 1983; Godinot and Dagosto, 1983; Godinot and Jouffroy, 1984; Godinot, 1991; Bacon and Godinot, 1998).
Adapis parisiensis was a medium-sized primate with an estimated body weight of about 1.3 kg (Fleagle, 1999). Most of the postcranial features referred to this Adapis species indicate increased mobility of joints, especially for movements out of the sagittal plane. Basically, A. parisiensis appears as a slow-moving arboreal-quadruped primate (climber), which did not include significant leaping activities in its locomotor repertoire (Dagosto, 1983). However, other postcranial analyses have shown the existence of two categories of activities in the locomotor repertoire of Adapis, thereby suggesting the existence of distinct but close species among the “Adapis parisiensis” group. From the functional morphology of the hand bones referred to Adapis from Rosières 2, Godinot and Jouffroy (1984) have shown that this arboreal quadruped primate was rather a branch-running and walking form, capable of climbing but without strong specialization. From the morphofunctional anatomy of the femora, Bacon and Godinot (1998) have shown that some Adapis femora belonged to individuals, which were branch walking and running forms, using climbing less frequently, and some others, which were less specialized for running and that used climbing more frequently.
Compared to the tali of living primates, the BV/TV values recorded in the talar body of fossils appear noticeably high. This is particularly shown for the tali of Leptadapis, which record the highest BV/TV values (Table 6). However, a question arises as to whether such a strong density of bone in this taxon reflects natural condition, or if it is the result of an artificial increase due to diagenesis (i.e., increase related to the mineral replacement during the fossilization process). In Leptadapis, the trabeculae are indeed rather thick, and much thicker than in tali of certain living primates for which we have recorded strong Tb.Th values [e.g., Cebus and Propithecus (Table 3)], the body mass of which approximates that of Leptadapis [i.e., 3–5 kg (Table 2)]. The same seems to be true for the tali of Adapis, which exhibit lesser but noticeably thick trabeculae compared to living taxa of the same body mass category (1–2 kg). For the tali of Necrolemur, it seems difficult to claim an effect of diagenesis, because the values of all the trabecular bone parameters, notably those reflecting bone density, enter in the range of variation recorded in tali of living species of similar body mass. Regardless this possible diagenetic effect in tali of Leptadapis and Adapis (which would introduce a bias on the Tb.Th, and by extension on the measure of the bone volume fraction), the Tb.N in their tali remains, however, in the range of Tb.N values recorded in tali of certain living primates. The same is true for the values of SVD-DA and SVD-E, which are for the three fossils, in the range of the fabric anisotropy and elongation values recorded in tali of living primates. For the three taxa, there is no strong mediolateral difference in the bone volume fraction. Only the tali of Leptadapis record a slightly higher bone density in their lateral side. In this taxon, the Tb.N approximates that observed in Propithecus, Hapalemur, or Daubentonia (Tables 3 and 6). For the tali of Adapis and Necrolemur, the Tb.N is moderately high, in the range of that observed in Lepilemur, Loris, and Tarsius (Tables 3 and 6). However, the talar bone structure of Necrolemur compared to that of Adapis, as well as of Leptadapis, differs substantially in the pattern of the fabric anisotropy. The trabecular structure in tali of Necrolemur is clearly more oriented (especially in the medial side). The degree of anisotropy and elongation in Necrolemur approximate those observed in tali of Propithecus, Cebus, Cebuella, Saimiri, or Leontopithecus, which are primates engaged in a kind of arboreal quadrupedalism with some good abilities to leap. In contrast, in tali of Adapis and Leptadapis, the trabecular structure appears more randomly oriented as it is shown by the rather low values of SVD-DA-E, which are in the range of some primates who are arboreal quadruped, without leaping or frequent leaping activities in their locomotor repertoire (e.g., Loris, Perodicticus, and Nycticebus, but also Microcebus, Daubentonia,). In sum, it is clear that the trabecular bone structure of the tali of Necrolemur, with a moderate degree of anisotropy and elongation indicates that the ankle bone in this extinct taxon was subjected to moderately strong and directed loading conditions at the ankle joints, thereby demonstrating a leaping activity. This corroborates the functional conclusions deriving from the external morphology of the talus of this Eocene primate. However, although the external talar morphology in this fossil taxon is quite similar to that found in Tarsius and Galago, the degree of anisotropy indicates that Necrolemur did not exhibit extreme specialization for leaping, as it is the case for Tarsius and Galago. The values of SVD-DA-E recorded in tali of Necrolemur are elevated but clearly lower than those recorded in Tarsius and Galago. According to the whole trabecular bone parameters measured, compared to those in living taxa, it seems that Necrolemur was a small arboreal quadruped primate, which was capable of leaping but also climbing, although not particularly specialized for either of these activities. This locomotor behavior hypothesis is confirmed by the discriminant analysis (Fig. 9B), which primarily allocates Necrolemur to the vertical clingers and leapers (A1: P = 0.4; A2: P = 0.32), but also to the small arboreal agile quadrupeds (B: P = 0.28), albeit to a lesser extent. In contrast, the trabecular bone parameters measured in tali of Leptadapis and Adapis indicate that leaping was probably not an important component of their locomotor repertoire. The less anisotropic and dense (although possibly artificial) trabecular structure recorded within their talar body indicates that the bone was rather adapted for less strong directional loads, thereby suggesting more emphasis on quadrupedalism and climbing. However, in the tali of Adapis and Leptadapis, we have not recorded a strong mediolateral difference in the bone volume fraction, as it is the case in most primates who are frequent climbers. For living primates, we have hypothesized that the mediolateral variation in the bone volume fraction might be linked to the forces generated by sustained inverted foot postures, which seems to load the medial aspect of the talar body more strongly. The external morphology of the tali of these two fossil primates indicates that they were able to practice foot inversion (Dagosto, 1983). However, in Adapis and Leptadapis, the loading pattern at the ankle joints associated with the inverted foot position for climbing might have been more balanced mediolaterally, thereby involving a more uniform distribution of trabeculae (weakly oriented) in both sides of their talar body. Nycticebus, which is a nonleaping, slow-moving arboreal quadruped, exhibits a similar case of mediolateral uniform pattern of bone volume fraction, but it slightly differs in the pattern of the fabric anisotropy. The discriminant analysis (Fig. 9B) revealed strong affinities with the medium-sized lemuriform branch-running and walking type (E1: P = 1) for Adapis and Leptadapis. This would indicate that A. parisiensis and L. magnus exhibited some degree of proficiency for leaping (springing) as it does in the living species of this locomotor subcategory (e.g., Lemur, Eulemur, and Varecia, but also Daubentonia; Table 1). Both fossil taxa, especially Leptadapis, have been generally regarded as slow-moving arboreal-quadruped primate (climber with labored locomotion), which did not included very important leaping activities (less efficient abilities) in their locomotor repertoire (Dagosto, 1983). Regarding the locomotor repertoire of Adapis, the functional interpretation of the postcranial remains referred to this genus has proven to be more mixed in terms of postural activities and positional behaviors, which included branch walking and running forms, using climbing less frequently, and other forms less specialized for running that used climbing more frequently. For Adapis, we have therefore sampled here primarily the tali of the individuals, which were rather belonging to the branch-running and walking forms, as those evidenced by Bacon and Godinot (1998) from the femoral anatomy. For Leptadapis, the LDA results are somewhat surprising, given the rather plate-like but rather low anisotropy observed on tali of this taxon (very low value of SVD-E in the lateral side of the talar body). Leptadapis was certainly an arboreal quadruped who was able to run and walk on branches with some abilities for climbing (without extreme specialization), but most likely with less-efficient leaping abilities than the living primates classified as branch-running and walking type (E1). However, for the fossil tali of Leptadapis, we must keep in mind that a diagenesis effect might have biased the measure of the three-dimensional architecture of the trabecular bone.