Trabecular architecture in the forelimb epiphyses of extant xenarthrans (Mammalia)

Abstract

BackgroundBone structure has a crucial role in the functional adaptations that allow vertebrates to conduct their diverse lifestyles. Much has been documented regarding the diaphyseal structure of long bones of tetrapods. However, the architecture of trabecular bone, which is for instance found within the epiphyses of long bones, and which has been shown experimentally to be extremely plastic, has received little attention in the context of lifestyle adaptations (virtually only in primates). We therefore investigated the forelimb epiphyses of extant xenarthrans, the placental mammals including the sloths, anteaters, and armadillos. They are characterised by several lifestyles and degrees of fossoriality involving distinct uses of their forelimb. We used micro computed tomography data to acquire 3D trabecular parameters at regions of interest (ROIs) for all extant genera of xenarthrans (with replicates). Traditional, spherical, and phylogenetically informed statistics (including the consideration of size effects) were used to characterise the functional signal of these parameters.ResultsSeveral trabecular parameters yielded functional distinctions. The main direction of the trabeculae distinguished lifestyle categories for one ROI (the radial trochlea). Among the other trabecular parameters, it is the degree of anisotropy (i.e., a preferential alignment of the trabeculae) that yielded the clearest functional signal. For all ROIs, the armadillos, which represent the fully terrestrial and fossorial category, were found as characterised by a greater degree of anisotropy (i.e., more aligned trabeculae). Furthermore, the trabeculae of the humeral head of the most fossorial armadillos were also found to be more anisotropic than in the less fossorial species.ConclusionsMost parameters were marked by an important intraspecific variability and by a size effect, which could, at least partly, be masking the functional signal. But for some parameters, the degree of anisotropy in particular, a clear functional distinction was recovered. Along with data on primates, our findings suggest that a trabecular architecture characterised by a greater degree of anisotropy is to be expected in species in which the relevant epiphyses withstand a restricted range of load directions. Trabecular architecture therefore is a promising research avenue for the reconstruction of lifestyles in extinct or cryptic species.Electronic supplementary materialThe online version of this article (10.1186/s12983-017-0241-x) contains supplementary material, which is available to authorized users.

Trabecular architecture in the humeral metaphyses of non‐avian reptiles (Crocodylia, Squamata and Testudines): Lifestyle, allometry and phylogeny

“…Bone volume fraction (BV/TV) shows no dependence with size in squamates and in turtles. BV/TV was also reported to be independent of body size in mammals, through various sampled bones in a wide variety of taxa (Barak, Lieberman, & Hublin, ), but also in more restricted samplings: in thoracic vertebrae of hominoids (Cotter et al, ) or in fore limb epiphyses of xenarthrans (Amson et al, ). However, other analyses have found that BV/TV had a positive allometry in the femoral epiphyses of mammals and birds (Doube et al, ), in the lumbar vertebrae of strepsirrhine primates (Fajardo et al, ), in the humeral and femoral heads of primates (Ryan & Shaw, ) and in the femoral heads of sciuromorphs (Mielke et al, ).…”

“…Average branch length (Av.Br.Len) scales with a significant negative allometry in squamates and in turtles. This parameter has rarely been used in other studies focused on allometries to our knowledge, but it was significantly correlated to body size in the fore limb epiphyses of extant xenarthrans (Amson et al, ).…”

“…Then eight trabecular parameters were measured with BoneJ (raw measurements given in Table , means for each lifestyle in Table , for Squamata and Testudines in Table , see Fiji Macro in Supporting Information, file 3). These parameters were often used by others authors, except for average branch length (Av.Br.Len, only measured by Amson et al, ). Thickness (Tb.Th) and Av.Br.Len are expressed in mm; bone surface (BS) in mm 2 ; bone volume (BV) in mm 3 ; connectivity (Conn) is approximately the number of trabeculae in the VOI; connectivity density (Conn.D) in number/mm 3 ; number (Tb.N) in number/mm.…”

“…In another broader study on anthropoid primates, trabecular architecture from the humeral and femoral heads was found to be similar in arboreal and terrestrial locomotor groups (Ryan & Shaw, ). In a study focused on the fore limb epiphyses of xenarthrans, trabeculae have shown the clearest functional signal through their anisotropy: armadillos, fully terrestrial and fossorial, have the most anisotropic trabecular architecture in xenarthrans (Amson, Arnold, van Heteren, Canoville, & Nyakatura, ). In a study focused on the sciuromorph femoral head, four trabecular parameters have shown functional signals related to the various lifestyles found in this clade (Mielke et al, ).…”

“…Thanks to the development of X‐ray computed microtomography, 3D trabecular architecture could be extensively studied in birds (e.g., Bishop et al, ; Doube, Kłosowski, Wiktorowicz‐Conroy, Hutchinson, & Shefelbine, ; Fajardo, Hernandez, & O'Connor, ; Pontzer et al, ) and mammals (e.g., many orders [Doube et al, ], bovids [Mittra, Rubin, & Qin, , Sode, Burghardt, Nissenson, & Majumdar, ], lagomorphs [Marchand, Chen, Buschmann, & Hoemann, , van der Meulen et al, ], primates [Barak, Lieberman, Raichlen, et al, , Cunningham & Black, , Kivell, Skinner, Lazenby, & Hublin, , Lazenby, Skinner, Kivell, & Hublin, , Sode et al, ], rodents [Carlson, Lublinsky, & Judex, , Lambers et al, , Sode et al, ], sciuromorphs [Mielke et al, ], suids [Ben‐Zvi, Reznikov, Shahar, & Weiner, ], and xenarthrans [Amson et al, ]). In comparison, 3D trabecular architecture of nonavian reptiles has received little attention.…”