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Life-history traits of the Miocene Hipparion concudense (Spain) inferred from bone histological structure - PubMed

  • ️Wed Jan 01 2014

Life-history traits of the Miocene Hipparion concudense (Spain) inferred from bone histological structure

Cayetana Martinez-Maza et al. PLoS One. 2014.

Abstract

Histological analyses of fossil bones have provided clues on the growth patterns and life history traits of several extinct vertebrates that would be unavailable for classical morphological studies. We analyzed the bone histology of Hipparion to infer features of its life history traits and growth pattern. Microscope analysis of thin sections of a large sample of humeri, femora, tibiae and metapodials of Hipparion concudense from the upper Miocene site of Los Valles de Fuentidueña (Segovia, Spain) has shown that the number of growth marks is similar among the different limb bones, suggesting that equivalent skeletochronological inferences for this Hipparion population might be achieved by means of any of the elements studied. Considering their abundance, we conducted a skeletechronological study based on the large sample of third metapodials from Los Valles de Fuentidueña together with another large sample from the Upper Miocene locality of Concud (Teruel, Spain). The data obtained enabled us to distinguish four age groups in both samples and to determine that Hipparion concudense tended to reach skeletal maturity during its third year of life. Integration of bone microstructure and skeletochronological data allowed us to identify ontogenetic changes in bone structure and growth rate and to distinguish three histologic ontogenetic stages corresponding to immature, subadult and adult individuals. Data on secondary osteon density revealed an increase in bone remodeling throughout the ontogenetic stages and a lesser degree thereof in the Concud population, which indicates different biomechanical stresses in the two populations, likely due to environmental differences. Several individuals showed atypical growth patterns in the Concud sample, which may also reflect environmental differences between the two localities. Finally, classification of the specimens' age within groups enabled us to characterize the age structure of both samples, which is typical of attritional assemblages.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Geographic locations of the Miocene sites studied.

The map shows the location of the two fossil sites studied in the present paper. LVF: Los Valles de Fuentidueña (Segovia, Duero Basin) and CD: Concud (Teruel, Calatayud-Teruel Basin).

Figure 2
Figure 2. Different degrees of histological preservation in Hipparion concudense.

The Hipparion concudense sample includes (a) specimens with a well-preserved histological structure 30656a (Mt), (b) specimens with taphonomical alterations that do not obscure the histological details 43971 (Mt), and (c) specimens that are badly damaged 30604 (Mc). The pictures show details of the cortical bone from the Los Valles de Fuentidueña specimens. Mt: metatarsal; Mc: metacarpal. Scale bar: 500 µm.

Figure 3
Figure 3. Bone histology of Hipparion concudense from Los Valles de Fuentidueña.

Detail of the bone microsctructure observed in the transverse thin sections of mid-shaft from (a) humerus 30779a, (b) femur 30694, (c) tibia 30682, and (d) metapodial 30657-355x. Scale bar: 5000 µm.

Figure 4
Figure 4. Detail of high bone remodeling.

Tibia 28826 shows secondary osteons throughout the cortical bone that obscure histological features. Scalebar: 5000 µm.

Figure 5
Figure 5. Distribution of bone remodeling areas in limb bones of Hipparion concudense.

Green lines delimited the highly remodelled areas in each skeletal element. (a) humerus 30702, (b) tibia 38686, (c) metatarsal 67917, and (d) femur 30694. Scalebar: 5000 µm.

Figure 6
Figure 6. Growth marks in humeri of Hipparion concudense.

The figure shows (on the left) the cross sections of humeri 30702 (top) and 30779a (down) with the lines of arrested growth identified in the cortical bone and (on the right) a detail of the cortical bone with these growth marks. Red lines are LAGs; green lines indicate the LAGs in the bone remodelled areas; gray lines show the inferred position of the LAGs in regions of the section lacking the cortical bone; black lines show the partial marks observed in the section; red arrows indicate the growth marks within the cortical bone; and vertical red lines show the EFS. Scalebar: 5000 µm.

Figure 7
Figure 7. Growth marks in femora of Hipparion concudense.

The figure shows (on the left) the cross sections of femora 30698 (top) and 30694 (down) with the lines of arrested growth identified in the cortical bone and (on the right) a detail of the cortical bone with these growth marks. Red lines are LAGs; green lines indicate the LAGs in the bone remodelled areas; grey lines show the inferred position of the LAGs in regions of the section lacking the cortical bone; black lines show the partial marks observed in the section; red arrows indicate the growth marks within the cortical bone; and vertical red lines show the EFS. Scalebar: 5000 µm.

Figure 8
Figure 8. Growth marks in tibiae of Hipparion concudense.

The figure shows (on the left) the cross sections of tibiae 30686 (top) and 30685 (down) with the lines of arrested growth identified in the cortical bone and (on the right) a detail of the cortical bone with these growth marks. Red lines are LAGs; green lines indicate the LAGs in the bone remodelled areas; gray lines show the inferred position of the LAGs in regions of the section lacking the cortical bone; red arrows indicate the growth marks within the cortical bone; and vertical red lines show the EFS. Scalebar: 5000 µm.

Figure 9
Figure 9. Growth marks in metapodials of Hipparion concudense.

The figure shows (on the left) the cross sections of the metatarsal 30613-xfisura from Los Valles de Fuentidueña (top) and 17215 from Concud (down) with the lines of arrested growth identified in the cortical bone and (on right) a detail of the cortical bone with these growth marks. Red lines are LAGs; green lines indicate the LAGs in the bone remodelled areas; red arrows show the growth marks within the cortical bone. Scalebar: 5000 µm.

Figure 10
Figure 10. Bone histology of the metapodials of Hipparion concudense from Los Valles de Fuentidueña and Concud.

The figure shows the histological features characterizing the three ontogenetical groups established in the Hipparion concudense sample from skeletechronological data (a–c) and different growth patterns (d–f). (a) 31186: immature specimens with vascular canals open to the periosteal surface (white arrows); (b) 17083: subadult specimen with fibrolamellar bone tissue, two LAGs and no periosteal canals; (c) 67917: adult specimen showing intracortical fibrolamellar bone with two LAGs and periosteal lamellar with EFS. Red arrows indicate growth marks; (d) 30599: one LAG, one inner EFS (4 LAGs) and one outer EFS (2 LAGs); (e) 17242: one LAG and one EFS (4 LAGs); 17184: (f) two EFSs (6 LAGs in the inner EFS and 3 LAGs in the outer EFS). Growth marks are indicated with red arrows. Scale bar: 500 µm.

Figure 11
Figure 11. Distribution of metapodials in both populations of Hipparion concudense.

The graph shows the number of metacarpals (Mc) and metatarsals (Mt) in the two samples from Los Valles de Fuentidueña (LVF) and Concud (CD), considering the number of growth marks. Red: metacarpals and Blue: metatarsals.

Figure 12
Figure 12. The age structure of the Los Valles de Fuentidueña and Concud samples.

The high number of adults and the scarcity of two–year-old subadult individuals point to an attritional model, in which the specimens are acumulated in the assemblage due to a combination of factors mainly affecting the vulnerable age groups.

Figure 13
Figure 13. Different degrees of bone remodeling in Hipparion concudense.

The figure shows different degrees of bone remodeling (a) specimen 30657-355x (Mc, LVF) shows a primary cortical bone with no secondary osteons; (b) specimen 67917 (Mt, LVF) shows an increase in bone remodeling; secondary osteons appear in the layer of woven bone tissue among rows of primary osteons (black arrows indicate a row of secondary osteons); (c) the cortical bone in specimen 30613-599x (Mt, LVF) is highly remodelled. Mt: metatarsal; Mc: metacarpal. Scale bar: 500 µm. (d) The graph shows the general increase in secondary osteon density in the ontogeny and differences between populations. The metatarsals from Concud are more remodelled than the metacarpals, whereas the metatarsals from LVF show a peculiar bimodal distribution.

Figure 14
Figure 14. Bone section measurements and distribution of the specimens throughout the ontogenetic groups.

The graphs show the increase in (a) antero-posterior diameter, (b) bone area, and (c) the cortical thickness throughout the three ontogenetic groups established in this study from skeletochronological data.

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Grants and funding

This study was funded by the research project CGL2010-19116/BOS (Ministerio de Economia y Competitividad, Spain). CMM was supported by a JAE-DOC postdoctoral contract (CSIC) co-funded by the European Social Fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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