1. Introduction
Ruminants represent a diverse group of animals employed in the field of animal production and constitute a component of wild fauna. Their distinctive morphological characteristics, particularly those pertaining to distal portions of their limbs, are a hallmark of their anatomical configuration. Classified as artiodactyls, the autopodial bones of these creatures have consistently garnered research interest from a myriad of scientific disciplines, including evolutionary studies, archaeozoology, physiology, and pathology. The significance of research into digital bones is multifaceted, having inspired investigations into archaeology, adaptation, biomechanics, and pathology in animals (
Table 1).
The digital skeleton of the ruminants consists of two digits (third or medial or inner and fourth or lateral or outer). The skeleton of a fully developed digit consists of a proximal (first) phalanx, a middle (second) phalanx, and a distal (third) phalanx.
The digital bones of mammals have been the subject of discussion from the evolutionary point of view [
24]. These skeletal elements are known to reflect ecology and locomotory habits in the animals. Furthermore, the phalanges have been identified as a valuable archaeological resource, facilitating the identification of excavated skeletal elements and enabling the study of animal adaptation [
9].
Lameness is a prevalent health concern in domestic ruminants. Given that the great majority of lameness cases are attributed to digital and claw lesions, many researchers have explored the potential correlation between the anatomy of the autopodium and claw diseases [
1,
3,
16].
Sheep and goats represent a substantial proportion of the total population of ruminants in Greece. However, the extant literature on the morphometry of the phalanges in these species, and especially in indigenous breeds, is limited. The Karagouniko sheep originates from central Greece, with the majority of the population being located in the Thessaly region. It is a lowland breed, characterized by its thin tail and mixed wool. The breed is notable for its relatively high milk production and its ability to adapt to marginal conditions [
25]. The Hellenic goat is the primary breed in Greece. It is an indigenous breed that is also referred to as
Capra prisca [
26].
The objective of the present study was to provide osteometric data on the phalanges of Karagouniko sheep and Hellenic goats, with a view to assembling the morphological profile of these two animal species. The data thus obtained will facilitate comparisons with other ovine and caprine measurements, aid the interpretation of metric data, and provide further information on the profile of the metric parameters of both the sheep and goat. Furthermore, the potential relationships with functional morphology and their potential association with the pathology of the autopodium were evaluated.
2. Materials and Methods
The distal extremities of the fore and hind limbs from 30 ewes of the Karagouniko breed and 30 Hellenic goats aged more than 2 years (median age 3.7 years), based on the number of permanent incisors [
27], were used in the study. The extremities were obtained from a commercial slaughterhouse and immediately subjected to identification (forelimbs and hind limbs) and grouping according to the animal. Subsequently, the autopodia were skinned, macerated, cleaned, and dried.
The first, second, and third phalanges were manually measured by the same person with the aid of a caliper, which had the capacity to measure up to 0.01 mm. The definition of linear measurements performed is depicted in
Figure 1 and
Table 2. The majority of measurements were taken according to the method previously described by von den Driesch [
28], with an additional measurement in the third phalanx (height in the region of the extensor process). All linear measurements were in millimeters. In order to avoid errors during the measurements, the identical anatomical reference points, including the fovea articularis, the articular surface, the process, the protuberance, and the borders of the bones, were also considered. All parameters were measured three times, and the mean values were recorded. A series of indexes was calculated as the ratio of the length to the smaller width for the first and second phalanges and the ratio of the length to the height of the extensor process for the third phalanx (
Table 3). The total length of the third and fourth digits was calculated by summing the lengths for the first and second phalanges and the length of the dorsal surface of the third phalanx of the relevant digits.
The data were analyzed using the statistical software package SPSS version 21. Paired-sample t-tests were run to compare the data obtained for each measurement between the fore and hind limbs and the third and fourth digit for each animal species. Pearson’s correlation coefficient was used to identify potential linear relationships among the parameters evaluated. Linear regression analysis was used to create prediction equations using variables with a Pearson correlation coefficient higher than 0.7. A significance level of p ≤ 0.05 was used in all comparisons.
3. Results
In sheep and goats, the length of the second and third phalanges of the fore third digit were significantly higher than those of the fourth digit (
p < 0.05;
Table 4). No significant difference was detected on the length of the first phalanx between the third and the fourth digits. Furthermore, a significant decrease in the length of the first phalanx in the hind third digit compared to the fourth hind digit was observed (
p < 0.05;
Table 4) in both sheep and goats. Additionally, a similar trend was noted for the length of the third phalanx in goats (
p < 0.05;
Table 4). Conversely, in sheep, the length of the third phalanx was found to be significantly higher at the third digit compared to the fourth digit (
p < 0.05;
Table 4). In goats, the length of the second phalanx was significantly higher in the third than the fourth hind digit (
p < 0.05;
Table 4). However, no significant difference was detected in sheep (
p>0.05;
Table 4).
In sheep, the breadth of the proximal end of the first and second phalanges was significantly higher in the third than the fourth digit in fore and hind limbs (
p < 0.05;
Table 4). In goats, no such difference was observed (
p > 0.05;
Table 4), except for the first phalanx of the fore limbs (
p < 0.05;
Table 4). The breadth of the distal end of the phalanges was comparable between the third and fourth digits in both species in fore and hind limbs (
p > 0.05;
Table 4) with the exception of the first phalanx, where it was higher in the third than the fourth fore digit (
p < 0.05;
Table 4). Furthermore, the smallest breadth of the diaphysis of the first and second phalanx was significantly higher in the third than the fourth digit in fore and hind limbs in both species (
p < 0.05;
Table 4). However, this difference was not observed in the first digit of the hind limbs of goats (
p > 0.05). In goats, the length of the dorsal surface of the third phalanx of the fore limbs was significantly higher in the third than the fourth digit (
p < 0.05). In contrast, no significant differences were observed in sheep or hind limbs of goats (
p > 0.05). However, in sheep and in the fore limb of goats, the height in the region of the extensor process of the third phalanx was significantly higher in the third than the fourth digit (
p < 0.05). In the hind limb of goats, there was not such a difference (
p > 0.05). In both species, the total length of the third digit was found to be significantly higher in the fore limb and significantly lower in the hind limb than the fourth digit.
The lengths of all phalanges of the third digit were found to be significantly higher in the fore compared to the hind limb in sheep and in goats (
p < 0.05;
Table 5). In the fourth digit, the lengths of the first and second phalanges were not significantly different between the fore and hind limb (
p > 0.05;
Table 5), whereas the length of the third phalanx was significantly higher in the fore than the hind limb (
p < 0.05;
Table 5). Furthermore, the breadth of the proximal and distal ends and the smallest breadth of the diaphysis of the first and second phalanges were significantly higher in the fore than the hind limb (
p < 0.05;
Table 5) in both species. Additionally, the length of the dorsal surface and the height in the region of the extensor process were also significantly higher in the fore compared to the hind limb (
p < 0.05;
Table 5). The total lengths of the third and fourth digits were significantly higher in the fore compared to the hind limb in both sheep and goats (
p < 0.05;
Table 5).
In sheep, the index in the fore first phalanx was significantly lower in the third digit compared to the fourth, but the opposite was observed for the second phalanx (
p < 0.05;
Table 6). In the hind limb, the indexes for the first and second phalanges were significantly lower in the third compared to the fourth digit. The index for the third phalanx was not significantly different between the third and the fourth digit in either the fore or the hind limb. All indexes of the phalanges were significantly different between the fore and the hind digits, and the indexes of the first phalanx of the third and the fourth digits and of the second phalanx of the fourth digit were significantly higher in the hind than the fore limbs (
p < 0.05;
Table 6). The indexes of the second phalanx of the third digit and of the third phalanx of the third and fourth digits exhibited significantly higher values in the fore compared to hind limb (
p < 0.05;
Table 6). In goats, the indexes of the first fore and of the first and second hind phalanges were significantly higher in the third than in the fourth digit (
p < 0.05;
Table 6). The other indexes were not significantly different between the third and the fourth digits (
p > 0.05;
Table 6). Furthermore, the indexes in the first and second phalanges of the third and fourth digits were significantly higher in the hind than the fore limb (
p < 0.05;
Table 6). Conversely, the indexes of the third phalanx were not significantly different between the fore and the hind limbs in either the third or fourth digit. Between species, all indexes calculated for the third phalanx, the index for the second phalanx of the third fore digit, and the index of the first phalanx of the third hind digit were significantly higher in goats than in sheep (
p > 0.05;
Table 6). However, no other significant difference was detected on the indexes between species (
p > 0.05;
Table 6).
The prediction equations between measurements with R > 0.7 are presented in
Table 7. The length of the first phalanx of the fourth fore digit for sheep and the first phalanx of the fourth hind digit in goats were the most useful measurements for the prediction of the lengths of the other bones, with R
2 values higher than 0.85. In sheep, the same measurement can be used for the prediction of the height in the region of the extensor process of the third phalanx, with R
2 higher than 0.73.
4. Discussion
The objective of this study was to provide osteometric data on the phalanges of Karagouniko sheep and Hellenic goats. These breeds were selected due to their importance as indigenous local breeds of the Mediterranean basin, and their morphotypes are certainly close to those that can be found on ancient archaeological sites [
29], despite their differences in size from modern breeds. All measurements were made manually with the aid of a caliper to determine the absolute bone dimensions. This method was selected over X-rays or digital images, because direct manual measurements have advantages in terms of reliable identification of the exact location of anatomical points, as well as direct visibility.
An interesting finding of this study is the difference between the lengths of the third and fourth digits, as reflected by the differences in phalanx lengths and their sums. In the fore limbs, the third digit is longer than the fourth digit and the opposite occurs in the hind limbs in both sheep and goats. To the best of our knowledge, such information is scarce in the extant literature on sheep and goats. However, similar results have been obtained in studies of cattle [
1]. Muggli et al. [
3] investigated the length asymmetry of the bovine digits of the fore and hind limbs, finding that the first and second phalanges of the fourth digit were significantly longer than their counterparts of the third digit, whereas the third phalanx of the third digit was longer than its lateral partner. Furthermore, Keller et al. [
17] investigated the autopodia of four species of wild artiodactyls using X-rays, revealing that the paired digits differed in length, with the fourth digit being longer than the third. The authors proposed that a longer outer digit might be advantageous on soft ground to maximize the stability of the center of the body mass during walking and also at faster speeds [
17]. Additionally, the latter authors hypothesized that this anatomical variation may confer a competitive edge in contexts such as intra-species combat or evasive maneuvers in predator–prey interactions, owing to an enhanced grip strength.
The differences in the length of digits or digital bones have been suggested as risk factors for locomotor disorders and lameness in cattle [
1,
3,
30]. However, such a connection seems to occur, at least in sheep, for fore but not for hind limbs. In a previous study, it was observed that the majority of lesions that cause lameness occur in the inner claw in both fore and hind limbs [
31]. Similar results were obtained regarding the prevalence of white line lesions in the fore limbs of sheep [
32], where most of them were detected at the claw of the third digit. These observations suggest that bone length is likely to be only one of several contributing factors to lameness, with other anatomical structures such as joints, ligaments, and hooves also playing a role in locomotion. Furthermore, the presence of digital lesions and lameness is significantly influenced by infectious agents.
Another interesting finding was the observed difference in the length and the breadth of the proximal and distal ends and the smallest breadth of the diaphysis of the first and second phalanges and of the length of the digits between fore and hind limbs. The distinct functions of the fore limbs and hind limbs in cursorial quadrupeds suggest a potential correlation with the distribution of body weight across the limbs during locomotion. In sheep, for instance, approximately 30% of the body weight is allocated to each fore limb and 20% to each hind limb [
33]. A similar phenomenon was observed in another study [
34], where 31.34% of the body weight was found to be distributed between the forelimb and 18.79% between the hind limb in sheep. The direct relationship between these length differences and the prevalence of digital lesions and lameness remains uncertain and requires further investigation. Some studies have indicated a higher prevalence of lameness in the fore limb [
35,
36], while others have found it to be more prevalent in the hind limb [
31,
37,
38].
The indexes have been demonstrated to be of significant value in facilitating comprehension of the morphology and functionality of the bones. The disparities observed between the fore and hind limbs in both species are indicative of the previously mentioned body weight distribution. Furthermore, from an archaeological perspective, the indexes are also useful for the differentiation of the bones between the different species. The metapodial index has been proposed as a means of differentiating between sheep and goats [
39]. The results of the present study suggest that the index of the third phalanx can also be used for the differentiation between sheep and goats. Apart from the differentiation between species, the indexes seem to be useful for the differentiation between the fore and hind limb phalanges, but not for the third phalange of goats.
From an archaeological perspective, the prediction equations also proved to be of significant value. The results obtained from the analysis indicate that the most useful parameter for the prediction of the length of the first and second phalanges in sheep is the length of the first phalanx of the fourth fore digit. In goats, the equivalent parameter is the first phalanx of the fourth hind digit.