How the even‐toed ungulate vertebral column works: Comparison of intervertebral mobility in 33 genera

Abstract

In this study, we used a previously developed osteometry‐based method to calculate available range of motion in presacral intervertebral joints in artiodactyls. We have quantified all three directions of intervertebral mobility: sagittal bending (SB), lateral bending (LB), and axial rotation (AR). This research covers 10 extant families of artiodactyls from 33 genera and 39 species. The cervical region in artiodactyls is the most mobile region of the presacral vertebral column in SB and LB. Mobility is unevenly distributed throughout the joints of the neck. The posterior neck joints (C4–C7) are significantly more mobile (on average by 2.5–3.5°) to anterior joints (C2–C4) and to the neck–thorax joint (C7–T1) in SB and LB. An increase in the relative length of the cervical region in artiodactyls is accompanied by an increase in the bending amplitudes (SB: Pearson r = 0.781; LB: r = 0.884). Animals with the most mobile necks (representative of Giraffidae and Camelidae) are 2–3 times more mobile in SB and LB compared to species with the least mobile necks. The thoracic region in artiodactyls, as in other mammals, is characterized by the greatest amplitudes of AR due to the tangential orientation of the zygapophyseal articular facets. The lowest AR values in the thoracic region are typical for the heaviest artiodactyls—Hippopotamidae. The highest AR values are typical for such agile runners as cervids, musk deer, pronghorn, as well as large and small antelopes. SB mobility in the posterior part of the thoracic region can be used by artiodactyls during galloping. The highest values of SB aROM in the posterior part of the thoracic region are typical for small animals with high SB mobility in the lumbar region. The lumbar region in mammals is adapted for efficient SB. Both the cumulative and average SB values in the lumbar region showed correspondence to the running type employed by an artiodactyl. The greatest SB amplitudes in the lumbar region are typical for small animals, which use saltatorial and saltatorial–cursorial running. An increase in body size also corresponds to a decrease in lumbar SB amplitudes. The lowest SB amplitudes are typical for species using the so‐called mediportal running. Adaptation to endurance galloping in open landscapes is accompanied by a decrease in lumbar SB amplitudes in artiodactyls. The consistency of the approach used and the wide coverage of the studied species make it possible to significantly expand and generalize the knowledge of the biomechanics of the vertebral column in artiodactyls.

In this study, we used a previously developed osteometry‐based method to calculate available range of motion in presacral intervertebral joints in artiodactyls. The purpose of this study is the exploration of the three directions of mobility throughout the presacral region of the vertebral column in diverse even‐toed ungulates. This research covers 10 extant families of artiodactyls from 33 genera and 39 species. This study is not only the first wide screening of backbone mobility in mammals but also considers the relationship of intervertebral mobility in artiodactyls with linear proportions of the vertebral column, running technique, phylogeny‐based taxonomic grouping, habitat, and animal's diet.

1. INTRODUCTION

This study examines the mobility of the presacral vertebral column in even‐toed ungulates. All terrestrial representatives of the Cetartiodactyla clade are united under this name. To prevent the reader from false phylogenetic suspicions, in this study we will not use the Latin term “Artiodactyla” from the outdated taxonomy. Instead, we will use the trivial terms “artiodactyls” and “even‐toed ungulates,” which unite all ungulate‐morphotype members of the clade Cetartiodactyla. These animals are known for their running abilities, speed, stamina, and maneuverability, as well as jumping over obstacles, capacities which are retained in a wide range of body sizes. Not only the legs but also the vertebral column is involved in these activities. However, the vertebral column of artiodactyls is obviously less mobile than that of carnivores that compete in running with artiodactyls as predators with prey. The difference is so pronounced that Gambaryan (1974) opposed the ungulates and the carnivores as “the dorsostable runners” and “the dorsomobile runners,” respectively. Contrary to this opposition, Alexander et al. (2009) suggested the positive role of backbone elasticity in galloping at high speeds for both carnivores (domestic dog) and artiodactyls (fallow deer). However, the vertebral column mobility of artiodactyls was never studied quantitatively across a wide range of species.

The study of the biomechanics of the vertebral column and range of motion (ROM) in particular, in any large mammal, including artiodactyls, is methodologically complicated. Such studies are rare and, in general, rather fragmentary in terms of the coverage of the studied taxa. Differences in approaches used to estimate ROM values often prevent a correct comparison of the results obtained by different researchers with each other. There are two main approaches. One is to measure used ROM (uROM) or movement in living animals (in vivo studies). The other is to measure available ROM (aROM) or mobility studied on syndesmological specimens of the vertebral columns (in vitro studies). In most detailed studies, all three directions of intervertebral movement or mobility are analyzed: sagittal bending (SB), lateral bending (LB), and axial rotation (AR). We failed to find any publications on in vivo measurements of intervertebral movements in artiodactyls. At best, only rough estimates of the general curvature of the vertebral column as a whole in the sagittal plane (e.g., Alexander et al., 2009) and the cervical region in the sagittal and lateral plane can be found (Dzemski & Christian, 2007).

In vitro studies are based on study of specially prepared syndesmological specimens, cleared of muscles but retaining ligaments. These studies require precise equipment for correct estimates of aROM values under controlled loading by torque in one of the three planes of mobility. In early in vitro studies (Gál, 1993; Pylypchuk, 1975), the aROM values of the specimens were estimated using X‐ray. The lumbosacral region was bent as a whole, not segmented into functional spinal units (FSU—pairs or triples of vertebrae used in such experiments today). Pylypchuk (1975) has not yet used standardized torque values applied to intervertebral joints. Gal (1993) brought the procedure closer to the standards of well‐established medical research of human spinal biomechanics (see White & Panjabi, 1990) using a special spine tester for accurately applying the appropriate torque loading to the lumbosacral region. Pylypchuk (1975) studied SB and LB aROM in the lumbar and lumbosacral joints of Capra hircus (three individuals). Gal (1993) studied SB aROM in the lumbar and lumbosacral joints of Ovis aries (one individual). The most precise aROM estimates for artiodactyls were obtained later as a by‐product in medical research of human spinal biomechanics and intervertebral disk properties. Domestic artiodactyls became model animals in this field (Alini et al., 2008; Smit, 2002; Szotek et al., 2004). At the new stage of research, aROM in all three directions (SB, LB, and AR) was studied using a spine tester device with fixed torque values applied to each FSU with a sample of 5–6 individuals per joint. There are several papers that include accurate numerical data on aROM values in all three directions for each presacral joint of the mammalian vertebral column with the exception of the atlas‐occipital and lumbosacral joints. These are papers on merino sheep (Wilke et al., 1997a) and domestic pig (Wilke et al., 2011). In the papers on cow (Wilke et al., 1997b) and red deer (Kumar et al., 2002), the neck was excluded from the analysis. There are also alternative, but less complete data on aROM in sheep (Kandziora et al., 2001) and pig (Busscher et al., 2010). Several other papers used somewhat different methods. In a study on aROM in the cervical region in llamas and alpacas (Stolworthy et al., 2015), the nuchal ligament was removed prior to measurements. In studies on the lumbar region in goats, either noticeably lower torque values were applied (Krijnen et al., 2006), or posterior (spinous) and transverse processes were removed (Detiger et al., 2013). In a study on aROM in the cervical region in giraffe and okapi (Gunji & Endo, 2016), researchers measured the SB amplitudes using animal carcasses.

In addition, some researchers attempt to roughly estimate uROM and aROM in artiodactyls using photographs, video recordings, and manipulations with dry vertebrae (Dzemski & Christian, 2007). The accuracy of such estimates of amplitudes in individual joints is doubtful, especially in respect of LB and AR.

In addition to studies in which measurements of aROM and uROM were carried out, in some modern studies estimation of ROM was carried out based on manipulation with 3D models of vertebrae (in silico studies). Using this approach, all three directions of mobility in the C7–T1 joint in 37 artiodactyl species (Müller et al., 2021), as well as SB and LB in the cervical spine in giraffe (Vidal et al., 2020) were studied. A more rigorous and close to real amplitudes, but also more laborious method of computer modeling, which can also be conditionally referred to in silico studies, is presented by finite element analysis. This method was used to estimate all three directions of aROM in the cervical region of sheep (DeVries Watson et al., 2014).

On the whole, currently available aROM measurements in artiodactyls (Table 1) cover 5 extant families and only 10 (6 domestic and 4 wild) out of more than 200 extant species (Pavlinov, 2006; Wilson & Reeder, 2005).

TABLE 1.

Available measurements of the vertebral column mobility in artiodactyls

Family	Species	Cervical				Thoracic			Lumbar
		SB	LB	AR		SB	LB	AR	SB	LB	AR
Suidae	Sus scrofa domestica	10	10	10		9, 10	9, 10	9, 10	9, 10	9, 10	9, 10
Tayassuidae	N/A	N/A
Hippopotamidae	N/A	N/A
Camelidae	Camelus bactrianus	8, 12	8, 12	12		N/A
	Lama glama
	Vicugna pacos
Tragulidae	N/A	N/A
Antilocapridae	N/A	N/A
Giraffidae	Giraffa camelopardalis	8, 13	8	N/A
	Okapia johnstoni
Cervidae	Cervus elaphus	N/A				6	6	6	6	6	6
Moschidae	N/A	N/A
Bovidae	Bos taurus	3, 5	3, 5	3, 5		3, 4	3, 4	3, 4	1, 2, 3, 4, 7, 11	1, 3, 4, 7, 11	3, 4, 7, 11
	Capra hircus
	Ovis aries
1. Pylypchuk (1975)—in vitro 2. Gál (1993)—in vitro 3. Wilke et al. (1997a)—in vitro 4. Wilke et al. (1997b)—in vitro 5. Kandziora et al. (2001)—in vitro 6. Kumar et al. (2002)—in vitro					7. Krijnen et al. (2006)—in vitro 8. Dzemski and Christian (2007)—video, manipulation 9. Busscher et al. (2010)—in vitro 10. Wilke et al. (2011)—in vitro 11. Detiger et al. (2013)—in vitro 12. Stolworthy et al. (2015)—in vitro 13. Gunji and Endo (2016)—in vitro

The purpose of this study is the first large‐scale analysis of the three directions of mobility throughout the presacral region of the vertebral column in even‐toed ungulates. This study is largely exploratory; in it we will consider the relationship of intervertebral mobility in artiodactyls with various factors: characteristics of the vertebral column (sizes, length proportions of regions and divisions, the number of joints in the regions, the number of joints with a certain type of zygapophyses facets); locomotion characteristics (using the typology of running forms in ungulates proposed by Gambaryan); phylogeny‐based taxonomic grouping; habitat; and animal's diet. Intervertebral mobility characteristics noted in the study in various representatives of even‐toed ungulates will be discussed separately in the discussion section for the cervical, thoracic, and lumbar regions of the vertebral column.

2. MATERIALS

In our study, only osteological material that is stored in museum collections was used. No interaction with live animals occurred during the study. This study covers representatives of all 10 extant terrestrial Cetartiodactyla families belonging to 33 genera and 39 species (Table S1). The studied material is stored in the following collections: A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences (IEE); Royal Museum for Central Africa (RMCA), Tervuren, Belgium; Zoological Institute of the Russian Academy of Sciences (ZIN), Saint Petersburg; Zoological Museum of the Lomonosov Moscow State University (ZMMU), Moscow.

2.1. Fusions and facet losses in vertebral column

In some cases, the calculation of all three directions of intervertebral mobility or some of these directions was not possible. This is associated with cases of fusions and facet losses in the vertebral column.

Only three cases of fusion of the vertebrae with each other with a complete loss of mobility in the joint were noted on the studied material. All these cases belong to the thoracolumbar region. Two cases are in the tangential facets division: at the T4–T5 joint in the dromedary and the T11–T12 joint in the pygmy hippopotamus; and one case is in the radial facets with a lock division at the T12–L1 joint in the llama (see Figures in Supplementary Material S2). In all cases, fusion occurs along the ventral part of the vertebral bodies, and also between the left zygapophyses in the llama.

In addition to the fusion of the vertebrae, the disappearance of the right or left zygapophyseal articulation (through loss of respective post‐ and prezygapophyseal facets) in the Tf division was noted. This was noted in the T9–T10 joint in the European bison (ZMMU S‐193088) and in the interval T6–T10 in the giraffe (ZMMU S‐175340).

2.2. Terminology for vertebral column parts

Joint numbering—joint 1 is posterior to vertebra 1, etc.

Regions—cervical, thoracic, lumbar, sacral—traditionally defined by rib development: cervical ribs are pleurapophyses, thoracic ribs are free, lumbar ribs are absent, and sacral ribs mediate sacroiliac fusion (Figure 1).

FIGURE 1.

Regions (cervical, thoracic, lumbar, and sacral) and divisions (radial [Rf], tangential [Tf], and radial with a lock [RfL] facet types) of the Bos gaurus (ZIN 8827) vertebral column. Left‐side (a) and dorsal (b) view

Divisions — by zygapophyseal facet type — from anterior to posterior end of thoracolumbar vertebral column there is a succession of radial facets (Rf), tangential facets (Tf), and radial facets with a lock (RfL) (Figure 1). Transitional vertebra with Tf prezygapophyses and RfL postzygapophyses is historically termed “diaphragmatic vertebra,” Tf division corresponds to the prediaphragmatic part of the thoracic region; RfL division corresponds to the postdiaphragmatic part of the thoracic region plus the whole lumbar region (Slijper, 1946).

Loci of transitional status. There are two facet type transitions in the mammalian presacral vertebral column, Rf‐to‐Tf and Tf‐to‐RfL transition. In the studied artiodactyls, both transitions show variability in location. The transitional vertebra bears one facet type on its prezygapophyses and the other type on postzygapophyses. As to Rf‐Tf transition, it usually occurred on vertebra T1 but sometimes on T2. Therefore, in the whole sample of artiodactyls, the T1–T2 joint which number is 8, counting from the atlas, is the first locus of transitional status — it can be either of Rf or of Tf type. The second locus of transitional status is more extended including the joints number 16–20. This means that the transitional vertebra with Tf prezygapophyses and RfL postzygapophyses can be represented by any vertebra in the range from T9 to T14. The joint number 15 in front of T9 is the last non‐transitional one that was of Tf type in all studied artiodactyls, and the joint number 21 at the posterior end of T14 was the first one that was always of RfL type (see Figure 1 and Table S1).

3. METHODS

3.1. Amplitude calculations

To calculate intervertebral mobility, we used a recently developed and validated osteometry‐based method (Belyaev et al., 2021). It is based on the assumption of the functional interrelation between aROM and the geometry of vertebrae and, in particular, of zygapophyseal articular facets (Kuznetsov & Tereschenko, 2010). Trigonometric formulae are used for aROM calculation. The general formula for the angle of rotation is the ratio of the arc of motion length (numerator) to the radius of this arc (denominator). In this study, we calculated the amplitudes (aROM values) for the three degrees of freedom in every presacral intervertebral joint except the atlas‐axis (its number is 1). For SB, the calculated amplitude is the sum of ventral flexion and dorsal extension, and for LB and AR it is the sum of respective motions to the left and to the right.

In the course of evaluation of the optimal formulae for calculating aROM values, it was found that separate formulae for different zygapophyseal facet types (radial [Rf], tangential [Tf], radial with a lock [RfL]) give significantly greater accuracy in aROM calculation than the formulae for the presacral vertebral column as a whole, and greater accuracy than the separate formulae for different vertebral column regions (cervical, thoracic, and lumbar) (Belyaev et al., 2021). In artiodactyls, the Rf type (left and right facets together form a V‐like pattern in the transverse plane) is present in the cervical region and the neck–thorax transition (joints C2–T1), plus the T1–T2 joint in Tayassu, Pecari, Giraffa, and, as individual variation, in Choeropsis. In the anterior and middle parts of the thoracic region, there is the Tf type (left and right facets form a ⁀‐like pattern in the transverse plane). In the end of the thoracic region and up to the lumbo‐sacral joint, there is the RfL type (left and right facets together form a U‐like pattern in the transverse plane). The RfL zygapophyseal type in artiodactyls differs from the simple Rf type of the neck by additional interlocking structures such as ridges and labra (Halpert et al., 1987). In all individuals studied in this paper, the RfL division includes not only the entire lumbar region but also the last joints of the thoracic region.

Reliable in vitro aROM data are available for pigs, sheep, and cows (Wilke et al., 1997a, 1997b, 2011). These data were used for optimization of the values of numeric coefficients K _R and K _S in the formulae (see the procedure details in Belyaev et al., 2021). The pig‐specific, sheep‐specific, and cow‐specific coefficient values were obtained, as well as the general (pig+sheep+cow) coefficients. For greater accuracy, the pig‐specific coefficient values can be used for Suidae, the sheep‐specific values for Caprinae, and the cow‐specific coefficient values for Bovini. However, for other groups (e.g., Camelidae), their own specific coefficients are not available. Therefore, we have decided to use the general coefficients for all artiodactyls which can be named “pan‐artiodactyl coefficients.” This ensures that all the interspecific differences in aROM identified subsequently in this study are associated with the geometry of the vertebrae, and not with differences in the coefficients used (final formulae are represented in Table 2). The disadvantage of using general coefficients for all species is some loss of accuracy of the calculated aROM values in Caprinae, Bovini, and Suidae. For the representatives of these three taxa, the aROM values were additionally calculated using specific coefficients (Table S3), but they were not used for data analysis. The differences in the aROM values calculated with the different coefficients are summarized for the entire sample of studied artiodactyls in Figure 2.

TABLE 2.

Formulae optimized for the aROM calculation in artiodactyls

Motion type	Facet type	Formula
SB	Rf	$\phi$ = [arcsin(Llong/1.38Rvert) – 0.72arcsin(Lshort/1.38Rvert)]•360/$\pi$
	Tf	$\phi$ = [arcsin(Llong/2Rvert) – 0.76arcsin(Lshort/2Rvert)]•360/$\pi$
	RfL	$\phi$ = [arcsin(Llong/2Rvert) – 0.64arcsin(Lshort/2Rvert)]•360/$\pi$
LB	Rf	$\phi$ = [arcsin(Llong/2Rlat) – 0.18arcsin(Lshort/2Rlat)]•360/$\pi$
	Tf	$\phi$ = [arcsin(Wlong/2Rlat) – 0.52arcsin(Wshort/2Rlat)]•360/$\pi$
	RfL	$\phi$ = [arcsin(Dmax _ long/2Rlat) – 0.86arcsin(Dmax _ short/2Rlat)]•360/$\pi$
AR	Rf	$\phi$ = [arcsin(Wlong/2Rvert) – 0.74arcsin(Wshort/2Rvert)]•360/$\pi$
	Tf	$\phi$ = [arcsin(Wlong/2Rlat) – 0.54arcsin(Wshort/2Rlat)]•360/$\pi$
	RfL	$\phi$ = [arcsin(Dmax _ long/2Rlat) – arcsin(Dmax _ short/2Rlat)]•360/$\pi$

FIGURE 2.

aROM variability (range from maximum to minimum) in the presacral vertebral column joints in artiodactyls calculated with different values of coefficients K _R and K _S in the formulae. aROM calculated with the general “pan‐artiodactyl” coefficients is shown by the colored zone. (a) SB aROM; (b) LB aROM, (c) AR aROM. Abscissa axis is graduated by joint numbers

3.2. Model assumptions and limitations

Georges Cuvier's principle of correlation of parts underlies the approach used. The basic assumption of the model is that the passive structures that determine aROM, namely, the geometry of articular surfaces (facets) and the ligamentous apparatus, are quite precisely adjusted to each other. In particular, the size of the articular surfaces does not go beyond the limits set by the ligaments, and the ligaments are not of an excessive length that would allow the articular surfaces to come off each other. The same goes for interference with the ribs. We proceed from the assumption that the geometry of the articular facets of the thoracic region corresponds to the mobility of the vertebral column as part of the integral thorax. In reference in vitro studies, to which our formulae are optimized, aROM measurements were done on the so‐called “functional spinal units” (FSU—pairs or triples of vertebrae used in such experiments) after removal of the ribs and sternum. However, the proximal parts of the ribs were retained in situ, without damage to their joints with the vertebrae (Wilke et al., 2011). This gives us the right to hope that in vitro studies for the thoracic region do not overestimate the aROM in comparison with the lifetime values inherent in the integral thorax. In more detail, the effect of ribs and sternum removal on the results of in vitro measurements was referred to in methodological study (Belyaev et al., 2021).

The question of what kind of relationship is there between aROM and uROM was partially considered in the previous publication of the authors (Belyaev et al., 2021) and is beyond the scope of the current research.

The four cases of discrepancies between the reference and calculated data were described in detail in the methodological study (Belyaev et al., 2021). The data analysis took into account these model limitations.

It should also be noted that uniplanar amplitudes of SB, LB, and AR aROM may not reflect the animal's full ability for motion. Controlled “manipulation” with 3D models of vertebrae allowed researchers to assume that the amount of possible mobility in a certain direction may increase with movement in other directions (Krings et al., 2017). This assumption of reciprocally facilitated aROMs finds its experimental confirmation at least in the avian neck (Kambic et al., 2017). However, even if a similar effect occurs in mammals, the in vitro data we use to calibrate the model only provide information on uniplanar motions. In some cases, our formulae consistently overestimate these in vitro aROM values. It cannot be ruled out that these overestimations may reflect nonplanar aROM that is the amplitude extended due to movement in other directions.

3.3. Length measurements

We also measured the length of the regions (cervical, thoracic, lumbar, and sacral) and divisions (Rf, Tf, and RfL) of the vertebral column (see Table S1) to study the relationship between the linear dimensions of the vertebral column and intervertebral mobility. The length was measured on the articulated vertebral column, along the ventral sagittal line. For example, the length of the cervical region was measured from the anterior edge of C1 (atlas) to the posterior edge of C7, etc.

Based on these measurements, the following proportions were calculated: cervical region length/trunk length (it is thoracolumbar plus sacral length); thoracic region length/thoracolumbar region length; lumbar region length/thoracolumbar region length; Tf division length/thoracolumbar region length; RfL division length/thoracolumbar region length.

3.4. The size of the studied artiodactyls

The in vitro reference data used in the method validation characterize medium‐ and large‐sized mammals. Therefore, it is uncertain how efficiently the method used here can work on small‐sized mammals. With a decrease in the size of the body and vertebrae in particular, the influence of random errors when measuring with a caliper on the accuracy of the final calculations increases. Therefore, for small mammals, the accuracy of the calculations needs to be verified against reliable in vitro experimental aROM estimates. To our knowledge, at present, the smallest mammals studied in this way are the white rabbit (Grauer et al., 2000) and domestic cat (Jones et al., 2020). Therefore, this study focuses mainly on medium and large representatives of artiodactyls (Table S1).

3.5. Age of the studied artiodactyls

We noted that the geometry of the vertebra and its articular processes may differ markedly in juvenile and adult animals, which was previously described for dogs (Benninger et al., 2004). In juvenile individuals, the degree of morphologic features is not fully developed in comparison with adult animals. For a more accurate data analysis, we resorted to using juveniles in this study only in the absence of the necessary material for adults.

3.6. Data analysis

Data were analyzed in IBM SPSS Statistics 23. The data analysis took into account the model limitations described in detail in the methodological study (Belyaev et al., 2021).

Before analyzing the results, the variables were tested for normal distribution using the Kolmogorov–Smirnov test. The K‐S test results are shown in Tables 3, 4, 5, 6, 7, 8.

TABLE 3.

Numerical characteristics and length proportions of the vertebral column in artiodactyls

Variable	N	Min	Max	Mean	SD	K‐S test (Sig)	Family		Species
							Min	Max	Min	Max
C+T+L vertebrae number	50	25	27	26.14	.495	.000	Multiple	Multiple	Multiple	Multiple
T vertebrae number	50	12	15	13.32	.768	.000	Camelidae	Hippopotamidae	Multiple	Multiple
L vertebrae number	50	4	7	5.82	.850	.000	Hippopotamidae	Camelidae	Multiple	Multiple
Rf joints number	53	6	7	6.11	.320	.000	Multiple	Multiple	Multiple	Multiple
Tf joints number	50	8	13	10.10	.995	.000	Suina	Giraffidae	S. scrofa dom.	O. johnstoni
RfL joints number	50	6	12	8.94	1.132	.000	Giraffidae	Suina	G. camelopardalis	S. scrofa dom.
Length ratio C/(T+L+S)	47	.204	1.188	.448	.220	.000	Giraffidae	Suina	G. camelopardalis	S. scrofa dom.
Length ratio T/(T+L)	49	.545	.778	.647	.057	.010	Tragulidae	Hippopotamidae	T. javanicus	G. camelopardalis
Length ratio L/(T+L)	49	.222	.455	.353	.057	.010	Hippopotamidae	Tragulidae	G. camelopardalis	T. javanicus
Length ratio Tf/(T+L)	42	.389	.730	.535	.075	.058	Tragulidae	Giraffidae	S. scrofa dom.	G. camelopardalis
Length ratio RfL/(T+L)	42	.270	.611	.465	.075	.058	Giraffidae	Tragulidae	G. camelopardalis	S. scrofa dom.

Abbreviations: C, cervical; L, lumbar; N, number of skeletons involved in respective measurement; S, sacral region; T, thoracic.

TABLE 4.

aROMs in Rf division of the vertebral column

Variable	N	Min (°)	Max (°)	Mean (°)	SD (°)	K‐S test (Sig)	Family		Species
							Min	Max	Min	Max
SB aver	53	10.18	21.35	15.31	2.89	.042	Hippopotamidae	Giraffidae	C. liberiensis	L. guanicoe
SB cum	53	61.1	136.5	93.66	19.21	.024	Hippopotamidae	Giraffidae	C. liberiensis	G. camelopardalis
LB aver	51	15.07	38.01	25.03	4.92	.033	Hippopotamidae	Giraffidae	S. scrofa dom.	G. camelopardalis
LB cum	51	90.4	266.1	153.4	34.19	.000	Hippopotamidae	Giraffidae	S. scrofa dom.	G. camelopardalis
AR aver	52	3.98	7.85	5.92	1.01	.200	Suina	Large antelopes	G. camelopardalis	T. eurycerus
AR cum	52	24.6	47.1	36.14	6.04	.056	Suina	Large antelopes	S. scrofa dom.	T. eurycerus

Abbreviations: aver, average; cum, cumulative.

TABLE 5.

aROMs in Tf division of the vertebral column

Variable	N	Min (°)	Max (°)	Mean (°)	SD (°)	K‐S test (Sig)	Family		Species
							Min	Max	Min	Max
SB aver a	50	4.00	9.10	5.48	1.03	.004	Antilopinae	Suina	S. tatarica	S. scrofa
SB cum	50	42.5	79.1	56.47	9.54	.200	Camelidae	Bovini	O. aries	B. bonasus
LB aver	49	9.25	13.93	11.80	1.11	.054	Hippopotamidae	Large antelopes	C. liberiensis	O. leucoryx
LB aver a	48	9.71	15.41	12.71	1.32	.200	Hippopotamidae	Antilopinae	C. liberiensis	M. moschiferus
LB aver b	48	8.03	13.42	10.78	1.33	.080	Hippopotamidae	Bovini	O. moschatus	S. scrofa dom.
LB cum	49	76.0	145.5	116.93	16.73	.200	Hippopotamidae	Bovini	H. amphibius	B. bonasus
AR aver	48	8.90	13.50	11.35	1.12	.044	Hippopotamidae	Large antelopes	C. liberiensis	O. leucoryx
AR aver a	48	8.98	15.00	12.22	1.37	.200	Hippopotamidae	Antilopinae	C. liberiensis	M. moschiferus
AR aver b	48	7.70	13.00	10.37	1.28	.200	Hippopotamidae	Bovini	O. moschatus	S. tatarica
AR cum	48	73.1	140.2	111.58	16.79	.200	Hippopotamidae	Bovini	H. amphibius	B. bonasus

^a In the anterior half of the Tf division.

^b In the posterior half of the Tf division.

TABLE 6.

aROMs in Tf‐to‐RfL transitional locus of the vertebral column

Variable	N	Min (°)	Max (°)	Mean (°)	SD (°)	K‐S test (Sig)	Family		Species
							Min	Max	Min	Max
SB cum	47	17.82	47.47	33.37	5.53	.200	Hippopotamidae	Caprinae	C. liberiensis	C. capreolus
LB cum	48	26.61	59.94	48.19	6.84	.200	Hippopotamidae	Bovini	C. liberiensis	B. gaurus
AR cum	48	10.56	46.4	28.62	9.13	.200	Hippopotamidae	Bovini	S. scrofa dom.	B. bonasus

TABLE 7.

aROMs in RfL division of the vertebral column and thoracic RfL joints

Variable	N	Min (°)	Max (°)	Mean (°)	SD (°)	K‐S test (Sig)	Family		Species
							Min	Max	Min	Max
SB aver	48	5.96	10.71	8.01	1.18	.026	Hippopotamidae	Antilopinae	O. ammon	C. falconeri
SB aver a	48	5.15	10.33	7.43	1.18	.200	Hippopotamidae	Caprinae	C. bactrianus	C. capreolus
SB cum	48	36.3	86.3	63.45	13.58	.200	Giraffidae	Antilopinae	B. bison	C. capreolus
SB cum a	48	5.9	39.6	15.49	8.33	.049	Giraffidae	Suina	S. caffer	S. scrofa
LB aver	46	7.75	13.93	9.80	1.35	.200	Hippopotamidae	Large antelopes	A. cervicapra	C. gnou
LB aver a	46	6.7	13.9	9.20	1.63	.096	Camelidae	Giraffidae	O. aries	S. caffer
LB cum	46	54.4	114.3	77.65	13.55	.090	Giraffidae	Suina	G. camelopardalis	S. scrofa dom.
LB cum a	46	6.9	52.3	19.42	10.12	.009	Camelidae	Suina	S. scrofa	L. guanicoe
AR aver	46	0.79	6.74	2.55	1.25	.022	Antilopinae	Giraffidae	P. gutturosa	C. gnou
AR cum	46	6.3	49.5	19.96	9.26	.038	Antilopinae	Large antelopes	P. gutturosa	T. pecari

^a In the thoracic RfL joints.

TABLE 8.

aROMs in lumbar region of the vertebral column

Variable	N	Min (°)	Max (°)	Mean (°)	SD (°)	K‐S test (Sig)	Family		Species
							Min	Max	Min	Max
SB aver	48	5.94	11.02	8.22	1.36	.192	Bovini	Antilopinae	T. pecari	A. cervicapra
SB cum	48	25.6	75.7	47.91	11.83	.200	Hippopotamidae	Antilopinae	C. liberiensis	L. guanicoe
LB aver	46	7.72	14.54	10.10	1.48	.200	Hippopotamidae	Large antelopes	A. cervicapra	T. pecari
LB cum	46	33.4	85.2	58.35	10.29	.090	Hippopotamidae	Large antelopes	C. liberiensis	C. gnou
AR aver	46	0.56	6.91	2.51	1.36	.020	Hippopotamidae	Large antelopes	A. cervicapra	C. gnou
AR cum	46	2.26	41.46	14.54	7.75	.200	Hippopotamidae	Large antelopes	H. amphibius	C. gnou

If the K‐S test showed that the distribution is normal, then parametric statistics was used for further analysis. Student's t test (Paired samples) was used to compare the mobility in different loci of the vertebral column. The ANOVA was used to compare the mobility of the vertebral column among various groups of artiodactyls. If the K‐S test showed that the sample does not have a normal distribution, then nonparametric statistics was used. The Wilcoxon signed‐rank test was used to compare mobility in different loci of the vertebral column. The Kruskal–Wallis H test was used to compare the mobility of the vertebral column among various groups of artiodactyls. The Pearson correlation coefficient (r) was used to assess the monotone interrelation among different variables.

Student's t test (Paired samples) and the Wilcoxon signed‐rank test were used to compare mobility in Tf and RfL joints, thoracic and lumbar RfL joints, as well as in joints of anterior and posterior half of the Tf division. We assigned the joint located between the last thoracic vertebra and L1 to the lumbar region. When the number of joints in the Tf division is even, the Tf joints are divided into equal parts between the anterior and posterior half of the Tf division. With an odd number of joints in the Tf division, one more joint is added to the anterior half of the Tf division.

During one‐way ANOVA, three methods of Post Hoc Multiple Comparisons were used: Duncan, Scheffe, and Tukey's b. Taxonomic grouping, running form (by Gambaryan, 1974), habitat, and feeding type were used as grouping variables for ANOVA.

Taxonomic grouping was carried out by families for Hippopotamidae, Camelidae, Giraffidae, and Cervidae. Due to the large number of representatives and diversity of forms, the Bovidae family was divided into four subgroups: two subfamily (Caprinae and Antilopinae), one tribe (Bovini), all other bovids studied by us were combined into the morphotype of large antelopes (representatives of Alcelaphinae, Hippotraginae, and Tragelaphini). We considered representatives of monospecific families together: Moschidae with Cervidae, Antilocapridae with Antilopinae. Musk hogs (Tayassuidae) was analyzed together with Suidae. Final artiodactyls groups: Suina (Suidae + Tayassuidae), Camelidae, Hippopotamidae, Giraffidae, Cervidae (+ Moschidae), Caprinae, Antilopinae (+ Antilocapridae), Bovini, large antelopes (Alcelaphinae, Hippotraginae and Tragelaphini). The representatives of the Tragulidae were not analyzed together with the rest of the artiodactyls due to the concerns expressed in Section 3.4. However, the specificity of aROM of the presacral vertebral column in mouse–deer is considered separately in Section 4.5.

Gambaryan (1974) identified the following six running forms in artiodactyls:

1. Cursorial form is an adaptation to life in open landscapes, characterized by maximum speeds and endurance. Its distinctive features are a shallower trajectory (smaller take‐off angles) of the center of gravity of the body in unsupported stages during gallop rather than during trot or pace, and the method of speed gain mainly via an increase of stride frequency compared to length (typical examples are reindeer, wildebeest, pronghorn, and saiga).

2. Saltatorial–cursorial form—fast but with less endurance than cursorial (running), characterized by a steeper trajectory (larger take‐off angles) of the center of gravity of the body in unsupported stages during gallop rather than during trot or pace. The speed gain is mainly achieved through an increase in stride length (by lengthening unsupported stages) compared to frequency. Typical for gracile forest ungulates (e.g., black‐tailed gazelle; roe deer; mouse–deer).

3. Saltatorial form—running typical to some mountainous species. This form of running is associated with adaptation to large single leaps (e.g., markhor, mountain goat).

4. Mediportal form—running typical for large and heavy artiodactyls (e.g., bovines). The vertical fluctuations of the center of gravity of the body are reduced. The limb contact phase is characterized by decreased limb joint amplitudes and decreased pace angle (i.e., the angle by which the limb as a whole turns around the point of its contact with the ground).

5. Battering‐ram form—typical for robust forest ungulates (e.g., peccary, wild boar). Its features are similar to those of the saltatorial–cursorial form (see above). The difference was not explicitly formulated by Gambaryan, except for somewhat higher limb joint amplitudes than in saltatorial–cursorial running, but the term “battering‐ram” by itself implies low maneuverability.

6. Stilt form—running on extremely tall limbs remaining straightened in the contact phase (e.g., giraffe, camel, moose).

The feeding type was defined by us in the most general form and was divided into four groups: omnivore, browsers, mixed browsers/grazers, and grazers. To determine the type of feeding, we used data on feeding in various artiodactyls (Janis, 1982; Sokolov, 1979; Wilson & Mittermeier, 2011).

The habitat and feeding type were not indicative among the grouping variables we used. Conclusions for these grouping variables most often duplicated taxonomic ones due to the similar sets of animals in the subgroups. The grouping variable by running forms (Gambaryan, 1974) proved to be extremely effective, but only in the RfL division and lumbar region. Taxonomic grouping was found to be indicative in all regions and divisions of vertebral column.

A Hierarchical Cluster (HC) (Z‐Scores, Between‐groups linkage, Euclidean distance) was performed using nine aROM variables (cumulative SB, LB and AR aROMs in Rf, Tf and RfL divisions). We compared the mobility of the vertebral column in representatives of all 10 modern families of even‐toed ungulates, representatives of the family Bovidae were divided into the four groups indicated above (Caprinae, Antilopinae, Bovini, and large antelopes).

4. RESULTS

4.1. Characteristics of vertebral column

The number of presacral vertebrae is stable (25–27) in all families (Table 3). The vertebral formula in representatives of one species usually differs by no more than one vertebra in the thoracic and/or lumbar regions (Table S1).

The cervical region in all representatives consists of seven vertebrae (Figure 3). The transition from the radial type of facets, which is typical for joints starting from C2–C3 to the tangential type of facets in most representatives, takes place on the first thoracic vertebra (T1). A more posterior transition from the Rf to the Tf type taking place on T2 was noted only for peccaries (Tayassu pecari and Pecari tajacu), one of two pygmy hippos (Choeropsis liberiensis), and all three giraffes studied (but not okapi).

FIGURE 3.

Cervical region (C1–T1) in various representatives of artiodactyls. (a) Ovibos moschatus (ZMMU S‐135832), (b) Hippopotamus amphibius (ZIN 24305), (c) Bos gaurus (ZIN 8827), (d) Sus scrofa domestica (ZMMU S‐106943), (e) Bison bonasus (ZMMU S‐193088), (f) Choeropsis liberiensis (ZMMU S‐166224), (g) Tragulus javanicus (ZMMU S‐175329), (h) Moschus moschiferus (ZMMU S‐191852), (i) Gazella subgutturosa (ZMMU S‐150883), (j) Hippotragus niger (ZMMU S‐163601), (k) Cervus elaphus (ZMMU S‐149937), (l) Lama guanicoe (ZMMU S‐113400), (m) Camelus bactrianus (ZIN 11173), (n) Giraffa camelopardalis (ZMMU S‐175340)

The thoracic region in artiodactyls consists of 12–15 vertebrae, the lumbar region of 4–7 vertebrae (Tables S1 and S4) (Figure 4). The Kruskal–Wallis H test indicates statistically significant differences between the groups of artiodactyls in both the number of thoracic (χ ² = 36.805, Sig = 0.000) and lumbar vertebrae (χ ² = 33.365, Sig = 0.000). The group with the least numerous thoracic vertebrae and the most numerous lumbar vertebrae includes Camelidae (T: Mean = 12; L: Mean = 7). The group with the most numerous thoracic vertebrae and the least numerous lumbar vertebrae includes Giraffidae (T: Mean = 14.67; L: Mean = 4.67) and Hippopotamidae (T: Mean = 15; L: Mean = 4).

FIGURE 4.

Thoracolumbar region (T1‐S) in various representatives of artiodactyls. (a) Bison bonasus (ZMMU S‐193088), (b) Hippopotamus amphibius (ZIN 24305), (c) Camelus bactrianus (ZIN 11173), (d) Ovibos moschatus (ZMMU S‐135832), (e) Giraffa camelopardalis (ZMMU S‐175340), (f) Tragulus javanicus (ZMMU S‐175329), (g) Tayassu pecari (ZIN 30967), (h) Moschus moschiferus (ZMMU S‐191852), (i) Capra falconeri (ZMMU S‐181396), (j) Capreolus capreolus (ZMMU S‐117768)

The transition from Tf to RfL divisions always occurs anterior to the boundary between the thoracic and lumbar regions of vertebral column (this boundary is marked by the disappearance of the ribs). The most anterior transition is noted in T9 in one of the two studied domestic pigs, the most posterior transition is noted in T13, T14 in European bison, and Giraffidae (see Table S1).

The number of Tf joints is 8–13, the number of RfL joints shows a twofold variation—6–12 joints (Table 3). The Kruskal–Wallis H test indicates statistically significant differences among various groups of artiodactyls in the number of both Tf (χ ² = 33.686, Sig = 0.000) and RfL joints (χ ² = 25.998, Sig = 0.001). The group with the least numerous Tf and the most numerous RfL joints includes Suina (Tf: Mean = 8.83; RfL: Mean = 10.17). The group with the most numerous Tf and the least numerous RfL joints includes Bovini (Tf: Mean = 11.14; RfL: Mean = 7.86) and Giraffidae (Tf: Mean = 12; RfL: Mean = 6.67).

In various artiodactyls, the length of the cervical region in relation to the trunk length differs almost sixfold (Table S1, Table 3). The Kruskal–Wallis H test indicates statistically significant differences in various groups of ungulates (χ ² = 40.392, Sig = 0.000). Post Hoc Multiple Comparisons indicate that Giraffidae, not surprisingly, form the subset with the maximum neck elongation (Mean = 101.21%); only in giraffes, the neck length exceeds trunk length (106.19%–118.78%). Camelidae form the second subset in terms of neck elongation (Mean = 69.81%). Moreover, the neck length in representatives of the Lama genus (69.93%–77.06%) slightly exceeds that in camels (61.2%–65.4%) and okapi (61.54%). The subset with the shortest cervical region is formed by Suina (Mean = 24.17%), Hippopotamidae (Mean = 26.36%) and Tragulidae (Mean = 28.92%).

The studied material shows that the length of the thoracic region exceeds the length of the lumbar region, on average, almost twice (Table S1, Table 3). The Kruskal–Wallis H test indicates statistically significant differences among various groups of artiodactyls (χ ² = 32.307, Sig = 0.000). The thoracic region makes up the greatest portion of the entire thoracolumbar region in Bovini (Mean = 68.88%), Giraffidae (Mean = 74.77%), and Hippopotamidae (Mean = 75.46%). The lumbar region makes up the greatest portion of the whole thoracolumbar region in Camelidae (Mean = 39.14%), Caprinae (Mean = 40.07%), and Tragulidae (Mean = 43.38%). The most elongated lumbar region (45.5%) was observed in Tragulus javanicus.

The Tf division is slightly shorter, and the RfL division is slightly longer in comparison with the thoracic and lumbar regions, respectively (Table 3). ANOVA indicates statistically significant differences of Tf‐to‐thoracolumbar and RfL‐to‐thoracolumbar length ratios among various groups of artiodactyls (F = 8.337, Sig = 0.000). In Tragulidae (Mean = 44%), Suina (Mean = 46.7%) and Hippopotamidae (Mean = 47.5%), the Tf division is, on average, shorter than the RfL division. The Tf division makes up the smallest portion of the thoracolumbar region in one of the two studied domestic pigs (38.9%). Bovini (Mean = 63.56%) and Giraffidae (Mean = 68.25%) belong to the subset with the relatively longest Tf division.

4.2. aROM distribution in the intervertebral joints

Tables with SB, LB, and AR aROM values in each intervertebral joint for all studied individuals are presented in Tables S4 and S5.

The range of aROM variability per joint is presented in Table S4 with joints sorted by facet type, and in Figure 2 and Table S5 with straightforward joint numbering.

The greatest mobility and the greatest variability of amplitudes in joints are typical for SB and LB aROMs in the cervical region (Figure 2a,b). The greatest AR aROM values are located in the anterior part of the thoracic region where Tf joints are found. The greatest variability of AR aROM is found in joints 16–20 which are of the Tf type in some species and RfL in the others (Figure 2c).

4.3. Vertebral column mobility in even‐toed ungulates

The HC results show that representatives of the families Antilocapridae, Cervidae and the subfamilies Caprinae and Antilopinae have the most similar vertebral columns from an intervertebral mobility perspective (Figure 5). These taxa combine small‐ and medium‐sized animals that are adapted to various habitat conditions. All of these taxa have a fairly similar body build.

FIGURE 5.

Hierarchical Cluster diagram. Comparison of the vertebral column mobility in various even‐toed ungulates taxa. Mobility variables included SB in Rf division, LB in Rf division, AR in Rf division, SB in Tf division, LB in Tf division, AR in Tf division, SB in RfL division, LB in RfL division, and AR in RfL division

Among Pecora, only the representatives of Giraffidae significantly differ from the rest of the taxa in vertebral column mobility. Giraffes are most distinguished from other artiodactyls by their high mobility in the Rf division (SB and LB aROM) and low mobility in the RfL division (SB and LB aROM).

4.4. Mobility diversity

4.4.1. Rf division

Localization of SB and LB aROM in Rf division. The K‐S test shows that the mobility in the joints of the cervical region in our sample does not have a normal distribution (SB: n = 324, Sig = 0.000; LB: n = 312, Sig = 0.001). The Fisher–Pearson coefficient of skewness (SB: 0.884; LB: 0.752) indicates that the distribution is skewed right. The aROM values in the joints of the cervical region are unevenly distributed. The Kruskal–Wallis H test indicates that the differences in average aROM values in joints are statistically significant (SB: χ ² = 37.992, Sig = 0.000; LB: χ ² = 29.488, Sig = 0.000). The mean ranks in the C4–C7 joints (SB: 186.46–198.83; LB: 169.03–187.16) noticeably exceed those in the C2–C4, and C7–T1 joints (SB: 120.44–147.13; LB: 105.82–159.23). Post Hoc Multiple Comparisons distinguish two or three homogeneous subsets among the joints of the cervical region. Joints C2–C3, C3–C4, and C7–T1 belong to the subset with lower mobility (SB: Mean = 13.26–14.82°; LB: Mean = 21.8–25.03°). Joints C4–C5, C5–C6, and C6–C7 belong to the subset of higher mobility (SB: Mean = 16.49–17.09°; LB: Mean = 26.14–26.82°).

SB aROM

The cumulative SB aROM in the Rf division differs by more than twofold in artiodactyls (Table 4). The Kruskal–Wallis H test indicates statistically significant differences between groups of artiodactyls (χ ² = 27.890, Sig = 0.000). The lowest mean rank is typical for Hippopotamidae (13; Mean = 75.53°), Bovini (15.79; Mean = 80.47°), and Suina (18.93; Mean = 83.07°), and the highest for Camelidae (47; Mean = 122.12°) and Giraffidae (50; Mean = 128.27°).

LB aROM

The range of cumulative LB aROM in Rf division differs almost threefold in artiodactyls (Table 4). The Kruskal–Wallis H test indicates statistically significant differences among various groups of artiodactyls (χ ² = 36.878, Sig = 0.000). The lowest mean rank is noted for Hippopotamidae (7.33; Mean = 119.14°) and Suina (11.71; Mean = 123.77°), and the highest for Camelidae (45.33) and Giraffidae (50). According to Post Hoc Multiple Comparisons, only Giraffidae (Mean = 246.53°) belong to the subset with the highest cumulative aROM; Camelidae (Mean = 193.14°) fall into the second subset with the high mobility.

SB and LB aROM have high positive correlations (Pearson r > 0.5) with the absolute length of the neck and especially with the length of the neck relative to trunk length (Table 9), as well as with each other (Table 10).

TABLE 9.

The Pearson correlation coefficient (r) of aROMs in joint divisions (vertical table dimension) vs numeric and metric characteristics of the vertebral column (horizontal table dimension)

		Number of vertebrae		Number of joints			Absolute lengths									Length ratios
		T	L	Rf	Tf	RfL	C	T	L	S	Rf	Tf	RfL	T+L+S	T+L	C/ (T+L+S)	T /(T+L)	Tf /(T+L)
Rf	SB cum	−.175	.164	.437	.132	−.207	.617	.006	.045	−.200	.577	.008	−.161	−.045	.018	.762	−.017	.156
	LB cum	−.157	.058	.519	.365	−.466	.826	.288	.272	.117	.805	.309	−.015	.224	.295	.883	.135	.415
	AR cum	−.239	.187	−.172	.391	−.411	−.084	−.034	.049	−.056	−.018	−.086	−.177	−.068	−.010	−.167	−.183	.009
Tf	SB aver a	.067	−.184	−.087	−.139	.046	−.141	.143	.041	.233	−.134	.121	.103	.176	.118	−.316	.194	−.013
	SB cum	.060	−.108	−.033	.274	−.296	−.020	.183	.061	.251	−.022	.258	−.069	.203	.153	−.181	.148	.192
	LB aver	−.187	.205	−.121	.225	−.114	.099	−.112	−.013	−.193	.099	−.012	−.148	−.078	−.086	.253	−.216	.020
	LB cum	−.118	.096	.020	.627	−.534	.244	.122	.141	.044	.228	.319	−.169	.132	.133	.292	−.028	.544
	AR aver	−.162	.105	−.132	−.008	.011	−.057	−.109	−.066	−.084	−.047	−.012	−.147	−.045	−.100	.007	−.123	−.026
	AR cum	−.149	.078	−.305	.550	−.400	−.092	.062	.102	.059	−.118	.228	−.124	.105	.077	−.118	−.054	.469
Joints 16–20	SB cum	−.386	.454	−.221	−.381	.462	−.336	−.470	−.268	−.393	−.323	−.414	−.270	−.406	−.428	−.180	−.548	−.486
	LB cum	−.176	.202	−.196	.281	−.140	−.142	.020	.122	.063	−.142	.143	−.086	.086	.053	−.172	−.233	.212
	AR cum	.008	−.031	.099	.785	−.678	.272	.353	.308	.297	.256	.484	−.035	.347	.354	.142	.107	.696
RfL	SB RfL aver	−.400	.425	−.225	−.079	.170	−.145	−.467	−.220	−.473	−.155	−.394	−.321	−.431	−.414	.160	−.492	−.221
	SB L aver	−.338	.330	−.225	−.129	.185	−.162	−.411	−.216	−.426	−.179	−.402	−.255	−.411	−.371	.091	−.404	−.269
	SB RfL cum	−.370	.531	−.314	−.593	.749	−.413	−.594	−.246	−.531	−.405	−.625	−.108	−.511	−.515	−.129	−.632	−.723
	SB L cum	−.685	.783	−.407	−.123	.326	−.119	−.447	.038	−.459	−.141	−.365	−.181	−.358	−.317	.097	−.778	−.316
	LB RfL aver	.132	−.112	.189	.216	−.225	−.092	−.001	−.054	−.010	−.078	.097	−.167	.008	−.016	−.072	.098	.295
	LB L aver	.179	−.216	.232	.054	−.150	−.184	−.013	−.130	−.028	−.174	.054	−.150	−.039	−.050	−.200	.182	.197
	LB RfL cum	.029	.228	−.086	−.528	.656	−.469	−.366	−.182	−.312	−.466	−.395	−.004	−.308	−.326	−.401	−.301	−.523
	LB L cum	−.514	.648	−.241	.028	.192	−.162	−.246	.169	−.272	−.170	−.083	−.101	−.140	−.128	−.102	−.605	−.047
	AR RfL aver	.148	−.119	.308	.225	−.257	.066	.118	.036	.049	.079	.157	−.080	.094	.098	.041	.175	.308
	AR L aver	.073	−.053	.307	.137	−.184	.009	.032	−.009	−.041	.019	.092	−.123	.004	.021	.001	.099	.236
	AR RfL cum	.114	.021	.211	−.046	.078	−.102	−.030	−.008	−.045	−.075	−.023	−.029	−.006	−.024	−.090	.008	.012
	AR L cum	−.137	.217	.123	.121	−.057	−.008	−.033	.095	−.108	−.004	.056	−.077	−.018	.006	−.006	−.153	.143

The higher is the positive correlation, the darker brown is the cell, and the higher is the magnitude of negative correlation, the darker blue is the cell. The cells with insignificant correlations are retained white.

^a Average SB was here taken into account for only the anterior half of the Tf division; other abbreviations as in Tables 3 and 4.

TABLE 10.

The Pearson correlation coefficient (r) between aROMs within the vertebral column

		Rf			Tf						Joints 16–20			RfL
		SB cum	LB cum	AR cum	SB aver a	SB cum	LB aver	LB cum	AR aver	AR cum	SB cum	LB cum	AR cum	SB RfL aver	SB L aver	SB RfL cum	SB L cum	LB RfL aver	LB L aver	LB RfL cum	LB L cum	AR RfL aver	AR L aver	AR RfL cum	AR L cum
Rf	SB cum		.860	.179	−.248	−.174	.040	.101	.081	−.027	.094	.024	.148	.248	.191	.049	.222	.039	−.020	−.126	.121	.121	.119	.043	.140
	LB cum	.860		.143	−.248	−.041	.182	.390	.197	.129	−.087	.036	.362	−.040	−.010	−.252	.029	.049	−.050	−.333	−.008	.150	.122	−.012	.098
	AR cum	.179	.143		−.203	.138	−.020	.315	.008	.240	.028	.202	.425	.202	.188	−.106	.180	.118	.049	−.236	.113	.138	.110	.009	.111
Tf	SB aver a	−.248	−.248	−.203		.704	.113	.038	.126	.045	−.009	.020	.082	−.272	−.260	−.140	−.309	.131	.226	.130	−.028	.088	.081	.081	.030
	SB cum	−.174	−.041	.138	.704		.286	.475	.264	.371	.210	.316	`.368	−.128	−.180	−.252	−.188	.203	.226	−.067	.079	.100	.090	.002	.064
	LB aver	.040	.182	−.020	.113	.286		.783	.986	.726	.278	.437	.201	.074	.021	.029	.079	.184	.181	.138	.247	.031	.079	.035	.106
	LB cum	.101	.390	.315	.038	.475	.783		.780	.913	.091	.573	.689	.013	−.064	−.309	−.010	.269	.199	−.213	.203	.176	.185	.004	.180
	AR aver	.081	.197	.008	.126	.264	.986	.780		.747	.290	.470	.241	.121	.063	.068	.127	.206	.172	.137	.270	.050	.078	.048	.116
	AR cum	−.027	.129	.240	.045	.371	.726	.913	.747		.079	.654	.657	.093	.031	−.176	.096	.306	.245	−.095	.301	.181	.193	.045	.211
Joints 16–20	SB cum	.094	−.087	.028	−.009	.210	.278	.091	.290	.079		.277	−.128	.611	.484	.708	.570	.031	.039	.380	.380	−.142	−.074	.024	.051
	LB cum	−.024	.036	.202	.020	.316	.437	.573	.470	.654	.277		.736	−.004	−.122	−.086	.017	.704	.605	.421	.617	.525	.495	.505	.526
	AR cum	.148	.362	.425	−.082	`.368	.201	.689	.241	.657	−.128	.736		−.147	−.235	−.510	−.172	.556	.432	−.124	.304	.559	.493	.349	.459
RfL	SB RfL aver	.248	−.040	.202	−.272	−.128	.074	.013	.121	.093	.611	−.004	−.147		.957	.778	.873	−.293	−.352	−.108	.069	−.335	−.306	−.297	−.188
	SB L aver	.191	−.010	.188	−.260	−.180	.021	−.064	.063	.031	.484	−.122	−.235	.957		.756	.842	−.406	−.431	−.191	−.074	−.437	−.415	−.405	−.315
	SB RfL cum	.049	−.252	−.106	−.140	−.252	.029	−.309	.068	−.176	.708	−.086	−.510	.778	.756		.793	−.346	−.334	.338	.172	−.392	−.324	−.156	−.162
	SB L cum	.222	.029	.180	−.309	−.188	.079	−.010	.127	.096	.570	.017	−.172	.873	.842	.793		−.327	−.399	−.005	.323	−.341	−.286	−.243	−.069
	LB RfL aver	.039	.049	.118	.131	.203	.184	.269	.206	.306	.031	.704	.556	−.293	−.406	−.346	−.327		.930	.583	.640	.916	.886	.867	.833
	LB L aver	−.020	−.050	.049	.226	.226	.181	.199	.172	.245	.039	.605	.432	−.352	−.431	−.334	−.399	.930		.588	.597	.855	.892	.830	.810
	LB RfL cum	−.126	−.333	−.236	.130	−.067	.138	−.213	.137	−.095	.380	.421	−.124	−.108	−.191	.338	−.005	.583	.588		.654	.482	.520	.730	.585
	LB L cum	.121	−.008	.113	−.028	.079	.247	.203	.270	.301	.380	.617	.304	.069	−.074	.172	.323	.640	.597	.654		.577	.650	.674	.815
	AR RfL aver	.121	.150	.138	.088	.100	.031	.176	.050	.181	−.142	.525	.559	−.335	−.437	−.392	−.341	.916	.855	.482	.577		.967	.937	.913
	AR L aver	.119	.122	.110	.081	.090	.079	.185	.078	.193	−.074	.495	.493	−.306	−.415	−.324	−.286	.886	.892	.520	.650	.967		.933	.956
	AR RfL cum	.043	−.012	.009	.081	.002	.035	.004	.048	.045	.024	.505	.349	−.297	−.405	−.156	−.243	.867	.830	.730	.674	.937	.933		.926
	AR L cum	.140	.098	.111	.030	.064	.106	.180	.116	.211	.051	.526	.459	−.188	−.315	−.162	−.069	.833	.810	.585	.815	.913	.956	.926

Abbreviations and coloration as in Table 9.

AR aROM

The variability of the cumulative AR aROM in various artiodactyls is within 25° (24.6–47.1°). ANOVA indicates a statistically significant difference in cumulative aROMs in various groups of artiodactyls (F = 3.186, Sig = 0.005). However, Post Hoc Multiple Comparisons make it possible to separate only pigs (Mean = 30.9°) and large antelopes (Mean = 43.1°).

4.4.2. Tf division

Student's t test (Paired samples) shows that the average LB aROM in the joints of the anterior half of the Tf division statistically is significantly greater than the aROM in the posterior half of the Tf division (n = 48, Mean Diff = 2.05°, t = 9.155, Sig = 0.000, 95% Confidence Interval of the Difference from 1.6° to 2.5°) (Table 5).

SB aROM

The average mobility in the anterior half of the Tf division in artiodactyls differs by more than twofold (Table 5). The highest average mobility was observed in wild boars, wildebeest, hippos, American and European bison, and warthog (6.45–9.15°), the lowest in Antilopinae and sheep (<5°).

The Kruskal–Wallis H test indicates statistically significant differences in the average mobility in the anterior half of the Tf division in various groups of artiodactyls (χ ² = 23.616, Sig = 0.003). The lowest mean rank is typical for Antilopinae (9.9; Mean = 4.56°) and Giraffidae (13.5; Mean = 4.90°), and the highest for Hippopotamidae (38; Mean = 6.15°) and Suina (39.43; Mean = 6.65°). Mobility in the anterior half of the Tf division has a negative correlation (r = −0.316, Sig = 0.035) with the length of the neck relative to trunk length (Table 9) and cumulative SB aROM in the lumbar region (r = −0.309, Sig = 0.031) (Table 10).

The cumulative SB aROM in the Tf division differs almost twofold in various artiodactyls (Table 5). ANOVA indicates statistically significant differences in cumulative aROM in various groups of artiodactyls (F = 2.457, Sig = 0.025). However, in homogeneous subsets (by Duncan), only Camelidae and Antilopinae (Mean = 47.9–47.92°) differ significantly from Bovini (Mean = 65.5°).

LB aROM

The cumulative LB aROM in the Tf division in artiodactyls differs twofold, and the average LB aROM in Tf division differs less than twofold (Table 5). ANOVA indicates statistically significant differences in cumulative LB aROM in various groups of artiodactyls (F = 8.385, Sig = 0.000). According to Post Hoc Multiple Comparisons, the subset with low cumulative aROM includes Hippopotamidae (Mean = 84.48°) with high cumulative aROM large antelopes (Mean = 131.72°), Giraffidae (Mean = 133.46°) and Bovini (Mean = 136.33°). Average LB aROMs statistically differ insignificantly (F = 2.088, Sig = 0.055); by Post Hoc Multiple Comparisons, and only Hippopotamidae (Mean = 9.74°) are distinguished into a separate subset with the lowest aROM.

AR aROM

The cumulative AR aROM in the Tf division in artiodactyls differs twofold while the average differs less than twofold (Table 5). Both the average (F = 2.510, Sig = 0.023) and cumulative (F = 6.682, Sig = 0.000) amplitudes of the AR statistically differ significantly in the groups of artiodactyls. According to Post Hoc Multiple Comparisons, the subset with low average AR aROM includes (by Tukey's b and Duncan) Hippopotamidae (Mean = 9.04°). The subset with low cumulative aROM includes Hippopotamidae (Mean = 78.4°), and the subset with high cumulative aROM includes large antelopes and Bovini (Mean = 127.02°, Mean = 131.47°).

4.4.3. aROM in transitional locus from Tf to RfL division

The transition between the Tf and RfL type of zygapophyses occurs in the studied artiodactyls from the 16th joint (T9–T10) to the 20th joint (T13–T14) (Table S1).

SB aROM

The cumulative SB aROM differs by two and a half times in the studied artiodactyls (Table 6). ANOVA indicates statistically significant differences among various groups of artiodactyls (F = 3.139, Sig = 0.008). According to Post Hoc Multiple Comparisons (by Tukey's b and Duncan), the subset with the lowest cumulative aROM includes Hippopotamidae (Mean = 26.19°) and Giraffidae (Mean = 26.58°). The subset with high cumulative aROMs includes Cervidae (Mean = 36.29°), and Caprinae (Mean = 37.75°). By the running form, ANOVA indicates significant differences in cumulative aROM in the studied artiodactyls (F = 2.696, Sig = 0.035). Post Hoc Multiple Comparisons distinguishes (by Tukey's b and Duncan) the saltatorial running form (Mean = 41.82°) as subset with the highest cumulative aROM.

SB aROM in the locus from the 16th to the 20th joints has significant negative correlations with almost all linear size characteristics of animals (r from −0.323 to −0.47) (see Table 9). SB aROM in the locus from the 16th to the 20th joints also has high positive correlations with the average and cumulative SB aROM in the RfL division and lumbar region (r from 0.484 to 0.708) (Table 10).

LB aROM

The range of the cumulative LB aROM in the transitional locus differs twofold (Table 6). ANOVA indicates statistically significant differences among various groups of artiodactyls (F = 7.583, Sig = 0.000). According to Post Hoc Multiple Comparisons, the subset with the lowest cumulative aROM includes Hippopotamidae (Mean = 33.57°). The subset with the highest aROM includes large antelopes (Mean = 53.2°) and Bovini (Mean = 55.91°). By the running form, ANOVA indicates significant differences among various groups of artiodactyls (F = 3.378, Sig = 0.012). The subset with the lowest aROM includes the stilt running form (Mean = 44.06°). The subset with the highest aROM includes the mediportal running form (Mean = 54.75°).

AR aROM

The range of cumulative AR aROM in the transitional locus differs almost fivefold (Table 6). ANOVA indicates statistically significant differences among various groups of artiodactyls (F = 8.007, Sig = 0.000). According to Post Hoc Multiple Comparisons, the subset with the lowest cumulative aROM includes Hippopotamidae (Mean = 16.31°) and Suina (Mean = 21.67°). The subset with the highest aROMs includes large antelopes (Mean = 35.6°), Giraffidae (Mean = 38.53°) and Bovini (Mean = 42.34°). By the running form, ANOVA indicates significant differences among various groups of artiodactyls (F = 5.323, Sig = 0.001). The subset with the lowest aROM includes the battering‐ram running form (Mean = 21.67°). The subset with the highest aROM includes the mediportal running form (Mean = 40.62°).

AR aROM in the locus from the 16th to the 20th joints has a high negative correlation with the cumulative SB aROM in the RfL division (r = −0.510) (Table 10).

4.4.4. RfL division

The RfL division is considered both in full and separately for the thoracic RfL and lumbar RfL joints.

Student's t test (Paired samples) shows that the average SB aROM in the RfL division statistically significantly exceeds SB aROM in the Tf division (n = 50, Mean Diff = 2.49°, t = 10.476, Sig = 0.000, 95% Confidence Interval of the Difference from 2.02° to 2.97°); LB and AR aROM in the RfL division are statistically significantly inferior to LB and AR aROM in the Tf division (LB: n = 48, Mean Diff = −1.99°, t = −8.518, Sig = 0.000, 95% Confidence Interval of the Difference from −2.46° to −1.52°; AR: n = 48, Mean Diff = −8.82°, t = −36.719, Sig = 0.000, 95% Confidence Interval of the Difference from −9.33° to −8.36°).

Student's t test (Paired samples) shows the average aROM in the lumbar region slightly, yet statistically and significantly, exceeds aROM in the thoracic RfL joints in SB aROM (n = 50, Mean Diff = 0.80°, t = 3.986, Sig = 0.000, 95% Confidence Interval of the Difference from 0.40° to 1.21°) and LB aROM (n = 47, Mean Diff = 0.88°, t = 4.265, Sig = 0.000, 95% Confidence Interval of the Difference from 0.46° to 1.29°).

SB aROM

Among various representatives of artiodactyls, the cumulative SB aROM in the RfL division and lumbar region differs more than twofold, and the average SB aROM differs less than twofold (Tables 7 and 8).

ANOVA shows that the average SB aROM in the groups of artiodactyls statistically is significantly different both in cumulative aROM values (RfL: F = 6.606, Sig = 0.000; Lumbar: F = 7.448, Sig = 0.000) and average aROM values (RfL: F = 2.983, Sig = 0.010; Lumbar: F = 3.172, Sig = 0.007).

RfL division. According to Post Hoc Multiple Comparisons (by Tukey's b and Duncan), the subset of animals with the lowest average per joint aROM values include Hippopotamidae (Mean = 6.92°) and Bovini (7.05°). The subset of animals with the lowest cumulative aROM values include Giraffidae (Mean = 42.20°) and Bovini (Mean = 48.44°). Antilopinae belong to the subset with the highest average (Mean = 9.46°) and cumulative aROM (Mean = 75.70°). ANOVA shows that the average and cumulative SB aROM statistically differ significantly in artiodactyls using different running forms (average: F = 3.180, Sig = 0.017; cumulative: F = 4.583, Sig = 0.002). The subset with the lowest mobility in joints includes the species adapted to the mediportal running form (average Mean = 7.12°; cumulative Mean = 49.95°). The subset with the highest mobility in joints includes species adapted to the saltatorial–cursorial (average Mean = 8.62°; cumulative Mean = 71.89°) and saltatorial (average Mean = 9.84°; cumulative Mean = 73.40°) running forms.

Lumbar region. According to Post Hoc Multiple Comparisons, the subset of animals with the lowest average aROM values includes Bovini (7.08°). The subset of animals with the lowest cumulative aROM values includes Hippopotamidae (30.47°) and Giraffidae (34.60°). The subsets with high average and cumulative aROM include Antilopinae (average Mean = 10.18°, cumulative Mean = 61.10°). Beside Antilopinae, the subset with high cumulative aROM also includes Caprinae (Mean = 54.81°) and Camelidae (Mean = 60.25°). ANOVA shows that the average and cumulative SB aROM statistically differ significantly in artiodactyls using different running form (average: F = 2.500, Sig = 0.047; cumulative: F = 3.317, Sig = 0.014). Species adapted to the mediportal running forms (average Mean = 7.12°; cumulative Mean = 40.18°) belong only to the subset with minimum aROM. The subset with the highest aROM includes species adapted to the saltatorial–cursorial (average Mean = 8.92°; cumulative Mean = 56.46°) and saltatorial (average Mean = 9.73°; cumulative Mean = 58.40°) running forms. Regarding the habitat (ANOVA: F = 4.314, Sig = 0.009), mountain species (Mean = 56.11°) belong to the subset with an increased cumulative aROM.

Both average and cumulative SB aROM have significant negative correlations with all variables reflecting the linear dimensions of the vertebral column (Pearson r from −0.317 to −0.625) (Table 9). As well as negative correlations with AR aROM in the RfL division and lumbar region (r from −0.297 to −0.437, Sig from 0.045 to 0.003) (Table 10).

LB aROM

The cumulative LB aROM in both the lumbar region and the RfL division differs in artiodactyls more than twofold, and the average LB aROM differs less than twofold (Tables 7 and 8).

ANOVA indicates that the average values in various groups of artiodactyls are statistically significant, different only in the cumulative aROM (RfL: F = 3.430, Sig = 0.005; Lumbar: F = 5.324, Sig = 0.000).

RfL division. According to Post Hoc Multiple Comparisons, the subset with the minimum cumulative aROM includes Giraffidae (Mean = 55.2°), the subset with the maximum cumulative aROM includes Suina (Mean = 94.32°).

Lumbar region. According to Post Hoc Multiple Comparisons, the subset with the minimum cumulative aROM includes Hippopotamidae (Mean = 36.29°) and Giraffidae (Mean = 43.60°), the subset with the maximum cumulative aROM includes large antelopes (Mean = 67.04°).

The cumulative LB aROM in the RfL division has negative correlations with the linear dimensions of the vertebral column (Pearson r from −0.308 to −0.469) (Table 9).

AR aROM

The variation of AR aROM both average and cumulative in the RfL division is low (Table 7). ANOVA does not distinguish statistically significant differences in the average AR aROM values among various groups of artiodactyls (both in average and cumulative AR aROM) for any of the grouping variables.

Average AR aROM in the RfL division and lumbar region has significant negative correlations with average and cumulative SB aROM in the RfL division and lumbar region (r from −0.297 to −0.437, Sig from 0.047 to 0.003) (Table 10).

4.5. Vertebral mobility in Tragulidae

Representatives of the Tragulidae family were subtracted from the analysis of other artiodactyls due to the concerns regarding the precision of measurements of such small vertebrae, as expressed in Section 3.4. However, in this paragraph, we attempt to consider tragulid distinctive features but cautiously.

We did not find any remarkable features of the calculated aROMs in the Rf and Tf divisions in Tragulidae. On the other hand, Tragulidae strongly differ from other artiodactyls in terms of mobility in the transitional locus (joints 16–20) and in the RfL division. In Tragulidae, in the transitional locus of the vertebral column, the cumulative mobility of SB aROM is the highest among all studied species (Mean = 47.31°). This value is almost 10° more to the respective maximum among non‐tragulid artiodactyls (Caprinae Mean = 37.75°). The cumulative LB aROM in transitional locus of Tragulidae (Mean = 55.84°) is close to the maximum found in other artiodactyls (53.2–55.91° in large antelopes and Bovini).

Both the cumulative and average values of SB and LB aROMs in the RfL division and lumbar region of the vertebral column are the highest among the studied artiodactyls. The cumulative SB aROM in the RfL division of Tragulidae (Mean = 94.36°) exceeds the respective value of Antilopinae by ~19° and of Caprinae by ~24°. The cumulative LB aROM in the RfL division of Tragulidae (Mean = 103.02°) exceeds this value in Suina by ~9° and in large antelopes by ~22°. Cumulative SB aROM in the lumbar region (Mean = 70.65°) exceeds this value in Antilopinae by ~9.5° and in Camelidae by ~10.5°; the cumulative LB aROM in the lumbar region (Mean = 75.65°) exceeds this value in large antelopes by ~8.5° and in Camelidae by ~12°.

Also, in Tragulidae, the morphology of the spinous processes in the lumbar region differs markedly. They do not have any pronounced expansion of the tip in the anteroposterior direction (see Supplementary Material S2) and visually their spinous processes are more similar to those of carnivores than artiodactyls. This may be due to the small size and weight of the mouse deer, which do not require development of a passive ligamentous framework to strengthen the vertebral column, and the lumbar region in particular.

5. DISCUSSION

5.1. Some methodological aspects

5.1.1. Sensitivity of the calculation formula to injuries and pathologies

Among studied individuals, we noted a guanaco specimen (ZMMU S‐113400) which has the consequences of a serious intravital traumatic event in the C5–C6 joint (see Figure 3l and Supplementary Material S2). The injury is represented by large ossification on the ventral side between the vertebral bodies of vertebrae C5 and C6. Ossification severely limited mobility in the joint, but did not completely limit it. As a result, this injury affected the size of the zygapophyseal facets. The amplitude of SB and LB in the C5–C6 joint of this guanaco specimen (SB = 12.5°; LB = 22.5°) significantly differs from all other studied Camelidae (n = 5: SB = 20.8–32.4°; LB = 34.5–41.6°) (see Tables S4 and S5).

This example indicates that in adult animals with pathologies in the joints of the vertebral column, the pathologies are reflected in the size and geometry of the zygapophyseal facets. The effect of these injuries on the aROM can be adequately quantified with the method which we use according to the previous evaluation and validation (Belyaev et al., 2021).

5.2. Cervical region and hypermobility

The cervical region is the most mobile region of the presacral vertebral column in terms of SB and LB aROM (Figure 2a,b). Average SB (15.31°) and LB (25.03°) amplitudes in the Rf joints significantly exceed average SB and LB amplitudes in the Tf (SB: 5.48°; LB: 11.80°) and RfL joints (SB: 8.01°; LB: 9.80°). The neck of artiodactyls is the main manipulator for interacting with the habitat.

The length of the cervical region relative to trunk length differs almost six times in artiodactyls. On average, the cervical region is slightly shorter than half of the trunk length—44.8% in the studied artiodactyls. Pigs, mouse–deer, and hippos have the shortest necks (less than 30% of trunk length). The length of the cervical region exceeds 60% of the length of the thoracolumbar and sacral region in camels and okapis. In llamas, the length of the cervical region is equal to 2/3–3/4 of the length of the trunk. In giraffes, the length of the cervical region even exceeds the length of the trunk (Figure 3; Supplementary Material S2).

The Rf type is present in typical cervical joints (C2–T1) in artiodactyls (Slijper, 1946; Virchow, 1907). In almost all cases, the transition from radial to tangential type of facets in artiodactyls occurs on the first thoracic vertebra (T1). The only exceptions are giraffes (but not okapi), peccaries, and one of the two studied pygmy hippos. In these artiodactyls, an additional T1–T2 joint has Rf‐type zygapophyses, and the transition from the Rf to Tf type occurs on the second thoracic vertebra (T2).

We are not aware of studies of the mobility of the occipital‐atlas joint in mammals. The most mobile point of the neck in artiodactyls (Wilke et al., 1997a, 2011) is the atlas‐axis joint which is synovial contrary to all other intervertebral joints of mammals (Table 11). AR aROM in the atlas‐axis joint exceeds cumulative AR aROM in all other joints of the cervical region, and LB aROM in the atlas‐axis joint exceeds average LB aROM in the cervical region only in sheep, while SB aROM in the atlas‐axis joint varies from average in the cervical region (in pigs) to very high (in sheep) (Table 11).

TABLE 11.

Comparison of in vitro aROM in the atlas‐axis joint (C1–C2) and in other (Rf) joints of the cervical region in various mammals

Species	SB aROM (°)		LB aROM (°)		AR aROM (°)
	C1–C2	Rf joints (average)	C1–C2	Rf joints (average)	C1–C2	Rf joints (average)
Homo sapiens a	23.8	11.98	8.3	10.54	75.9	11.92
Ovis aries b	50.32	14.53	34.52	24.02	98.04	10.88
Sus scrofa c	15.1	12.18	9	14.1	58.2	4.03

^a Wen et al. (1993).

^b Wilke et al. (1997a).

^c Wilke et al. (2011).

In the post‐axis cervical region, mobility is unevenly distributed in artiodactyls (Figure 2a,b). The greatest amplitudes of SB and LB are observed in the posterior neck joints (C4–C5, C5–C6, and C6–C7 joints). The aROM values are on average 2.5–3.5° lower in more anterior joints (C2–C3 and C3–C4) and in the neck–thorax joint (C7–T1).

SB and LB aROM have the maximum variability in the cervical joints. Average SB amplitude in the Rf joints has SD = 2.89°, average LB amplitude SD = 4.92°. In all other parts of the vertebral column, SD is less than 2° (see Tables 4, 5, 6, 7, 8).

The cumulative mobility in the Rf division among various artiodactyls differs in SB aROM more than twofold and in LB aROM almost threefold. Mobility in the cervical region has a very high correlation in artiodactyls with elongation of the cervical region relative to trunk length (Figure 6). Moreover, the neck/trunk length ratio has a higher correlation with LB aROM (Pearson r = 0.884) than with SB aROM (Pearson r = 0.781).

FIGURE 6.

Mobility in the cervical region in artiodactyls. (a) SB aROM; (b) LB aROM. Abscissa axis represents the neck elongation as a ratio (%) of the cervical length to the trunk length (T+L+S). Ordinate axis represents the cumulative mobility (°) in the cervical intervertebral joints. The mean values for all studied species are taken for the point of axes intersection (neck elongation Mean = 44.8%; cumulative SB aROM Mean = 93.66°; cumulative LB aROM Mean = 153.4°). The circles’ colors indicate the taxonomic group: Suidae (red), Tayassuidae (red/white), Camelidae (purple), Giraffidae (orange), Hippopotamidae (black), Tragulidae (lilac), Antilocapridae (turquoise), Moschidae (pink), Caprinae (azure), Antilopinae (pale green), Bovini (blue), large antelopes (green)

The least mobile Rf joints are typical for animals with short necks and large, heavy heads: Suina, Hippopotamidae, and Bovini (Figure 6; Tables S4 and S5). Similarly, low SB mobility was previously noted for the black rhinoceros (Belyaev, 2018). It is interesting to note that some Bovini, particularly African and Asian buffaloes, have one joint with a strongly increased aROM (especially SB), due to the greatly increased length of the articular facets of postzygapophyses. In the African buffalo, C4–C5 SB aROM is 23° versus Mean = 11.7° in the five remaining joints, and in the Asian buffalo C5–C6 SB aROM is 22.4° versus Mean = 10.97° in the five remaining joints, while in the gaur C7–T1 SB aROM is 18.2° versus Mean = 12.5° in the five remaining joints (Tables S4 and S5).

The most mobile Rf joints are typical for the longest‐necked artiodactyls—Camelidae and Giraffidae (Figure 6). This is consistent with the data of other researchers (Dzemski & Christian, 2007; Müller et al., 2021; Stolworthy et al., 2015). Calculated aROM values (SB, LB, and AR) for llamas and guanacos are very close to in vitro data for llamas and alpacas obtained by Stolworthy et al. (2015) (Table 12). This confirms the advantage of our choice of using pan‐artiodactyl values for the K _R and K _S coefficients for calculating aROM.

TABLE 12.

Lateral mobility in the neck of llamas and alpaca obtained by direct measurement on syndesmological vertebral units and by calculation

Species	LB aROM (°)
	In vitro a			Calculated using different values of K R and K S coefficients
				Sus coefficients			Ovis coefficients			General coefficients
	Min	Max	Mean	Min	Max	Mean	Min	Max	Mean	Min	Max	Mean
Lama glama	29.7	35	32.8	15.8	36.1	27.99	21.7	47.3	37.51	19.2	41.6	33.02
Lama guanicoe	N/A	N/A	N/A	17.8	33.8	25.91	25.7	46	35.48	22.5	40.3	32.57
Vicugna pacos	13.3	36.4	28.4	N/A	N/A	N/A	N/A	N/A	N/A	N/A	N/A	N/A

Bold is used to highlight the mean values.

^a Stolworthy et al. (2015); joints number 2, 3, and 5 were tested for L. glama, and 3–7 for V. pacos, but aROM values for individual joints were not presented.

In all studied giraffes, the Rf type of zygapophyses characterized by a V‐shaped orientation in the transverse plane is found in an additional T1–T2 joint. The unique morphology of the vertebrae and joints in the C6–T2 locus in giraffes was considered by researchers as an argument for the inclusion of vertebra in the cervical region. So Lankester (1908) believed that T1 of the giraffe is cervicalized, and Solounias (1999) believed that the giraffe's neck truly has one additional vertebra added in the neck in the interval of C2–C6. A solid argument supporting the cervicalization of T1 has been presented in recent studies (Danowitz & Solounias, 2015; Müller et al., 2021). The hypothesis that the T1–T2 joint functions as an additional neck joint in giraffes is supported by data obtained by Gunji and Endo (2016). The SB aROM in the T1–T2 joint is reduced compared to the anterior joints (C6–C7 and C7–T1), but it is still three times higher than the aROM in the subsequent thoracic joints. Our data are in good agreement with those of Gunji and Endo (2016). On average, the SB and LB aROMs calculated for the T1–T2 joint (n = 3, SB: Mean = 10.8°; LB: Mean = 25.9°) in giraffes are lower than in other joints of the Rf division (SB: Mean = 15–25.8°; LB: Mean = 30.5–41.8°), but higher than in the three subsequent Tf joints of the thorax (SB: Mean = 4.8–6°; LB: Mean = 12.7–14.7°) (Tables S4 and S5). In silico estimates of SB mobility by Müller et al. (2021) in C7–T1 joint (55.2°), are at least a twofold overestimation.

In the neck, LB aROMs in artiodactyls are noticeably higher than SB aROMs; AR aROMs, on the contrary, are limited in the Rf division in artiodactyls (Stolworthy et al., 2015; Wilke et al., 2011).

5.2.1. Features of joint morphology in the cervical region in Giraffidae and Camelidae

It is interesting to note that morphological adaptations to the greatest increase in the SB and LB aROM in artiodactyls are realized in different ways in Giraffidae and Camelidae.

Connection of the vertebral bodies. In camels and llamas, the anterior and posterior end‐plates of the cervical vertebrae bodies are slightly convex (Figure 3l,m, Supplementary Material S2). With this design, the largest thickness of the intervertebral disc is observed in the annulus fibrosus, and the smallest in the nucleus pulposus (Stolworthy et al., 2015). An increase in the length of the annulus fibrosus fibers leads to an increase in the possible displacement of the vertebral bodies relative to each other. In giraffes and okapi, the vertebrae are clearly opisthocoelous—concave posterior end‐plate and convex anterior end‐plate. This convexity is the sharpest among all artiodactyls (see Figure 3, Supplementary Material S2).

The connection of the articular processes. In Camelidae, an elongation of the arc of motion occurs due to increase in the facet lengths of the prezygapophyses. Student's t test (Paired samples) shows that the facet lengths of the prezygapophyses of each neck vertebra significantly exceed the facet lengths of the postzygapophyses of the preceding vertebra (n = 72, Mean Diff = 5.593 mm, t = 9.802, Sig = 0.000, 95% Confidence Interval of the Difference from 4.455 to 6.731 mm). In Giraffidae, on the contrary, an increase in the aROM occurs due to an increase in the facet lengths of the postzygapophyses as compared to the prezygapophyses of the next vertebra. Student's t test (Paired samples) shows that the facet lengths of the postzygapophyses significantly exceed the facet lengths of the prezygapophyses (n = 48, Mean Diff = 9.925 mm, t = 8.135, Sig = 0.000, 95% Confidence Interval of the Difference from 7.463 to 12.379 mm).

Geometrically, the center of interaction of the postzygapophyseal facet with the prezygapophyseal facet of the next vertebra is located in the center of the smaller of the facets. Thus, when the neck bends and extends in the sagittal plane, the center of interaction of the two articulated facets is not displaced relative to the body of the vertebra that bears the smaller facet. That is, in giraffes, this center is stationary in relation to the more posterior vertebra, and in camels, to the more anterior vertebra. The reason for this different design may be the feeding level typical of these animals. Camelidae feed at ground level (feeding height <0.5 m), while Giraffidae feed on tree leaves at a level above the articulation of the neck to the body. In both cases, the center of facet interaction in every pair of neck vertebrae is fixed relative to that vertebra which is located lower to the ground. What the advantage is of such a disposition is a question for future research.

5.2.2. Morphology of the end‐plates of the neck vertebrae in Caprinae

The specific adaptation of the cervical vertebrae was noted in the cervical region of all studied adults of the subfamily Caprinae (Capra falconeri, Ovibos moschatus, Ovis ammon, and Ovis aries). The anterior and posterior end‐plates of the vertebrae in the Caprinae are practically flat (platycoelous). The anterior end‐plates of the cervical vertebral body in the ventral part have paired, directed laterocranially convex outgrowths (Figure 7). The posterior end‐plates have corresponding depressions which house the aforementioned outgrowths of the next vertebra. This design helps to increase the area of contact of the vertebral bodies. The reason for this adaptation may be the overloads experienced by the cervical region in representatives of this subfamily of Bovidae during tournament fights. In contrast, in other tournament species (Cervidae, Bovini, and antelopes), the bodies of the cervical vertebrae are opisthocoelous and do not bear any additional end‐plate outgrowths. This difference may be due to the fact that for tournament fights among Caprinae, hard head‐on collisions are typical (ramming and fencing combat form), instead of stabbing and wrestling as in other tournament species. Caprine‐style head collisions may require the formation of additional mechanisms to prevent injuries to the neck joints.

FIGURE 7.

Additional outgrowths on the end‐plates of the cervical vertebral bodies in Caprinae. Ovis ammon (ZMMU S‐146149): anterior view (a), posterior view (b), posterolateral view (c). Capra falconeri (ZMMU S‐181396): anterior view (d), anterolateral view (e), and posterolateral view (f)

Vander Linden and Dumont (2019) showed that ramming species have shorter and wider vertebral centers and taller neural spine lever arms than wrestlers, stabbers, and fencers. Such adaptation of the vertebrae may help absorb high compressive forces during impact. An increase in the width and reduction in the length of the vertebral bodies does not lead in Caprinae to a significant reduction in the neck length relative to trunk length. This ratio is only slightly inferior in Caprinae (Mean = 37.17%) as compared to large antelopes (Mean = 40.75%) and Cervidae (Mean = 41.92%). The only representative of Caprinae studied by us with a significantly shortened neck is muskox (30.8%) whose neck length corresponds to that of Bovini (29.3%–34.7%).

The C5–C6 and C6–C7 joints in sheep are characterized by extremely high (for mammals) AR aROM values (Mean 18.9° in the C5–C6 and 17.5° in the C6–C7) (Wilke et al., 1997a). Also, SB and LB aROMs reach their maximum values in these two joints in the sheep. This indicates that the sheep, and probably Caprinae as a whole, avoid overloads during head‐on collisions in tournament fights by recruiting all three components of intervertebral mobility in the two posterior cervical joints.

5.3. Complex role of thoracic region

5.3.1. Kinetic energy absorption at the withers

The amplitude of SB in the Tf division decreases markedly compared to the Rf joints of the neck. In artiodactyls, the anterior part of the thoracic region, the withers, shows size‐dependent reinforcement. There is an elongation of the spinous processes of the vertebrae (Figure 4, Supplementary Material S2), as well as thickening of the supraspinal ligament, and increase in the number of interspinal ligament fibers (Gambaryan, 1974). Gambaryan terms this “the vertebral column rigidity organ.” The reinforcement of the vertebral column at the withers helps to carry the weight of the heavy head, neck, and thorax. Their weight tends to flex the vertebral column ventrally at the withers where the scapula is attached, which acts as a fulcrum for the entire anterior part of the body (Gambaryan, 1974; Kummer, 1959a, 1959b; Schilling & Hackert, 2006). An additional weight which tends to flex the withers even harder occurs in the forelimb contact phase in running and overcoming obstacles. The weight of the body is transmitted to the scapula by the m. serratus ventralis. This muscle becomes stronger in heavier mammals and is partially transformed into short ligaments in the heaviest ones, giraffes and elephants (Gambaryan, 1974; Gambaryan & Ruhkyan, 1974). Attachment of nuchal ligament in the area of the withers allows artiodactyls to store and recover elastic energy during vertical oscillations of the head and neck (Loscher et al., 2016). However, contrary to the idea of “the vertebral column rigidity organ,” the vertebrae in the withers area are never fused together to fully consolidate this region. More than that, in the Tf division, the calculated SB aROM reaches the highest cumulative and average values at the withers area in large, heavy animals with a massive anterior part of the trunk and a large head (hippopotamus, European bison, wildebeest, boars, and pigs). The lowest values of the calculated SB aROM are typical for small antelopes (Table 5, Tables S4 and S5). This may indicate that the withers are not the organ of rigidity, but the organ of absorption of kinetic energy of the body upon landing on the forelimbs. The reinforcement of the withers with taller spinous processes and stronger interspinal ligaments makes up the force against ventral flexion. The increased SB aROM results in longer braking distance. Both of them together increase the amount of mechanical energy that can be dissipated by the withers, and the development of both correlates with body size.

5.3.2. Tangential facets and their possible function

In artiodactyls, as in other mammals, zygapophyseal articular facets suddenly change their orientation. The transitional vertebra is T1, or sometimes T2 (Table S1). On the anterior side of the transitional vertebra, the facets are V‐shaped in anterior view. This is the Rf type characteristic to the mammalian cervical region and to the whole vertebral column of all other tetrapods. On the posterior side of the transitional vertebra, the facets are _⁀‐shaped in posterior view. This is the Tf type characteristic to the anterior part of the mammalian thoracic region named herein as Tf division. In this case, prezygapophyses do not form outgrowths, and their articular facets are located directly on the neural arches of the vertebrae and oriented along the circumference of the vertebral center—tangentially or almost horizontally (Slijper, 1946; Virchow, 1907). This structural type is unknown among non‐mammalian tetrapods beyond rare exceptions such as horizontal zygapophyseal articulations in a few presacral joints of pareiasaurians (Kuznetsov, 2020).

The current analysis allows to specify functional properties of Tf division in artiodactyls. It always includes joints 9–15, usually also joint 8 (first thoracic joint), and sometimes more posterior joints up to joint 20. In Tf division, SB aROM is the lowest in the whole presacral vertebral column (Figure 2a), while AR aROM is the highest (Figure 2c). It is greater than SB aROM and approximately equal to LB aROM (Figure 2b). The latter is a little higher here than it is in the more posterior RfL division. The LB and AR aROM profiles in Tf division parallel each other. This comes from the fact that the optimal formulae for both movements have the same numerator/denominator pair here, which is W/R_lat. There is only a small difference in the negative multiplier of the second term in the pan‐artiodactyl formula: −0.52 for LB and −0.54 for AR. As a result, in every intervertebral joint in Tf division LB and AR aROMs are roughly equal to each other. Both of them reach their greatest values in the anterior half of the Tf division, which statistically is significantly more mobile in LB and AR (but not in SB) than the posterior half. The most mobile are the most anterior joints. Animals with, on average, the most mobile joints in the anterior half of the Tf division are agile runners such as cervids, musk deer, pronghorn, and large and small antelopes. The least LB and AR aROMs in the Tf division are typical for Hippopotamidae. However, the variability of LB and AR (as well as SB) aROMs in the Tf division is too low to sort out ecological groups, or running forms.

The general adaptive significance of reformatting zygapophyseal articular facets in the anterior thorax from Rf to Tf type which is unique to mammals and is found, to our knowledge, in all of them, is a great topic for future research. Obviously enough, it is associated with acquisition of increased AR mobility, in favor of SB, in this part of the vertebral column. The first idea that could come to mind is that AR‐capable Tf joints are confined to the prediaphragmatic part of the mammalian trunk, which could imply some association with breathing movements. However, it is hard to imagine the use of AR in breathing. In general, two alternative kinds of adaptive significance can be thought of: locomotor and non‐locomotor. The latter was recently suggested by Jones et al. (2020, 2021) who treat body twisting as a possible adaptation for self‐grooming fur for thermoregulation. Although this explanation could work well for bipedal mammals, it is hardly applicable to the quadrupedal majority of them. Indeed, when all four feet are on the ground, AR in the anterior thorax cannot help to expose hairs. The neck mobility works perfectly for self‐grooming in a quadruped. It is quite possible that formation of the bicondylar occipital joint was acquired by mammals for expansion of cranio‐cervical LB aROM to groom abdominal hairs. However, the thoracic AR posterior to the forelimbs has, more probably, locomotor reasons.

Mammalian ancestors could obtain Tf articulations in the thorax for the same use of AR as is discovered in modern echidna (Gambaryan & Kuznetsov, 2013). Its gait is the pace‐like walk with somewhat decoupled steps of the forelimbs and the hindlimbs. Walking with the back curved in an arc, the echidna ensures this decoupling by means of the AR of the vertebra at the top of the arc. This makes the posterior half of the trunk tilt (roll) from side to side with some delay relative to tilting of the anterior half. This could be a typical walking technique of sprawling quadrupeds in mammalian lineage (Gambaryan & Kuznetsov, 2013; Kuznetsov, 1999). The same mechanism was later presumed for pareiasaurians based on trackway analysis and the presence of Tf‐type articulations anterior to the sacrum, otherwise unknown beyond mammals (Kuznetsov, 2020).

Expanded AR in anterior thorax, due to Tf articulations, can have a variable use in mammalian locomotion, not only in the peculiar archaic walking of monotremes. Generally speaking, it allows to tilt the parasagittal plane of the forelimbs to one or the other side relative to that of the hind limbs, and vice versa. The parasagittal plane is the plane of major limb movements and major limb forces in therian mammals. For instance, in burrowing, the hind limbs are held stationary on the ground, and the forelimbs scratch the ground. To dig not only the floor but also the side walls of the burrow, the body should be twisted between the fore and hind limbs. This is the probable use of AR in the anterior thorax, due to Tf articulations, in burrowing. Another example of the use of expanded AR in the Tf division is maneuvering. Independent rolling of the fore and hind halves of the body to the left or right side allows smart cornering in hares (Kuznetsov et al., 2017).

5.3.3. “Diaphragmatic” facet transition (joints 16–20) and involvement of posterior thoracic joints in gallop

The change in the zygapophyseal articulations from the Tf to RfL type in mammals may either coincide (in humans) with the boundary of the thoracic and lumbar regions or be located anterior or posterior to it. In artiodactyls, the Tf‐RfL transition always occurs anterior to the thoracic–lumbar transition (Table S1). The most anterior and posterior Tf‐RfL transition differs in studied artiodactyls by six joints (from T9–T10 to T14–T15 or from joint 16 to joint 21). It should be noted, that the aforementioned traditional term “diaphragmatic” for the transitional vertebra is misleading in fact. For instance, in Ovis aries which we dissected, the transitional vertebra was T11, while the lumbar portion (crura) of the diaphragm passed T12, T13, and L1 to insert on L2.

The change in the orientation (anticlination point) of the vertebral spinous processes from a backward to forward inclination in artiodactyls may or may not coincide with the change in the zygapophyseal facet type (Figure 4). In small species, these transitions are in good agreement with each other. In many large species, the spinous anticlination point either occurs in the lumbar region posterior to not only Tf‐RfL but even to thoracic–lumbar transition (in Bovini and Camelidae), or is not expressed at all (in giraffes) (see Figure 4 E and Supplementary Material S2).

The more anterior or posterior transition of the RfL type in different species can characterize the region of the vertebral column which is actively involved in running using a specific mammalian bounding gait, the gallop. As shown by Schilling and Hackert (2006), in various small mammals (Ochotona rufescens, Tupaia glis and Monodelphis domestica), not only the lumbar joints but also some of the thoracic RfL joints are actively involved during gallop. The same can be expected for the larger gallopers.

High values of SB aROM in the transitional joints 16–20 are typical for smaller artiodactyls (significant negative correlations with almost all linear dimensional characteristics, see Table 9), which are characterized by high SB mobility in the RfL division and lumbar region (see Table 10). The highest cumulative SB aROM in the transitional joints is typical for species adapted to the saltatorial running form. The lowest values are typical for the largest artiodactyls (Giraffidae and Hippopotamidae).

Not surprisingly, high values of AR aROM in the transitional joints are typical for species with the posterior position of Tf‐RfL transition (Giraffidae and Bovini). The lowest AR aROM in this locus is typical for hippos and pigs using the battering‐ram running form. They have the anterior position of Tf‐RfL transition. Therefore, their joints 16–20 are of the RfL rather than the Tf type. The exclusion of these joints from the Tf section manifests as reduction of maneuverability which conforms to battering‐ram running.

5.4. Role of the lumbar vertebral column during the gallop

5.4.1. RfL division and lumbar region

The RfL division and lumbar region in mammals are adapted for efficient action in the sagittal plane. This is an adaptation of quadrupedal mammals to gallop. When galloping, the elastic energy is stored in the m. longissimus aponeurosis during vertebral column flexion and hind limb protraction, and then recovers in an elastic recoil during vertebral column extension, when the hind limbs perform their thrust onto the ground. This makes the gallop the most energy efficient gait at high speeds (Alexander et al., 2009). The major SB occurs in the posterior vertebral column which has the RfL joints.

The joints in the RfL division in artiodactyls are characterized by a nearly vertical (parasagittal) orientation of the main surface of zygapophyseal facets. The morphology of the “locks” in the RfL division in artiodactyls is diverse. Thus, in giraffes in the posterior half of the RfL division, the facets are close to the simple Rf type (V‐like orientation of the facet pair without locks). In other artiodactyls, the prezygapophyses bear variously shaped ridges which capture the postzygapophyses of the previous vertebra (Figure 8).

FIGURE 8.

The “locks” morphology of the pre‐ and postzygapophyses in the RfL joints in various artiodactyls. Postzygapophyses of an anterior vertebra in a pair (a, c, e, g, i, k), prezygapophyses of a posterior vertebra in a pair (b, d, f, h, j, l). The examples are displayed in a sequence of increased lock closure. (a, b) Ovibos moschatus; (c, d) Giraffa camelopardalis; (e, f) Capra falconeri; (g, h) Phacochoerus africanus; (i, j) Alces alces; and (k, l) Ovibos moschatus

SB aROMs are unevenly distributed in artiodactyls along the RfL division. The average SB aROM in the lumbar joints in artiodactyls statistically significantly exceeds the average SB aROM in the thoracic RfL joints (Mean Diff =0.76°).

Both cumulative and average SB aROM in the RfL division and lumbar region have high negative correlations with the linear dimensions of the vertebral column (Table 9). All the lowest SB aROMs are typical for the largest representatives of artiodactyls—Hippopotamidae, Bovini, and Giraffidae (Figure 9). In fact, this is what was termed by Gambaryan (1974) “the dorsostability.” It can be hypothesized that the reduction of SB aROM in the lumbar region allows large animals to make the muscular fibers of the lumbar extensors shorter than would be required otherwise. The shorter the fibers, the stronger the muscle of a given mass. Making muscles relatively stronger in large animals is an example of allometry. It solves the known problem that if the muscles were enlarged without any change of proportions (isometrically), their force would grow like the surface area (second power of length) while the external demands would grow like the mass (third power of length) of the animal.

FIGURE 9.

Sagittal mobility in the lumbar region (a) and RfL division (b) in artiodactyls. Abscissa axis represents the absolute length (cm) of the trunk (T+L+S). Ordinate axis represents the cumulative SB aROM (°). The mean values for all studied species are taken for the point of axes intersection (trunk length Mean = 893.79 mm; cumulative SB aROM in lumbar region Mean = 47.91°; cumulative SB aROM in RfL division Mean = 63.45°). The circles’ colors indicate a taxonomic group as in Figure 6

SB aROM (both cumulative and average) in the RfL division and lumbar region of the vertebral column has a very high positive correlation with elongation of the lumbar region relative to the thoracolumbar region as a whole (r = 0.404–0.778, Sig = 0.005–0.000) (Table 9). Thus, for a given thoracolumbar length, the attainable curvature (determined by cumulative SB aROM) and the length of the lumbar region tend to become larger together. These are the two mutually additive ways to increase the path of the animal's center of gravity when the lumbar region extends from the maximally flexed to the straight position, for instance, before a jump.

This is in good agreement with the classification of running forms by Gambaryan (1974). Artiodactyls adapted to saltatorial and saltatorial–cursorial running forms have the most mobile RfL and lumbar joints (Figure 9). Artiodactyls adapted to the cursorial running form are characterized by average mobility in the RfL division and lumbar region. The lowest mobility in the RfL division and lumbar region is typical for animals using the mediportal running form (Figure 9).

A mountainous habitat also acts as a factor in increasing mobility in the lumbar region that animals use while jumping. Mountain species, in terms of cumulative SB aROM, exceed the respective maximum among non‐mountainous artiodactyls by an average of 7°.

In artiodactyls, the spinous processes of the vertebrae are used for attachment of the ligaments preventing excessive sagittal flexion. In the RfL division, the spinous processes are wide bony plates, the tips of which are extended in an anteroposterior direction. Therefore, the interspinal and especially the supraspinal ligaments connecting the spinous processes are short. The taller the spinous processes, the smaller the flexion angle they allow with the same length of the ligaments connecting their tips (Gambaryan, 1974). The most extended spinous processes relative to the length of the vertebral body in the lumbar region are observed in musk deer and Caprinae (see Supplementary Material S2).

AR aROMs in the RfL division and lumbar region in all artiodactyls are extremely low. The average AR aROM in the RfL division has negative correlations with the SB aROM in the RfL division and lumbar region (Table 10), which indicates that an increase in SB aROMs in the RfL division of the vertebral column in artiodactyls is accompanied by a decrease in AR aROM. This is quite expectable, because the lumbar SB is the basis of gallop, and AR in the same part of the vertebral column could cause problems. This is why AR, which is required for maneuvers, is located in a different part of the vertebral column—the Tf division.

Among small antelopes (with pronghorn included), higher SB aROM values were found for species using the saltatorial–cursorial running form (Gazella subgutturosa and Antilope cervicarpa), while in species adapted to endurance cursorial running, SB mobility is noticeably lower (Procapra gutturosa, Saiga tatarica and Antilocapra americana) (see Tables S4 and S5). Adaptation to cursorial running in artiodactyls is aimed at endurance gain by a decrease in vertical fluctuations of the center of gravity and an increase in stride frequency during the gallop (Gambaryan, 1974). On the contrary, for species with saltatorial–cursorial and saltatorial running forms, the vertical fluctuations of the center of gravity during the gallop are noticeably higher (it is higher than during trot or pace of the same animals, and than during gallop in cursorial ungulates). In the saltatorial–cursorial artiodactyls, the running speed increases mainly due to an increase in the stride length ensured by increased joint amplitudes not only in the limbs but also in the lumbar region.

6. CONCLUSION

Intervertebral mobility is unevenly distributed in the vertebral column of mammals. The different regions and divisions of the backbone are specialized to carry out different life activities. The amplitudes of mobility in the joints correspond to the animal's adaptations to the habitat and locomotion.

The cervical region in even‐toed ungulates is the main manipulator for interacting with the habitat. The cervical region is the most mobile part of the vertebral column in the sagittal and lateral plane. The high diversity of the relative length, shape, and robustness of the neck is reflected in the variability of the amplitudes of mobility. SB and LB reach their maximum variability just in the cervical region of the vertebral column. Mobility is unevenly distributed throughout the joints of the neck. The synovial joint between atlas and axis is the most mobile neck joint, although our analysis technique is not applicable to it. Among typical Rf joints of the neck, the posterior ones (C4–C7) are significantly more mobile in SB and LB (on average by 2.5–3.5°) as compared to anterior ones (C2–C4) and to the neck–thorax joint (C7–T1). Artiodactyls with the most mobile necks belong to Giraffidae and Camelidae. Their necks are 2–3 times more mobile in SB and LB compared to artiodactyls with the least mobile necks. Morphologically, the increased mobility is implemented in different ways in Giraffidae and Camelidae. In Camelidae, an elongation of the arc of motion occurs due to increase of the facet lengths of the prezygapophyses. On the contrary, in Giraffidae, the facets of the postzygapophyses are elongated.

The thoracic region of the vertebral column is responsible in mammals for interaction with the forelimb—support and maneuvering. Energy absorption when landing on the forelimbs is especially important for heavy animals with large and massive heads, which is reflected in the build‐up of the ligamentous apparatus, which is able to absorb the energy of a falling body. For maneuvering, mammals actively use LB and AR. LB aROMs in the anterior (prediaphragmatic) thorax characterized by specific Tf joints reaches its highest values in the thoracolumbar region, and AR aROMs in the Tf division reaches its highest values in all of the presacral region. The lowest LB and AR aROM in the thoracic region and Tf division are typical for the heaviest artiodactyls—Hippopotamidae.

The posterior part of the thoracic region (RfL division or postdiaphragmic locus) is most adapted in ungulates for use during gallop to increase the stride length. The most anterior change in the type of zygapophyseal facets from Tf to RfL type in the thoracic region, and the greatest elongation of the lumbar region relative to the thoracolumbar region as a whole is typical for species that actively use the extension of the backbone to enhance the extension of the hind limbs.

In the lumbar region of the vertebral column, SB aROM has a relationship with body size and running form that the animal uses. The greatest SB mobility in the lumbar region is typical for small‐ and medium‐sized animals using the saltatorial and saltatorial–cursorial running form. Animals adapted to endurance cursorial running in open spaces increase stride frequency during the gallop and are characterized by decrease of SB mobility in the lumbar region. Alternatively, the saltatorial–cursorial artiodactyls increase the stride length by increased joint amplitudes in the sagittal plane not only in the limbs but also in the lumbar region.

The HC results show that the most distinct combination of intervertebral mobility from other artiodactyls is found in the forms with the most unique body builds (Figure 5). The most distant characteristics of vertebral column mobility from the rest of artiodactyls are typical for giraffes, which are characterized by several unique anatomical features. These animals have not only an extremely long and mobile neck but also limited use of the SB mobility of the lumbar spine during galloping on their extremely long limbs. The most similar to each other are small‐ and medium‐sized artiodactyls, adapted to fast running and jumping.

CONFLICT OF INTEREST

None.

AUTHORS’ CONTRIBUTIONS

R.B. and N.P. worked with the material; R.B. and N.P. analyzed the data; R.B., N.P., and A.K. wrote the paper. All authors read and approved the final version of the manuscript.

Supporting information

Supplementary Material

Supplementary Material

Supplementary Material

Supplementary Material

Supplementary Material

Belyaev, R.I. , Kuznetsov, A.N. & Prilepskaya, N.E. (2021) How the even‐toed ungulate vertebral column works: Comparison of intervertebral mobility in 33 genera. Journal of Anatomy, 239, 1370–1399. 10.1111/joa.13521

DATA AVAILABILITY STATEMENT

Data are available for 37 figures with photographs of the vertebral column of the studied artiodactyls. All figures: cervical region (C1–T1) left‐side (a) and dorsal (b) view; thoracolumbar and sacral region left‐side (c) and dorsal (d) view.

Belyaev et al. (2021): Figures of various artiodactyls vertebral column. figshare. Figures. https://doi.org/10.6084/m9.figshare.13302365.