JOURNAL OF MORPHOLOGY 214:63-81 (1992)

The Functional Morphology of Xenarthrous Vertebrae in the Armadillo Dasypus novemcinctus (Mamrnalia, Xenarthra) TIMOTHY J. GAUDIN AND ANDREW A. BIEWENER Department of Organzsmal Biology and Anatomy, University of Chicago, Chicago, Illinois 60637

ABSTRACT In order to assess the mechanical properties of xenarthrous vertebrae, and to evaluate the role of xenarthrae as fossorial adaptations, in vitro bending tests were performed on posterior thoracic and lumbar vertebral segments excised from specimens of the armadillo Dasypus novemcinctus and the opossum Didelphis uirginiana, the latter being used to represent the primitive mammalian condition. The columns of the two species were subjected to dorsal, ventral, and lateral bending, as well as torsion, in order to determine their stiffness in each of these directions. During these tests, bone strains in the centra of selected vertebrae were determined using rosette strain gages. Overall stiffness of the armadillo backbone at physiologically relevant displacement levels was significantly higher than that of the opossum for both dorsal and lateral bending. The two species also exhibited significant differences in angular dwplacement of individual vertebrae and in vertebral strain magnitudes and orientations in these two directions. No significant differences were observed when the columns of the two species were subjected to torsion or to ventral bending. Our results suggest that some, but not all, of the mechanical differences between the two species are due to the presence of xenarthrae. For example, removal of the xenarthrae from selected vertebrae (LZ-L4) changes strain orientation and shear, but not strain magnitudes. Comparisons with functional data from other diggingmammals indicate that the modified mechanical properties of the Dasypus column are consistent with an interpretation of xenarthrae as digging adaptations and lend support t o the idea that the order Xenarthra represents an early offshoot of placental mammals specialized for fossoridity. o 1992 Wiley-Liss, Inc. The mammalian order Xenarthra is a small but morphologicallyvaried Neotropical group of 14 genera and 30 species (Wetzel, '85). Its living representatives, the armadillos, sloths, and anteaters, are but a small remnant of a highly diverse fossil assemblage. Throughout most of the Cenozoic era, this assemblage was one of the dominant mammalian groups inhabiting South America (Hoffstetter, '581, then an isolated island continent. The Xenarthra retain a number of primitive mammalian characters and lack derived features present in other placental mammals. This has caused some recent authors to suggest that xenarthrans represent the sistergroup to all other placental mammals (McKenna, '75; Novacek et al., '88). However, along with these primitive features, the group combines many unusual and often bizarre specializations. Xenarthrans exhibit a broad o 1992 WILEY-LISS, INC.

range of morphologies and ecologies, ranging from the completely fossorial fairy armadillo Chlamyphorus to the arboreal sloths Bradypus and Choloepus, which hang underneath tree branches suspended by their limbs. Despite the diversity in their modes of life, good evidence exists that the Xenarthra are monophyletic. This evidence consists of a large number of unusual and derived skeletal modifications, including a fusion of the ischium to the caudal vertebrae, the presence of a secondary scapular spine, the presence of dermal ossifications, and the reduction and/or simplification of the dentition (Engelmann, '85). Also included in this list of skeletal modifications is that feature for Address reprint requests to Timothy J. Gaudin, Department of Organismal Biology and Anatomy, University of Chicago, 1025 E. 57th St., Chicago, IL 60637.

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T.J. GAUDIN AND A.A. BIEWENER

Abbreuiations accessory process, a.k.a. anapophysis anterior zygapophysis mammillary process, a.k.a. metapophysis neural spine posterior zygapophysis transverse process vertebral centra

Fig, 1. Tupaia glis. First and second lumbar vertebrae shown in lateral view, with cranial surface to the left, caudal to the right. (Modified from Jenkins, ’74.)

aaa Paa sg

A

Abbreviations anterior accessory intervertebral facets (i.e., xenarthrae) on the mammillary processes and transverse processes posterior accessory intervertebral facets (xenarthrae) on the anapophysis (a.k.a. accessory process) strain gage,shown in position on the vertebral centrum

B

which the order was named, the xenarthrae. Xenarthrae and xenarthrous vertebrae have been described in detail by several investigators (Flower, 1885;Grasse, ’55;Jenkins, ’70). Xenarthrous vertebrae (Fig. 2) differ from more generalized mammalian vertebrae (Fig. 11,in that they bear supplementary intervertebral articulations. These articulations are termed xenarthrae, and are found only in the posterior thoracic and lumbar vertebrae. Xenarthrae vary somewhat in number and posiFig. 2. Dasypus nouemcinctus. Third and fourth lumtion both along the length of the vertebral vertebrae. A: Lateral view, cranial surface to the left, column and among species, but they typically bar caudal to the right. B: Anterior view above and posterior form between the anapophysis of one verte- view below. C: Anterior three-quarters view. Note that in bra and the lateral surface of the metapophy- the line drawings of A and B, the xenarthral articular sis (i.e., the mammillary process) and dorsal surfaces are indicated in black. surface of the transverse process of the succeeding vertebra. Whereas the morphology of xenarthrous vertebrae has been well charac- cally, the four armadillo genera of Engelterized, their function has remained rather mann’s (’85) clade “Dasypodidae,” habitupoorly understood. ally use enrollment as a defensive maneuver. Speculations on the function of xenarthrae It is therefore questionable whether this behave included the suggestion that they might havior characterized primitive xenarthrans. be linked to the behavior of certain xenarOther investigators have linked the develthrans which roll up into a ball when threat- opment of xenarthrae to the acquisition of ened. Winge (’41)hypothesized that xenar- fossorial habits by the common ancestor of thrae were induced to form by friction the order. The Xenarthra have long been between the anapophyses, zygapophyses,and thought to represent an early offshoot of transverse processes during such enrollment placental mammals specialized for digging behavior. Hoffstetter (’82) suggested that xe- (Simpson, ’31), and many of the skeletal feanarthrae might serve as a necessary mechan- tures characterizing the order have been ical link for enrollment, transmitting bend- viewed as adaptations for digging (Hoffsteting forces along the column. However, only a ter, ’58). This view reflects the assumption small subset of xenarthran genera, specifi- that because the first xenarthrans to appear

FUNCTIONAL MORPHOL.OGY OF XENARTHRAE

in the fossil record are armadillos, the first xenarthran was an armadillo-likeanimal that likely shared the burrowing habits of the living forms. However, it has yet to be demonstrated whether xenarthrae play any role in the digging behavior of extant xenarthrans, and if so, what that role might be. Frechkop ('49) noted that the giant armadillo Priodontes is facultatively bipedal, supporting itself solely on its hindlimbs while holding its trunk roughly horizontal. He speculated that xenarthrae evolved in early xenarthrans in order t o provide the backbone with extra rigidity, allowing the trunk to be supported by the hindlimbs and vertebral column, freeing the forelimbs for digging. Jenkins ('70) hypothesized that, in addition to stiffening the column, the xenarthrae might also serve to transmit the large forces generated in digging by the forelimbs to the pelvis and hindlimbs. However, the functional hypotheses of both Frechkop and Jenkins lack the support of any direct experimentaldata. Without more concrete data on the functional role of xenarthrae in living xenarthran diggers, assertions about their origin as digging adaptations in early xenarthrans have at best questionable validity. The principal aim of this study is therefore to provide quantitative information about the way that xenarthrae modify the mechanical properties of the xenarthran vertebral column compared to those of a more primitive mammalian condition. It should be noted that, in addition to the xenarthrae, the xenarthran axial skeleton exhibits a number of other structural modifications that will be covered briefly in the discussion section. Bending tests were performed in order to measure the stiffness of segments of the posterior thoracic and lumbar vertebral column of Dasypus nouemcinctus, the nine-banded armadillo. The burrowing habits of this species allow us to test whether xenarthrae play some role in digging behavior in a living xenarthran. Moreover, the xenarthrae of this species provide a fair representation of the primitive xenarthran condition.Dasypus possesses neither extra articulations, as does the giant armadillo Priodontes, nor are its articulations reduced, as in the two- and three-toed sloths (Grass& '55). Thus, our results may allow us to make some inferences about the origin of xenarthrae among early members of the order. A major difficulty of the present study, however, is that we have little information

65

about the mechanical properties of primitive mammalian backbones. In a widely cited study, Slijper ('46) provided qualitative measures of mobility in different regions of the vertebral column for a variety of mammals, rating them rather generally from highly mobile to immobile. Quantitative measures of the mechanical properties of vertebrae are available for human beings (see Brown et al., '57; King and Vulcan, '71; Cyron et al., '79; Schultz et al., '82; Adams and Hutton, '85; and references cited therein); however, human backbones are strongly modified to accommodate an upright, bipedal stance and, hence, are of little comparative value. Similar data for more typical mammals are practically nonexistent. Therefore, in order to provide information on the mechanical properties of a generalized mammalian backbone, tests were also performed on the Virginia opossum, Didelphis uirginiana. This species was selected because it is fairly conservative in its locomotory habits relative to the presumed primitive therian condition (Jenkins, '71). In addition, the skeletal morphology of the thoracic and lumbar vertebrae in Didelphis is similar t o that of other generalized therians (e.g., the tree shrew Tupaia glis, Jenkins, '74, personal observations); in the closely related species Monodelphis donestica (Pridmore, '921, the dorsoventral mobility of this portion of the spine is also quite similar to that of other generalized forms (e.g.,Tupaia, Jenkins, '74, and the cat, Felis domesticus, English, '80). Lastly, Didelphis is similar in body size to Dasypus. By comparing the mechanical properties of the vertebral columns of these two species, we attempt to evaluate xenarthrae as a potential adaptation for digging in ancestral xenarthrans. MATERIALS AND METHODS

Specimen preparation Sections of vertebral columns suitable for mechanical testing were obtained from freshly frozen Dasypus and Didelphis specimens purchased from licensed animal dealers in southern Florida. The animals were shipped and maintained frozen until testing. Three specimens were obtained from each species, ranging in size from 1.2 to 2.3 kg (opossums) and from 3.3 to 4.5 kg (armadillos). Before testing, each animal was thawed overnight and the anterior sacral vertebrae and ilium, along with 12-13 presacral vertebrae, were dissected out and removed. The column segment was stripped of its attached

66

T.J.GAUDIN AND A.A. BIEWENER

musculature, leaving the intervertebral ligaments intact as much as possible. The ends of the column were then potted in plastic tubing filled with epoxy resin. At the anterior end, the two anteriormost vertebrae were embedded in epoxy, while the sacral vertebrae and ilium were embedded posteriorly, leaving 10 presacral vertebrae available for testing. In Dasypus, it is these ten vertebrae that bear xenarthrae. The vertebrae and ligaments were kept moist with physiological saline while the epoxy was curing (about 15 min for the anterior end and 30 min for the posterior) and throughout the remainder of the tests. After the epoxy had set, a 6.5-mm hole was drilled through the center of both pots, so that the column could be mounted on the testing apparatus. In addition, the left ventrolateral surfaces of three vertebrae were cleaned using a periosteal elevator and methyl ethyl ketone, and rosette strain gages (Tokyo Sokki Kenkyujo Co., Ltd., type FRA-1-11) were bonded to the cleaned surfaces using a self-catalyzing cyanoacrylate adhesive. In Dasypus, which has 10 thoracic and 5 lumbar vertebrae, the strain gages were placed on T8/Ll/L4, whereas in Didelphis, which has 13 thoracic and 6 lumbar vertebrae, the gages were attached to Tll/L2/L5. To determine the orientation of the principal strains relative to the long axis of the column, the angle of the central element of each rosette strain gage relative to the long axis of the vertebral column was measured using a protractor. The column was mounted on the testing apparatus (Fig. 3) with the sacral pot immobilized and the thoracic pot resting freely on a horizontal surface. Mechanical loading and data collection Each section of vertebral column was subjected to cantilever bending in dorsal (i.e., dorsal concave), ventral (i.e., ventral concave), and lateral directions, as well as to axial torsion, by pulling on the thoracic end of the column with a force transducer (sensitivity = 1.9 NIV). For torsional tests, the thoracic end of each column was anchored to a horizontal cross bar in such a way that the vertebrae could rotate about the long axis of the column but were immobile dorsoventrally and laterally. The force transducer was then used to rotate the cross bar in a clockwise direction (in anterior view). Measurements were obtained for six repeated loading cycles in each loading mode (oneloading cycle being equivalent to a single loading and un-

I

1

Fig. 3. Didelphis uirginiana. Diagram of vertebral column mounted on experimental apparatus, in lateral view. T13, L1, and L6 represent the positions of the thirteenth thoracic and first and sixth lumbar vertebrae, respectively. F represents an applied dorsal bending moment. Lines AB and ABC represent successive measurements of displacement during a single repeated loading cycle; 8-10 such measurements were performed for each cycle.

loading of the backbone). In each cycle, the vertebral column was displaced up to its natural limit of bending or torsion; i.e., the column was displaced close to its maximum but with care taken not to cause any damage to the column. After completing the tests on intact Dasypus vertebral columns, the xenarthrous articulations between the second, third, and fourth lumbar vertebrae were removed by cutting the anapophyses with a pair of small bone shears. The anapophyses were severed from their vertebra of origin, but not removed entirely, in order to avoid damage to the vertebral ligaments. The xenarthrae in other portions of the column were left intact because their geometry rendered them inaccessible to removal. Although this limits our ability to eliminate completely the effect of the xenarthrae on the overall mechanical properties of the column, measurements of angular displacements and bone strain of those vertebrae lacking xenarthrous articulations provide a basis for evaluating how xenarthrae contribute to the observed differences i n mechanical properties of t h e armadillo and opossum backbones. After the removal of the posterior lumbar xenarthrae, the Dasypus columns were loaded again in torsion and in dorsal, ventral, and lateral bending. To record deflections of the vertebral columns in dorsal and ventral bending, the columns were filmed in lateral view using a video camera (Sony CCD video camera mod-

FUNCTIONAL MORPHOLOGY OF XENARTHRAE

ule, model XC-77). For the lateral bending tests, the column was filmed in dorsal view, and for the torsional loading tests, the column was filmed in anterior view. Because the thoracic pot obstructed the anterior view of the vertebrae (see Fig. 31, displacements of individual vertebrae were recorded using successively longer, alternating blue and white wire markers attached to the neural spines of each vertebra. Output from the strain gages and force transducer was amplified and entered into the computer via an AID converter for storage and analysis using ASYST software (Keithley Instruments). Force and strain measurements were synchronized to the video tape by means of a flashing LED in the field of view that emitted a series of voltage pulses monitored by the computer. Data analysis Displacements of the vertebral columns were analyzed by digitizing the video tapes of the mechanical loading tests using JAVA video analysis software (Jandel Scientific)run on a microcomputer. Deflections of the columns in dorsal, ventral and lateral bending were measured as follows (Fig. 3): in the initial video frame, the chord length of the displacement arc of the column relative to the horizontal was measured from a point at the end of the column (e.g., AB in Fig. 3); in subsequent frames, the chords of displacement arcs undergone by the column were measured relative to the position of the column in each previous frame (e.g., BC in Fig. 3). A cumulative sum of the chord length path was then determined for 8-10 frames spaced equally in time over the duration of each loading cycle. Note that, even for a large displacement arc, e.g., 150",the sum of the chord lengths should theoretically fall within 99.6-99.7% of the actual arc length. To account for differences in length of the vertebral column between the two species, as well as among individuals within each species, all displacements were normalized by dividing them by the total length of the column segment. In addition to overall deflection of the column, the angular displacements of each of the 10 individual vertebrae were measured relative to their resting positions. These measurements were taken at the natural limit of bending or torsion of the entire column in one of the six loading cycles of each animal tested in each of the four loading modes. These data provided information on the magnitude and location of deflections along the

67

length of each column segment. Torsional displacements were obtained from the angular displacements of the wire markers attached to the vertebral spines, relative t o their resting positions. In order to ensure equivalence of strain results between species and among different individual animals and different loading modes, principal strain angles and magnitudes (see Dally and Riley, 1978, for calculations) were measured for all three bending modes at an applied bending force of 4 N, and for torsion at an applied torque of 0.2 Nm. These levels resulted in strains of sufficient magnitude relative to background noise levels to yield reliable results. Moreover, these force levels were low enough to permit the inclusion of strain data from almost every loading cycle in both species and in all four loading modes, despite the wide range of maximum strains recorded in these experiments. Mean magnitudes and orientations of principal tensile and compressive strain were determined for each species. Two-tailed, unpaired t-tests were employed to test for differences in mean strain magnitudes and angles at different sites along the length of the columns, as well as at equivalent sites between the two species. In order to assess the repeatability of measurements for a single set of loading cycles within all four loading modes, overall displacements and applied force were measured in all six loading cycles of each loading mode in one opossum and one armadillo. Because of the time-consumingnature of the measurements, three randomly selected loading cycles out of the six tests obtained for each loading mode were analyzed in the remaining two individuals of each species. To avoid bias, comparisons of the pooled data for each species were based on three loading cycles per individual. RESULTS

Variability within individual tests Figure 4 shows that the force-displacement curves obtained for repeated loading cycles of the same animal are highly repeatable within a given loading mode for both Dasypus and Didelphis; however, torsion is somewhat more variable than the other three bending modes. (Although not included here, the corresponding curves of each loading mode for each species are generally comparable with respect to repeatability.) These graphs also show that the relationship between force and displacement is nonlinear. There is a low stiffness zone at relatively

T.J. GAUDIN AND A.A. BIEWENER

68

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Fig. 4. Applied bending moments (Newtons) versus displacement, which is measured as described in Figure 3 and normalized to the length of the individual vertebral column. (Note that in A, torsion, applied force is a torque measured in Newton-meters, and displacement is measured as the angular displacement of the anteriormost vertebra.) Each graph represents six repetitive loading cycles of an individual opossum or armadillo. A: Torsion

in the opossum Didelphzs. B: Ventral bending in Didelphis. C : Dorsal bending in the armadillo Dasypus. D: Lateral bending in Dasypus. Curves with open squares and black dots represent the first loading cycle, those with black diamonds the second, those with black squares and white dots the third, those with white diamonds the fourth, those with black squares the fifth, and those with white squares the sixth.

small displacements, and a higher stiffness region at larger displacements. Nonlinear force-displacement curves such as these are typical of systems in which soft tissues (e.g., ligaments, tendons) play a n important mechanical role (Wainwright et al., ’82).

a clear infection point. Therefore, these data have been split at this inflection point. The inflection point itself is included in both the low stiffness and high stiffness data sets. The dorsal and lateral bending tests lack a clearly distinguishable inflection point; therefore, their data have been divided in half. In those loading cycles represented by an odd number of data points, the middle value is included in both the low and high stiffness data sets. The torsional data, which deviates the least from linearity, have been left undivided. Reduced major axis regression lines have been fit to both regions of the force/displacement curves. The slopes of these regression lines for all

Overall vertebral column stiffness Because of the nonlinear nature of the force-displacement curves, stiffness measurements for use in comparison between species and among loading modes have been obtained by dividing each curve into a “low” stiffness and “high” stiffness region. Visual inspection of the ventral bending tests reveal

FUNCTIONAL MORPHOLOGY OF XENARTHRAE

loading cycles (n = 9) have then been averaged to establish the mean stiffness of the vertebral columns of the two species at small and large displacements. These stiffness values, as well as their variances, are listed in Table 1 and are illustrated (for the low displacement data sets only) in Figure 6. The backbone of armadillo #1 was damaged at the end of the ventral bending tests. The interspinous ligaments between L5/S1 and L3IL4 tore, resulting in inordinately large angular displacements in dorsal bending (Fig. 5B) and a much lower overall dorsal stiffness for this individual than for the other two armadillos (Fig. 5A). Therefore, these data were excluded from subsequent analyses. The damage at these joints in armadillo #1 did not noticeably affect the results obtained in torsion, presumably because of the torsional immobility of the lumbar vertebrae in the armadillo (see below), nor the results obtained in lateral bending, presumably because the damage occurred along the midline, coincident with the neutral axis of bending. Thus these data have been included in the analyses. In Dasypus (Tables 1and 2 , Fig. 6), roughly equivalent values of stiffness are obtained in dorsal and lateral bending at both small and large displacements. These stiffness values are significantly greater than those obtained TABLE 1. Stiffnessvalues forfour loading modes in the oDossum and armadillo Mean stiffness' 2 standard error

N

Low stiffness region

High stiffness region

6 9 9 9

7.30 t 2.34 0.25 t 0.23 6.04 t 1.63 0.040 t 0.005

30.15 f 9.03 15.82 f 2.90 32.48 f 3.43 NIA

Armadillo,without xenarthrae Dorsal 2 Ventral 3 Lateral 3 Torsion2 3

9.83 2 6.08 -0.04 t 0.56 6.49 2 1.92 0.048 t 0.005

37.83 I 12.16 18.70 % 4.14 33.70 2 13.86 NIA

Ooossum Dorsal Ventral Lateral Torsion2

1.70 t 0.36 0.46 t 0.29 0.93 2 0.16 0.049 c 0.014

14.99 f 2.69 15.24 t 2.01 11.86 2 1.64 NIA

Armadillo Dorsal Ventral Lateral Torsion*

9 9 9 9

'Stiffness values are given in Newtons per unit normalizeddisplacement. 2Torsional stiffness is given in Newton-meters per degree.

69

in ventral bending. A similar pattern holds true for Didelphis at low displacements, but at large displacements, no significant differences are observed among the values of stiffness obtained in the three different bending modes. Interestingly, removal of the xenarthrae from the posterior lumbar vertebrae of Dasypus does not affect the resulting stiffness values. Comparison of the data for the two species reveals little difference in ventral stiffness in either the low or high stiffness regions. Likewise, the two species have similar torsional stiffness. The stiffness of the armadillo backbone in dorsal and lateral bending, however, is much higher than that of the opossum at both low and high ranges of displacement. For all values, except dorsal stiffness at high displacement levels, these differences are significant (Table 2 ) .

Displacement of individual vertebrae One loading cycle of each loading mode has been analyzed for each individual animal in order t o determine the angular displacements of all ten vertebrae at maximum column displacement. As was the case with the stiffness data, the angular displacements obtained from the armaddlo column with all the xenarthrae intact do not differ from those obtained after some of the xenarthrae have been removed (Fig. 7). This applies to all four loading modes, even in the case of deflections that have been measured at vertebrae in which the xenarthrae were removed (L2, L3, L4). The shapes of the curves in all four loading modes are virtually identical in both Dasypus and Didelphis (Fig. 7A-D). This indicates that deflections in both species generally occur at similar locations along the length of the column. Although most of the rotation takes place in the anterior thoracic vertebrae in the two species when the column is loaded in torsion (Fig. 7A), a small amount of rotation also occurs in the posterior thoracic and anterior lumbar vertebrae in the opossum. By contrast, in Dasypus, rotation is restricted to the three anteriormost vertebrae tested, T6-T8, with none occurring in the lumbar and posterior thoracic vertebrae. Vertebral displacements in Dasypus and Didelphis are also similar in ventral bending (Fig. 7B). Ventral bending is distributed fairly evenly along the length of the column of both species, and comparable ranges of angular displacement are achieved. The largest differ-

T.J. GAUDIN AND A.A. BIEWENER '"

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Fig. 5. A: Applied dorsal bending moment graphed versus normalized displacement in the vertebral column of Dasypus. The graph shows nine loading cycles, three from each individual animal. B: Angular displacement in dorsal bending of each individual vertebra in the Dasypus

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column. Data points were measured at maximum column displacement in three loading cycles, one per individual. Vertebrae are numbered 1-10 on the x-axis, with 1 representing the most posterior vertebra (L5). Angular displacement is measured in degrees.

ences in angular displacement of individual the opossum and -40" in the armadillo (in vertebrae between the two species occur when pure torsion, these angles would be 545"). the columns are loaded in dorsal and lateral Note that the strain angles obtained in Dasbending (Fig. 7C,D); the armadillo column ypus are closer to the expected value of 45" allows substantially less angular displace- than those obtained for Didelphis, indicating ment than does that of the opossum. Most of a larger shear component in Dasypus. In these differences appear to be due to a greater ventral and lateral bending (Figs. BB, 9B), stiffness of the thoracic vertebrae of Dasypus the vertebral centra are subjected primarily compared with Didelphis. Whereas the deflec- to compression at the sites (located on the tions of the thoracic and lumbar vertebrae concave side of the bend) to which the strain differ only slightly in Didelphis, the thoracic gages were attached. In both species, the vertebrae of Dasypus are considerably stiffer absolute magnitudes of the principal compresthan the lumbar vertebrae, particularly in sive strains are greater than those of the dorsal bending. principal tensile strains, and are aligned roughly parallel to the long axis of each cenBone strain trum. At more posterior locations, principal I n both species and in all loading modes, compressive strains increase in magnitude, the patterns of bone strain recorded from the corresponding to the increased bending movertebral centra conform closely to the pat- ment applied to the column. Consequently, terns expected of a cantilever beam loaded in the strains recorded a t the posterior lumbar torsion or in bending. Overall, strains devel- strain gage are significantly greater than oped in torsion are smaller than those re- those at the posterior thoracic gage, except corded in bending (Table 3, Figs. 8, 9). Nei- when Dasypus is loaded in lateral bending, in ther Dasypus nor Didelphis shows much which case smaller principal compressive change in the magnitude of principal compres- strains occur posteriorly (Table 3 , Fig. 9B). sive and tensile strains along the length of During dorsal bending, on the other hand, the column in torsion. In addition, principal the centra of both species are subjected primacompressive and tensile strains are roughly rily to tension a t the strain gages recording similar in magnitude at all sites in both spe- sites (positioned on the convex side of the cies and deviate considerably from the long bend). The absolute magnitudes of principal axis of the vertebral column, indicating a tensile strains are larger than those of princilarge component of shear. Mean tensile strain pal compressive strains and are aligned close angles are all near 30" in Didelphis and 50" in to the long axis of the vertebral column (TaDasypus. Correspondingly, mean compres- ble 3, Fig. 9A). Consistent with the increase sive strain angles are approximately -60" in in bending moment, principal tensile strains

71

FUNCTIONAL MORPHOLOGY OF XENARTHRAE 0.6

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Fig. 6. Mean stiffness in Didelphis (---I and Dasypus 1 vertebral column for the following four loading modes. A: Torsion. B Ventral bending. C Dorsal bending. D: Lateral bending. Curves plotted in A torsion represent the full range of torsional displacements, while curves plotted in the remaining three graphs were calculated from the low displacement data sets only. The slopes (=stiffness) and intercepts of these lines were determined by averaging the slopes and intercepts of re-

duced major axis regression lines fit to each of nine individual loading cycles for both species (3 cycles per individual, 3 individuals per species), as described in the Results section. The numerical values of these slopes for all four loading modes, as well as their variance, are given in Table 1. Table 1 also presents values for mean stiffness at high displacements in ventral, dorsal, and lateral bending.

recorded in Dasypus, but not Didelphis, increase significantly at more posterior locations. Not only do the patterns of principal strain magnitude and orientations in the vertebral centra of both species conform closelyto those expected for a cantilever beam loaded in torsion and in ventral bending, but the patterns are also closely similar to each other (Fig. 8). Although the principal compressive strain axis in Dasypus shows a greater deviation relative to the long axis of the column than in Didelphis in both torsion and in ventral bending, other patterns of principal strain do not

differ significantlybetween the two species in either loading mode (Table 4). In addition, removal of the posterior lumbar xenarthrae results in no significant differences in principal strain magnitude for any of the four loading modes. The angle of principal compressive strain relative to the longitudinal axis of the vertebral centrum in ventral bending, however, is significantlyreduced. In contrast to the overall similarity between Dasypus and Didelphis in strain magnitude and orientation for torsion and ventral bending, the two species differ markedly in both dorsal and lateral bending. In dorsal

-(

72

T.J. GAUDIN AND A.A. BIEWENER

TABLE 2. Results ofunpaired, two-tailed t-tests of stiffness at low and high stiffnesslevels

Armadillo Dorsal vs. lateral Dorsal vs. ventral Lateral vs. ventral

P low stiffness region

P high stiffness regon

0.655 0.003' 0.003*

0.786 0.100 0.002*

DISCUSSION

Armadillo, with vs. without xenarthrae Dorsal Ventral Lateral Torsion

0.640 0.576 0.886 0.347

0.675 0.620 0.900

Opossum Dorsal vs. lateral Dorsal vs. ventral Lateral vs. ventral

0.068 0.017* 0.175

0.335 0.942

Opossum vs. Armadillo Dorsal Ventral Lateral Torsion

0.012* 0.569 0.007" 0.570

0.080 0.872

'Significant at the P

column (all sites within 2")than is the case in Didelphis (in which deviations typically range from 5" to 20" for other bending modes). Following removal of the xenarthrae from the posterior lumbar vertebrae, the orientation of principal compressive strain in Dasypus exhibits greater deviations from the longitudinal axis.

NIA

0.211

0.0001*

NIA

= 0.05 level.

bending (Table 3, Fig. 9A), the magnitude of principal tensile strain in the opossum vertebral centra does not increase but, if anything, declines posteriorly, counter to the increase expected due t o an increased bending moment at more posterior locations. Because of this decline, principal tensile strains in Dasypus are significantly higher in the lumbar vertebrae than those recorded in Didelphis. Consistent with strains recorded in ventral bending, however, dorsal bending strain axes in the armadillo exhibit stronger deviations from the long axis of the vertebral column than those in the opossum, this difference being most pronounced in the two lumbar vertebrae (Table 4). After the removal of the xenarthrae, the angles of principal compressive strain in Dasypus are reduced. In lateral bending, the compressive strains of the vertebral centra in Dasypus deviate most from the expected pattern for cantilever bending, as they remain relatively constant along the column's length (Table 3, Fig. 9B). Lateral bending strains in Didelphis, on the other hand, increase posteriorly. Correspondingly, principal compressive strains in the lumbar vertebrae of the armadillo are significantly lower than those recorded in the opossum. Only in lateral bending are the strain orientations in Dasypus more closely aligned with the longitudinal axis of the vertebral

It is clear from the comparisons of overall stiffness of the vertebral columns, of individual vertebral displacements, and of bone strain magnitudes and angles at several sites along the length of the backbone, that in dorsal and lateral bending the mechanical properties of the vertebral column of Dasypus novemcinctus are strongly modified relative to a generalized mammalian condition (as represented by the opossum Didelphis uirginiana). It is equally clear that in ventral bending and torsion the mechanical properties of the vertebral column of Dasypus do not differ significantlyfrom the putative generalized condition. The aim of this study, however, was to determine the mechanical role played by xenarthrae and to examine whether evidence exists t o suggest that xenarthrae might represent an adaptation to a fossorial way of life. Thus, the questions remain, whether the xenarthrae are responsible for the observed differencesbetween Dasyp u s and Didelphis and whether these modified mechanical properties can be ascribed some function in fossorial behavior. Our results fail to show that xenarthrae play any significant role in the mechanical properties of the armadillo backbone during ventral bending. The absence of any clear difference in ventral bending is not wholly unexpected. Slijper ('46) suggested that the primitive mammalian vertebral column was highly mobile in all regions of the column for all types of bending. In his own bending tests of the vertebral column of Didelphis, Slijper concluded that the thoracic and lumbar vertebrae were "very mobile" both dorsally and ventrally, in keeping with their conservative nature. Subsequent work, however, has shown that in mammals with purportedly limber (and hence mechanically conservative) spines, e.g., the tree shrew Tupaia glis (Jenkins, '74) and the cat Felis domesticus (English, '801, ventral displacements are much larger than the corresponding dorsal displacements during galloping locomotion. This higher ventral flexibility is supported by our results for Didelphis in which, at least

FUNCTIONAL MORPHOLOGY OF XENARTHRAE

73

'"1 1W

10

-1

-

I

60

0 -

'

I

WlO XB"

-10

A

4

2

'

6

8

10

c

160-

- Venhal Bending t

+

120-

0

100

0

+

-

80

-

60

-

40

-

0

+ 0

+ 0

. 03 0

P

0

2

4

6

100

.

80 60

.

40

,

2

10

120

i m

.

6

m

+

20-

4

140

o

o

=

+

i

160

+

140-

0

4

20 .

I

6

.

,

'

8

0

,

10

D

8

10

Vertebra Number (1 = Post.) Fig. 7. Angular displacement of 10 individual vertebrae in Didelphis (W)and Dasypus vertebral columns, the latter measured with xenarthrae intact (0) and with the posterior lumbar xenarthrae removed (+). Vertebrae numbered as in Fig. 4B; displacements are measured in degrees. Each point represents the average of three

values, one from each individual animal in the two species, measured at maximum column displacement. A: Torsion. B: Ventral bending. C : Dorsal bending. D: Lateral bending. Note that the plots of torsion (A) have been drawn to a scale of 40", rather than 160",in order to depict differences more clearly between the two species.

for the low stiffness data set, ventral stiffness is significantly lower than dorsal stiffness. The two values are much closer in the high stiffness data set, but the large displacements at which these higher stiffness values are obtained almost certainly are not physiologically relevant. In almost every case, the data were split into high and low displacement data sets at an angular displacement of about 40".The measurements of individual vertebral displacement show that maximum angular displacements of the whole column segments approached or exceeded 90" in all three bending modes in both species, reaching as high as 150"in ventral bending, so that the anteriormost vertebra was almost parallel with the posteriormost vertebra. Maximum angular displacements of the thoracic

and lumbar vertebrae measured during galloping in Monodelphis domestica (Pridmore, '92; Fig. 41, a close relative of Didelphis, as well as the tree shrew Tupaia glis (Jenkins, '741, the cat Felis domesticus (English, 'SO), and the gazelle (Halpert et al., '871, however, do not exceed 50". In addition, we recorded bone strains at an applied force of 4N, a level that is well within the higher stiffness range, but well below peak applied force. The strain magnitudes we obtained even at this "intermediate" applied force are high compared to those measured in vivo by Lanyon ('71, '72) in the lumbar and thoracic vertebral centra of sheep during walking, trotting, and normal respiration. In our mechanical loading tests, principal tensile strains reached magnitudes of over +500

74

T.J.GAUDIN AND A.A. BIEWENER TABLE 3. Principal tensile and compressive strain magnitudes for four loading modes in the opossum and armadillo Mean principal strain magnitude' t SE

Strain gage position Torsion

Post. thor. Ant. lumb. Post. lumb.

Ventral bending

Post. thor. Ant. lumb. Post. lumb.

Dorsal bending

Post. thor. Ant. lumb.

Post. lumb.

Lateral bending

Post. thor. Ant. lumb.

Post. lumb.

N

Tension

Compression

ODossum &madill0 Opossum Armadillo Opossum Armadillo Armadillo, without xenarthrae

9 9 9 9 9 9 3

183 t 48 215 f 45 128 t 32 131 f 13 169 rt_ 37 161 f 19 197 t 33

-184 t 55 -180 t 24 -46 t 43 -130 & 17 -117 -t 29 -140 2 19 -134 -t 18

Opossum Armadillo Opossum Armadillo Opossum Armadillo Armadillo, without xenarthrae

9 9 9 9 9 9 3

174 t 27 170 t 50 132 f 15 94 t 32 93 f 15 111 f 74 129 2 94

-196 f 14 -224 t 36 -294 t 61 -319 f 63 -428 t 16 -314 f 107 -316 f 157

Opossum Armadillo Opossum Armadillo Opossum Armadillo Armadillo, without xenarthrae

9 6 9 6 9 6

-560 -3 -22 -107 -24 -431 -356

2

2

520 2 165 198 f 13 163 t 34 424 i 118 313 f 54 399 ? 63 460 t 193

Opossum Armadillo Opossum Armadillo 0possum Armadillo Armadillo, without xenarthrae

9 9 9 9 9 9 3

164 t 54 223 t 30 425 t 37 97 t 29 433 t 115 248 t 53 169 1: 88

-230 -530 -543 -233 -761 -378 -336

t 85 f 137

125

* 40

f 14 t 19 t 33 f 19 t 105

76 51 t 151 t 54 130

f t

-

'Principal strain magnitudes are given in units of psirain.

kstrain and principal compressive strains in general, the thoracic and lumbar portions reached magnitudes of nearly -800 pstrain of the vertebral column are most flexible in a (overall difference: 1,300 pstrain). The larg- ventral direction. Armadillos apparently have est absolute differencebetween peak compres- not lost any of this primitive ventral flexisive and peak tensile vertebral strains re- bility. Members of the genus Tolypeutes, corded in vivo by Lanyon was only 487 which have well-developed xenarthrae, are kstrain. Although maximum vertebral strains capable of ventroflexing their column t o such during galloping may be greater than this an extent that they can completely roll themvalue, it seems unlikely that the strains we selves up into a ball, demonstrating considermeasured in vitro in Didelphis vertebral cen- able ventral flexibility (and contradicting sugtra, somewhat beyond the middle of the range gestions that xenarthrae have a role in of deflection in our bending tests, would be enrollment behavior: Winge, 1941; Hofftwice that of those measured in vivo in sheep. stetter, 1982). Our measurements of the meIt seems more likely that the strains we mea- chanical properties of the backbone in Dasysured lie somewhat outside the normal phys- pus novemcinctus support the assertion that armadillos retain a primitive mammalian iological range. Our results demonstrate that for physiolog- level of ventral flexibility in their backbones. ically relevant displacement levels in DidelThe similarities between Dasypus and Diphis and, by extension, primitive mammals delphis vertebral columns in ventral bending

75

FUNCTIONAL MORPHOLOGY OF XENARTHRAE

Post Thor

Ant Lumb

Post L i m b

xenarthrae

A Ventral Bending Post. Thor

Ant. Lumb.

Post. Lumb

Opossum

Armadillo

B

El -+.,"

Armadillo. without xenarthrae

Fig. 8 . Diagram of principal strain magnitudes and orientations in Dasypus and DideZDhis vertebral columns subjected to torsion (A) and ventral bending (B).The dark boxes represent the posterior thoracic, anterior lumbar, and posterior lumbar vertebral centra to which the rosette strain gages were applied, as seen in ventral view. The thin line through the middle of each box indicates the longitudinal axis of the vertebral column. The dashed lines in torsion (A) represent an axis set at 45"to the long axis of the column (corresponding to the expected orientations of principal strains in the case of pure torsion). The lines with outwardly directed arrows are principal tensile strains, those with the inwardly directed arrows are principal compressive strains. The

length of these lines are proportional to the magnitudes of mean compressive and tensile strains in the two species, as determined by averaging values from nine loading cycles from three individual animals in each species. Numerical values for the mean strain magnitudes, along with their variances, are listed in Table 3. The average value for the angle between the principal compressive strain axis and long axis of the vertebral centrum (in degrees) is given in the diagram; this angle is indicated on the diagram where practicable. This angle was determined by averaging strain orientations measured in nine loading cycles (3 cycles per individual, 3 individual per species) in each species.

are not surprising. However, it is curious that the mechanical properties of the backbones of Dasypus and Didelphis do not differ more markedly when subjected t o torsion, given the fact that the geometry of the xenarthrous articulations (Fig. 2), with horizontal articulations situated on either side of the vertical zygapophyses, would seem ideal for resisting torsion. The only important differ-

ence discovered in the mechanical properties of the vertebrae of the two species under torsional loads is that, in tests of individual vertebral displacement, all rotation is eliminated from the posterior thoracic and lumbar vertebrae in Dasypus, whereas rotation in Didelphis diminishes posteriorly but is not eliminated. This similarity between the two species under torsional loads is probably at-

T.J.GAUDIN AND A.A. BIEWENER

76

wl Post. Thor.

DorsalBending Post. Lurnb.

An!. Lurnb.

Opossum

P-I)

Armadillo

Armadillo, without xenarthrae

A Lateral Bending

Post. Thor.

Ant. Lurnb.

Post. Lurnb.

Opossum

Armadillo

Armadillo, without xenarthrae

6 Fig. 9. Diagram of principal strain magnitudes and orientations in Dasypus and Didelphis vertebral columns subjected to dorsal (A) and lateral (B) bending. Symbols

used in the diagram are identical to those used in Figure 8, and the values for strain magnitudes and orientations were determined as discussed in Figure 8.

tributable to modifications of the lumbar zygapophyses, which have their origin in the earliest mammals and are retained in both the opossum and armadillo. In early mammals, the lumbar zygapophyses become modified from the horizontal position of mammalian ancestors to a vertical position (Jenkins and Parrington, '76). These vertical zygapophyses, because of their geometry, strongly resist torsional displacement of the lumbar vertebrae. The backbone of Didelphis is already very stiff under torsional loads, and the development of xenarthrae in primitive xenarthrans seems to do little but augment this stiffness slightly from the primitive mammalian condition. Although the vertebral columns of Dasypus and Didelphis show few mechanical dif-

ferences in either torsion or ventral bending, they do show strong differences when their columns are loaded in dorsal and lateral bending. The armadillo column is in both cases significantly stiffer than that of the opossum, especially in the thoracic vertebrae. Unfortunately, we cannot demonstrate conclusively that these changes in dorsal and lateral stiffness are attributable to the xenarthrae. We have attempted to assess the contribution of xenarthrae to overall column stiffness by removing some of these accessory articulations. The lack of any significant change in overall stiffness resulting from the removal of the posterior lumbar xenarthrae, however, is likely not particularly instructive. Comparisons of overall column stiffness may be relatively insensitive to small isolated structural

77

FUNCTIONALMORPHOLOGYOFXENARTHRAE

TABLE 4. Results ofunpaired, two-sample t-tests of strain in the opossum a n d armadillo P-values Ventral Armadillo, with vs. without xenarthrae Posterior lumbar gage Tensile strain 0.897 Compressive strain 0.990 Strain angle 0.026* Opossum vs. armadillo Posterior thoracic gage Tensile strain 0.952 Compressive strain 0.534 Strain angle 0.084 Anterior lumbar gage Tensile strain 0.347 Compressive strain 0.790 Strain angle 0.008* Posterior lumbar gage Tensile strain 0.837 Compressive strain 0.431 Strain angle 0.433 ‘Significant at the P

=

Dorsal

Lateral

Torsion

0.699 0.288 0.057

0.471 0.728 0.074

0.355 0.863 0.900

0.157 0.006* 0.789

0.321 0.127 0.167

0.640 0.952 0.140

0.025* 0.003*

0.001*

0.0001* 0.004’ 0.917

0.939 0.083 0.020*

0.326 0.0001* 0.0001*

0.127 0.016* 0.0006*

0.851 0.520 0.0008*

0.06 level.

modifications of the column, such that more than three of the xenarthrous articulations would have to be removed to record an effect. The lack of any change in the angular displacement of individual vertebrae with the xenarthrae removed, particularly in those vertebrae in which the articulations have actually been modified, is more difficult to understand. If xenarthrae were responsible for resisting changes in angular displacement, this test should have been sensitive enough to detect a difference. It may be, however, that our method of “removing” the xenarthrae by severing, but not completely removing, the anapophyses from the vertebrae in question, does not effectively alter the mechanical properties of the vertebrae. It is quite possible that the differences in dorsal and lateral stiffness between Didelphis and Dasypus may reflect morphological differences in the two columns other than the presence or absence of xenarthrae, e.g., differences in the shape and cross-sectional area of the centra, in the length of the vertebral processes, and in the amount and distribution of intervertebral ligaments. These changes can drastically affect the moment of resistance of the column, and hence its stiffness, but they are difficult to quantify and we have not controlled for any such modifications in the present study. On the other hand, when our data are compared to similar data obtained by Halpert et al. (’871, it does seems likely that xenarthrae do play a significant role in increasing dorsal and lateral stiffness. Large bovids pos-

sess curved zygapophyses and zygapophyseal ridges and labra, structures that cause an interlocking of successive vertebra in a manner analogous to that caused by xenarthrae. Halpert et al. (’87) show that these structures contribute at least in part to the increased dorsal stiffness in the lumbar columns of large bovids. Unlike the former, our experiments do not show a corresponding increase in ventral stiffness; however, it must be remembered that the modifications in bovids are only analogous to those of xenarthrans, and represent modifications of the zygapophyses themselves rather than entirely new articulations formed lateral to the zygapophyses. Moreover, as Halpert et al. (1987) note, and we consider below, the zygapophyses (and xenarthrae) are only one part of an axial system composed ofmuscles, Iigaments, and bone that together control the stiffness of the lumbar region of the animal. In addition to changes in overall stiffness and angular displacement of individual vertebrae, Dasypus shows strong differences in bone strain magnitudes and orientations in dorsal and lateral bending in comparison to Didelphis. In dorsal bending, principal strain magnitudes are significantly smaller anteriorly and larger posteriorly in the armadillo than in the opossum. The posterior increase in strain magnitude in Dasypus is an expected result of cantilever bending. The unexpected decline in strain magnitude at more posterior locations in the backbone of Didelphis are likely attributable to a progressive increase in the moments of resistance of the

78

T.J. GAUDIN AND A.A. BIEWENER

more posterior vertebral centra (Slijper, '46). For all loading modes except lateral bending, principal strain orientations in Dasypus deviate more strongly from the longitudinal axis of the vertebral column than do those measured in Didelphis, indicating a greater shear component to centrum strains. Though principal strain magnitudes are unaffected, after subsequent removal of the xenarthrae, the resulting strain orientations are more closely aligned with the long axis of the vertebral centra (except in torsion, for which no significant change is recorded). The fact that shear is typically higher in the centra of Dasypus than in the centra of Didelphis, together with the fact that removal of the xenarthrae reduces shear, imply that xenarthrae are a t least partially responsible for the changes in strain orientations and increase in shear. It is possible that the articulations decrease the ratio of length to diameter (i.e., the aspect ratio) of the vertebral centra. Shear becomes increasingly important relative to tensile and compressive strains generated by bending loads in beams with very low aspect ratios (Roark and Young, '75). Hence, xenarthrae may serve to widen the effective compressive or tensile resisting area of the vertebral centra of Dasypus, so that the transverse, accessory, and mammillary processes, and not just the centrum itself, contribute to resisting compressive and tensile loads transmitted along the column's length. Such a n interpretation would be consistent with Jenkins's ('70) hypothesis that xenarthrae aid in the transmission of forces along the backbone from the forelimbs to the pelvic girdle. In contrast to the results obtained for torsion and for ventral and dorsal bending, in lateral bending the principal strains in the intact backbone of Dasypus are aligned more closely to the long axis of the centra than was the case in either Didelphis or Dasypus after the removal of the xenarthrae. The reason for this implied reduction in shear stress is unclear. Anterior principal strain magnitudes in Dasypus are greater than in Didelphis, and posterior principal strains are lower, exactly opposite the results obtained for dorsal bending. These data can be explained in part by differences in the shape of the centra in the two species. The vertebral centra of the armadillo are lower and wider than those of the opossum, and hence have a greater lateral moment of resistance. However, the lateral moments of resistance of the vertebral centra in the backbone of Dasypus do

not show a progressive increase posteriorly. Given the progressive increase in the bending moment posteriorly, these lateral moments of resistance alone do not seem to account for the posterior drop in strain magnitudes in Dasypus. We believe that the low lateral strains in the posterior regions of the column of Dasypus may be explained by the presence of xenarthrae. If xenarthrae increase the width of the effective load bearing area of the centra, as hypothesized above, they would provide a further increase in the lateral moments of resistance of the centra. Moreover, if Jenkins ('70) is correct in hypothesizing that xenarthrae increase the ability of the vertebral column to transmit force along its length and to the pelvic girdle, xenarthrae may be transmitting part of the force that, under lateral bending moments, normally passes through the vertebral centra from front to back. This would presumably further reduce the strain in the vertebral centra. The primary aim of this study was to analyze the functional role of xenarthrae by examining differences in the mechanical properties of the vertebral columns of Didelphis and Dasypus and determining whether these differences could be attributed to the presence of xenarthrae. The above results suggest that a t least some of the observed mechanical differences are indeed due to the presence of these accessory articulations. This study has also attempted to determine whether xenarthrae could be inferred to represent an adaptation to a fossorial way of life in the common ancestor of the order Xenarthra. Xenarthrae are a synapomorphy of the order. Thus they represent a potential adaptation of the order, in the true sense of the word (Gould and Lewontin, '79), as they are an evolutionary novelty that appeared in the common ancestor. However, in order to establish that the modifications in the mechanical properties of the Dasypus column in dorsal and lateral bending, which at least in part appear to be due to the presence of xenarthrae, play some role in digging behavior and hence could possibly represent adaptations to fossoriality, requires information about the function of the axial skeleton in digging mammals in general. Unfortunately, little is known about the function of the axial skeleton in mammals. Similarly, the functional morphology of digging mammals as a whole, axial function notwithstanding, has been largely ignored in the literature. As Hildebrand ('85) pointed

FUNCTIONAL MORPHOLOGY OF XENARTHRAE

out, most of the work on digging mammals has been in the form of descriptive studies of myology and osteology,which have then been used as a basis for speculation on how these elements function in a living animal. Kinematic studies of fossorial mammals are rare, and electromyographic studies nonexistent. Gasc et al. ('86) published a cinefluorographic study of digging in the Cape Golden Mole, Eremitalpa granti namibensis. The Cape Golden Mole is a sand swimmer, whereas Dasypus and all the other armadillo genera are surface scratch-diggers (Hildebrand, '851,and as Gasc et al. ('85)note, one must be cautious in generalizing between species that exhibit different modes of digging. However, there are likely enough similarities in the digging styles of the two species that a comparison seems worthwhile. Gasc et al. ('86) showed that the alternating digging stroke of the golden mole results in a lateral bending moment being exerted on the vertebral column. In addition, because the digging stroke is directed ventrally against the substrate, a dorsal reaction force is transmitted through the forelimbs and shoulder girdle to the vertebral column. Gasc et al. ('86) demonstrate that, in order to resist the dorsal reaction force and provide a stable base so that the forelimbs can concentrate muscular effort on tunneling through sand, the backbone of the golden mole is fully extended throughout the power stroke. The high dorsal stiffness of the posterior portion of the vertebral column in Dasypus allows it to serve an analogous role to that of Eremitalpa. Furthermore, the high lateral stiffness of the column of Dasypus would be useful in resisting the lateral bending moment exerted on the column by the alternating digging stroke, and could provide a stable platform from which the forelimbs could exert force. In as much as xenarthrae are responsible for the increased dorsal and lateral stiffness of the backbone, they play a significant role in the digging behavior of Dasypus. Since Dasypus retains a relatively primitive xenarthran vertebral morphology, we believe that our results are fully consistent with an interpretation of xenarthrae as an adaptation for fossorial behavior in the early members of the order Xenarthra. It should be noted that the idea of the backbone of the armadillo being used during digging as a rigid platform off of which the forelimbs operate is reminiscent of Frechkop's ('49) suggestion that, in the armadillo Przodontes, the

79

backbone is used as a stiff rod t o support the trunk, freeing the forelimbs for digging. However, Frechkop's hypothesis requires that the vertebral column resist a ventrally directed force, namely that produced by the weight of the trunk and forelimbs, not a dorsal reaction force generated by the forelimbs during digging. Our results clearly show that Dasypus does not increase ventral stiffness relative to the generalized mammalian condition as exemplified by Didelphis. In conclusion, we would like to note that the differences in mechanical properties of the posterior thoracic and lumbar vertebral column in Dasypus and Didelphis are not as dramatic as might have been anticipated, given the truly remarkable nature of the structural modifications of the intervertebral articulations in the former. However, the presence of xenarthrae is just one of a large suite of morphological differences between the axial skeleton of armadillos and that of Didelphis. These differences would include hypertrophy of the neural spines and mammillary processes; widening and flattening of the vertebral centra, so that they lose the cylindrical shape of opossum centra; anteroposterior expansion of the ribs; reduction in the overall length of the lumbar region of the spine, so that the hindmost ribs come to lie close t o the anterior border of the ilium; enlargement of the pelvic girdle and fusion of the ischium to the caudal vertebrae; tremendous increase in the volume of epaxial musculature; and the presence of a bony dermal carapace. All these modifications are likely to effect the overall stiffness of the axial skeleton, yet none of these modifications has been studied in detail with an eye toward its role in functioning of the axial skeleton in armadillos. Some of these modifications are also found in other digging mammals. For example, pangolins possess cylindrical lumbar zygapophyses (Frechkop, '49) similar to those found in the large bovids described by Halpert et al. ('%), and the enlargement of the pelvis and its attachment to the vertebral column is common to many digging mammals (Hildebrand, '85; personal observation). It would be of great interest to learn whether these structures play similar functional roles in different groups of digging mammals. Certainly if xenarthrae are adaptations for fossorial behavior, as we have suggested,then they are just one of many such modifications. Indeed, further study may reveal that the

80

T.J.GAUDIN AND AA. BIEWENER

primary role of xenarthrae is to serve as a n broad attachment surface for the enlarged epaxial musculature of xenarthrans. However, the present data set does suggest that the xenarthrae, one of the most notable synapomorphies of the order Xenarthra, represent an adaptation for digging, lending new credence to the old idea that the Xenarthra represent a n early fossorial offshoot of placental mammals. ACKNOWLEDGMENTS

We wish to thank Larry Frolich, William Turnbull, James Hopson, and John Flynn for their most helpful discussions of this project, and for their various insights and suggestions. Our thanks go as well to Drs. Hopson and Flynn, to Stuart Sumida, John Wible, Carl Gans, and to three anonymous reviewers for reading this manuscript and providing us with valuable comments and criticisms. We are grateful to John Gilpin for his help in constructing the testing apparatus, to Bill Stevens for the use of his video equipment, and to Michael LaBarbera for the loan of his force transducer. The animals used in these experiments were purchased from Scott Haas of Brandon, Florida, and from Ray Singleton & Co. of Punta Gorda, Florida. In addition, we wish to thank Joshua Laerm of the University of Georgia and William Stanley of the Field Museum of Natural History’s Division of Mammals for their help in obtaining specimens for preliminary studies. The videotapes of these experiments were digitized at the Field Museum’s morphometrics laboratory with the kind permission of Dr. Flynn. We are very grateful to all who assisted us in the preparation of specimens and the execution of these tests, including Larry Frolich, Suzanne Gaudin, Mark Schultz, Bill Stevens, Yu Chao, and Denise Nebgen. Finally, we wish to thank Claire Vanderslice for her advice on preparing some of the figures for this paper. This research was supported by a grant from the Hind’s Fund of the Committee on Evolutionary Biology at the University of Chicago. LITERATURE CITED Adams, M.A., and W.C. Hutton (1985) The effect of posture on the lumbar spine. J . Bone and Joint Surg. 67Br625-629. Brown, T., R.J. Hansen, and A.J. Yorra (1957) Some mechanical tests on the lumbosacral mine with Darticular reference to the intervertebral discs. J. BoAe and Joint Surg. 39At1135-1164. Cyron, B.M., W.C. Hutton, and J.R.R. Stott (1979) The mechanical properties of the lumbar spine. Eng. Med. 8.63-68.

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