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Keywords:

  • Allodesmus;
  • function;
  • mechanics;
  • Odobenus;
  • Otariidae;
  • Phocidae;
  • vertebral column

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Author contributions
  10. References
  11. Supporting Information

Regional variation in the axial skeleton of pinnipeds (seals and walruses) and its correlation with aquatic locomotory behaviour is examined using vertebral functional profiles. The results demonstrate clear morpho-functional differences in the thoracolumbar region of modern pinnipeds (Phocidae, Otariidae, Odobenus) that can be strongly linked to swimming style. Phocid seals have a rigid thoracic region attached to a highly flexible lumbar region with long muscular lever arms providing the necessary mobility and leverage to perform pelvic oscillations. Conversely, otariid seals have extremely flexible inter-vertebral joints along the length of the column which should enhance manoeuvrability and turning performance. They also have greater muscular leverage in the anterior thoracic region to support pectoral oscillations. Odobenus (walrus) shows vertebral characteristics most similar to phocids, but with some otariid qualities, consistent with an intermediate or mixed form of aquatic locomotion, with pelvic oscillation dominating over pectoral oscillation. Comparison of the vertebral functional profiles in the fossil taxon Allodesmus kernensis with those of modern pinniped clades reveals that this extinct pinniped may also have used a combination of pectoral and pelvic oscillatory movements during swimming, but in a manner opposite to that of Odobenus, with pectoral oscillatory movements dominating. This study raises questions about the evolution and diversification of pinniped locomotory behaviours, but also provides the necessary framework to begin to examine axial mechanics and locomotory stages in other fossil pinnipedimorphs and their relatives in more detail.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Author contributions
  10. References
  11. Supporting Information

The secondary adaptation of tetrapods to life in the water is a recurrent evolutionary theme which has taken place in phylogenetically diverse groups, including reptiles, birds and mammals (Mazin & de Buffrénil, 2001). Within mammals, secondarily aquatic forms range from fully aquatic cetaceans and sirenians to amphibious taxa that represent intermediate stages in the transition from fully terrestrial to fully aquatic modes of life. One such clade which has made the land-to-water transition is the largely aquatic Pinnipedia, which includes seals and walruses. Pinnipeds display numerous adaptations for moving through water that are common to most other marine forms, including streamlining and development of flippers. However, one of the most noticeable differences amongst modern pinnipeds (Phocidae, Otariidae and Odobenus) is the way in which aquatic locomotion is achieved.

In the water, phocids (true or earless seals) swim by pelvic oscillation with thrust being generated by horizontal undulations of the spine in conjunction with protraction and retraction of the hindflippers (Fish et al. 1988). In contrast, otariids (eared seals or fur seals and sea lions) swim by pectoral oscillation with thrust being produced almost exclusively by the enlarged foreflippers and the hindflippers only providing directional control (English, 1976b; Feldkamp, 1987). Odobenus (walrus), which contains only one modern representative, Odobenus rosmarus, use an intermediate form of locomotion. During swimming, Odobenus primarily uses horizontal pelvic oscillation of the posterior portion of the spine and hindflippers (phocid-like); however, the foreflippers are also used at slow speeds (otariid-like) (Gordon, 1981).

The striking contrast in aquatic locomotory behaviour amongst modern pinniped groups is reflected in modifications of their postcranial morphology: pelvic oscillators have narrow glenoid fossae, large crescent-shaped hindflippers and enlarged lumbar vertebrae, whereas pectoral oscillators have rounded glenoid fossae, enlarged supraspinous fossae marked with accessory spines, and foreflippers enlarged by the development of cartilaginous extensions of the digits (Berta & Adam, 2001; Berta et al. 2006). Whereas the relationship between limb morphology and locomotor performance in pinnipeds has been well studied (e.g. Tarasoff, 1972; English, 1976a,b, 1977; Gordon, 1983; Polly, 2008; Fujiwara, 2009), variation in vertebral morphology and its functional significance have received much less attention (Giffin, 1992). Considering that the axial musculoskeletal system plays a key role in directing mobility and transmitting forces generated during locomotion (e.g. Pabst, 2000; Long et al. 2002; Schilling & Carrier, 2010; Schilling, 2011), determining the existence, location, and extent of variation in the vertebral column is central to understanding the evolution and differentiation of pinniped locomotor styles.

Past investigations into the functional relevance of regional variation along the vertebral column have identified a strong link between vertebral anatomy and locomotor performance (e.g. Slijper, 1946; Hebrank et al. 1990; Gal, 1993a,b; Long et al. 1997). As such, vertebral functional profiles, i.e. variation in mechanically important vertebral parameters along the vertebral column, have been used as a comparative tool to interpret the evolution of locomotion stages in modern and extinct taxa (e.g. Finch & Freedman, 1986; Buchholtz, 1998, 2001a,b; Hua, 2003; O’Keefe & Hiller, 2006; Lindgren et al. 2007). In this study we aim to quantify morphological variation in the vertebral column of modern pinnipeds using vertebral functional profiles and correlate it with aquatic locomotory behaviour. We then use the comparative dataset to test hypotheses of aquatic locomotion potential in the Miocene pinniped, Allodesmus kernensis (Desmatophocidae; Phocoidea). As A. kernensis is known from a virtually complete vertebral column (Mitchell, 1966) it is an ideal fossil candidate to begin to examine and compare patterns of vertebral morpho-functional variation in extinct pinnipeds. Moreover, the primary mode of aquatic locomotion in A. kernensis has been a contentious issue.

It was originally thought that A. kernensis primarily used its forelimbs in aquatic locomotion (Mitchell, 1966; Barnes, 1972). However, analysis of the functional implications of neural canal anatomy by Giffin (1992) showed that both its fore- and hindflippers were quite heavily innervated, a pattern most consistent with carnivores that use both the fore- and hindlimbs during swimming. Berta & Adam (2001) claimed that A. kernensis retains several features consistent with forelimb propulsion but also displays adaptations for hindlimb swimming, although no details are given. Nonetheless, in an evaluation of locomotor evolution in pinnipedimorphs, they code A. kernensis as a hindlimb swimmer, presumably because this interpretation is most parsimonious with it belonging to the sister group to phocids. Most recently, Bebej (2009) assessed the skeletal proportions of A. kernensis (and other pinnipeds) in a quantitative framework. An examination of 14 trunk and limb measurements, of which only two were from the axial skeleton, found A. kernensis to be most similar to forelimb-dominated swimmers. Here we further explore swimming potential in A. kernensis using vertebral functional profiles and develop a locomotor hypothesis based on functional signals from both the vertebrae and limbs.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Author contributions
  10. References
  11. Supporting Information

Specimens and morphometrics

A total of 28 wild procured museum specimens were analysed in this study, which included: 13 phocids (including 10 genera and 10 species), 11 otariids (including seven genera and 10 species), three Odobenus (one genus and species) and one fossil specimen, A. kernensis (Supporting Information Table S1). As there are ∼ 34 species of modern pinniped currently recognised, this study encompasses ∼ 62% (21/34 species) of the taxonomic diversity present. Only specimens which were preserved disarticulated and with a complete vertebral series were examined. The majority of specimens were adults, but in a few cases large sub-adults (judged from limb epiphyseal/skull sutural fusion) were sampled. The study was restricted to the thoracic and lumbar (thoracolumbar) vertebrae, the region of the vertebral column suspended between the limbs and most likely to be engaged during locomotion. The cervical vertebrae, although possibly relevant to locomotor performance, were excluded from the analysis, as variation in the neck region was presumed to be more influenced by feeding behaviour. In pinnipeds there are typically 15 thoracic (rib-bearing) vertebrae and five lumbar vertebrae (except in Odobenus rosmarus and Hydrurga leptonyx (S. E. Pierce, personal observation), which have 14 thoracic and six lumbar vertebrae), for a consistent thoracolumbar count of 20 vertebrae in each species, including A. kernensis.

Morphometric measurements were selected to represent the major functionally relevant aspects of vertebral morphology, which reflect vertebral flexibility/stiffness, range of mobility, muscular leverage and orientation of musculature attachments. With this in mind, 11 biomechanically informative linear and angular measurements were taken on all thoracolumbar vertebrae (Fig. 1; Table S1); however, transverse process measurements were not possible on thoracic vertebrae 12–15 because at this point, ribs become single-headed and transverse processes disappear. Each of the 11 measurements was repeated three times and the mean calculated, with the final dataset consisting of 28 specimens, 560 vertebrae and 6160 measurements. Inter-zygapophyseal length (or the degree of zygapophyseal overhang) was determined by subtracting centrum length (CL) from zygapophyseal length (ZL); this measurement is comparable to that defined by Jenkins (1974) and takes into account the possible correlation between zygapophyseal length and centrum length. All measurements were taken by one observer (S.E.P.) to ensure reliability. Linear measurements were made with digital callipers to the nearest 0.01 mm and angular measurements were taken with a goniometer to the nearest degree.

image

Figure 1.  Biomechanically informative measurements. CH: centrum height (taken on posterior endplate). CL: centrum length (taken along the ventral margin). CW: centrum width (taken on posterior endplate). LW: lamina width (taken posterior to the transverse processes). NPLA: neural spine lever arm (taken from centre of endplate). NSA: neural spine angle (taken from the horizontal plane with anterior set to 0°). PZA: prezygapophyseal angle (taken between prezygapophyses). TPAP: transverse process anteroposterior projection (taken from the horizontal plane with anterior set to 0°). TPDV: transverse process dorsoventral projection (taken from the sagittal plane with dorsal set to 0°). TPLA: transverse process lever arm (taken from centre of endplate). ZL: zygapophyseal length (taken as maximum distance). Inter-zygapophyseal length (I-ZL) (or degree of zygapophyseal overhang) was calculated by subtracting CL from ZL. The images represent the second lumbar vertebra from Halichoerus grypus (Grey seal), UMZC K.7943.

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Data analysis

Prior to analysis, all linear measurements were size-normalised to ensure that variation along the thoracolumbar region could be attributed to shape differences, rather than size differences. Size was removed using the equation inline image, where Madj: size-adjusted measurement, M: original measurement, Ls: overall mean thoracolumbar length for all pinnipeds, Lo: thoracolumbar length (approximated by summing centrum length from each of the 20 vertebrae analysed), and b: slope of the regression of log10M on log10Lo for each measurement and using all specimens (Elliott et al. 1995). The size-normalised linear measurements were then log10-transformed.

To ascertain whether or not specimens could be combined to create average vertebral functional profiles for each of the three modern pinniped clades, a principal components analysis (PCA) was conducted on all size-normalised linear measurements. To ensure that size was not influencing the pattern of specimens in the resultant morpho-functional space, each significant principal component (PC), as determined by the broken stick method, was regressed on thoracolumbar length using ordinary least squares (OLS). Following the PCA, and to assess statistical significance, PC scores accounting for ∼ 90% of the variance in the data were extracted for each specimen and subjected to a manova, with each major modern pinniped clade (Phocidae, Otariidae, Odobenus) as the grouping variable.

To visualise patterns of variation along the thoracolumbar region, data for each modern pinniped clade were combined and the mean calculated for each of the 11 biomechanical measurements. The mean data were then plotted as a percentage of thoracolumbar length. Data for A. kernensis were plotted on the same graphs to compare its vertebral pattern against known functional profiles in order to hypothesise about locomotor potential in this fossil taxon. In addition to profile lines, the data were partitioned into four bins, each bin comprising 25% of the thoracolumbar length or five vertebrae. We then performed anovas on each bin, for each measurement, with the major clades (Phocidae, Otariidae, Odobenus, Allodesmus) as the grouping variable to assess statistical differences in each of the four regions of the axial skeleton examined, i.e. anterior thoracic region, middle thoracic region, posterior thoracic region, and lumbar region. These four regions also provide an important separation when assessing the functional anatomy of the transverse processes, as transverse processes in the thoracic region may not be serially homologous with those in the lumbar region.

All statistical analyses were conducted in past version 2.06 (Hammer et al. 2001). Missing data for A. kernensis were replaced by variable average substitution for linear measurements; missing data were not replaced for angle measurements so as not to influence the orientation of muscular attachments.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Author contributions
  10. References
  11. Supporting Information

Vertebral morpho-functional space

PCA of the size-normalised linear measurements found two major axes, with PC1 and PC2 accounting for 66.36% and 11.82% of the variance in the dataset, respectively (see Supporting Information Table S2 for variable loadings). OLS regressions of the first two PC axes on thoracolumbar length found a non-significant relationship (PC1 P = 0.8542; PC2 = 0.8925), indicating that the recovered pattern in morpho-functional space is due to shape variation and not specimen size. A scatter plot of PC1 and PC2 (Fig. 2A) clearly shows that all three major pinniped clades occupy distinct regions of morpho-functional space. It is also evident that A. kernensis occupies a central position in morpho-functional space, with a slight tendency towards otariids and Odobenus. Our manova of the PC scores along the first five PC axes (accounting for 89.413% of the total variance) recovered a significant difference between groups (Wilks’ lambda < 0.001), with each of the three modern pinniped clades occupying significantly different areas of morpho-functional space (Hotelling’s pairwise comparisons: phocids/otariids < 0.001; phocids/Odobenus P < 0.001; Otariids/Odobenus P = 0.002). This result indicates that our data can be confidently pooled to create average vertebral functional profiles for each of the modern pinniped clades.

image

Figure 2.  (A) Results from principal components analysis of log (size normalised) linear measurements. (B–H) Linear functional profiles plotted as a percentage of thoracolumbar length. Suggested functional implications of each measurement are depicted on the right-hand side of each graph. The dashed line indicates the transition between the thoracic and lumbar regions; this transition takes place one step/vertebra earlier in Odobenus rosmarus and Hydrurga leptonyx. Note that the first lumbar transverse process lever arm datum point for H. leptonyx was not used when calculating the phocid average for this measurement.

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Linear functional profiles

Centrum length (CL)

Phocids show extreme differentiation of CL along the thoracolumbar region. There is an almost exponential increase in CL anteroposteriorly, with the thoracic region having very short vertebrae and the lumbar region very long vertebrae (Fig. 2B). In contrast, otariids display an undifferentiated thoracolumbar region in terms of CL, with all vertebrae being moderate in length, whereas Odobenus shows a gradual but modest increase in CL along the length of the column (Fig. 2B). In all regions of the column, except the posterior thoracic region, phocid CL differs significantly from both otariids and Odobenus, whereas otariids and Odobenus only differ with respect to the anterior thoracic region (Table 1). The profile of A. kernensis shows a slight decrease in CL from the anterior thoracic to the posterior thoracic region and then a slight increase through the lumbar region (Fig. 2B). Visually, this pattern is the inverse of that seen in Odobenus; statistically, CL in A. kernensis is most similar to otariids and Odobenus and significantly different from that seen in phocids, with centra being longer in the anterior region and shorter in the posterior region of the column (Table 1).

Table 1. anova and pairwise comparison results for vertebral functional differences between the major clades of modern pinnipeds and Allodesmus kernensis. Data were grouped into bins comprising 25% of the thoracolumbar length or five vertebrae each; this is anatomically equivalent to the anterior thoracic, mid-thoracic, posterior thoracic and lumbar regions. Missing linear data for A. kernensis were replaced by variable column averages. Italics indicates significance at = 0.05. Bold indicates significance using a Bonferroni-corrected P-value (All groups = 0.008; Moderns only = 0.01). Dashed line indicates insufficient data to run analysis.
 anovaTukey’s pairwise comparison P-value
F test P-valuePhocids/OtariidsPhocids/OdobenusOtariids/OdobenusPhocids/AllodesmusOtariids/AllodesmusOdobenus/Allodesmus
  1. CL, centrum length; CH, centrum height; CW, centrum width; NSLA, neural spine lever arm; TPLA, transverse process lever arm; I-ZL, inter-zygapophyseal length; LW, lamina width; PZA, prezygapophyseal angle; NSA, neural spine angle; TPDV, transverse process dorsoventral projection; TPAP, transverse process anteroposterior projection.

CL, %
 5–25< 0.001< 0.001< 0.0010.004< 0.0010.035< 0.001
 30–500.002< 0.001< 0.0010.878< 0.0010.4770.885
 55–750.0020.1520.3410.953< 0.0010.0380.013
 80–100< 0.001< 0.001< 0.0010.572< 0.0010.7780.292
CH, %
 5–25< 0.0010.002< 0.0010.9740.0010.9930.999
 30–50< 0.001< 0.001< 0.001< 0.0010.0050.765< 0.001
 55–75< 0.0010.0090.415< 0.0010.2990.2620.017
 80–100< 0.001< 0.0010.731< 0.001< 0.001< 0.001< 0.001
CW, %
 5–25< 0.0010.106< 0.001< 0.001< 0.001< 0.0010.991
 30–50< 0.0010.758< 0.001< 0.0010.1340.0210.001
 55–75< 0.001< 0.001< 0.001< 0.0010.120< 0.001< 0.001
 80–100< 0.001< 0.0010.010< 0.0010.990< 0.0010.019
NSLA, %
 5–25< 0.001< 0.001< 0.0010.962
 30–500.0010.3240.0020.08510.3140.003
 55–75< 0.001< 0.0010.081< 0.001< 0.0010.444< 0.001
 80–100< 0.001< 0.0010.016< 0.0010.002< 0.001< 0.001
TPLA, %
 5–250.0080.1080.7360.0150.2170.9760.034
 30–50< 0.001< 0.0010.570< 0.001< 0.0010.868< 0.001
 55–75
 80–100< 0.001< 0.0010.562< 0.0010.009< 0.0010.115
I-ZL, %
 5–250.0130.54910.5550.0190.2320.020
 30–50< 0.001< 0.0010.371< 0.0010.0010.981< 0.001
 55–75< 0.0010.9090.0040.0010.9960.8150.007
 80–100< 0.001< 0.001< 0.0010.0040.0050.249< 0.001
LW, %
 5–250.0090.0080.9000.0330.6860.0740.973
 30–50< 0.001< 0.0010.343< 0.001< 0.001< 0.001< 0.001
 55–75< 0.001< 0.0010.003< 0.001< 0.001< 0.001< 0.001
 80–100< 0.001< 0.0010.347< 0.0010.988< 0.0010.215
PZA, %
 5–250.9950.9960.9990.995
 30–500.0030.27830.0030.043
 55–750.9060.9740.9240.9990.9990.9931
 80–1000.0450.081210.0750.9990.0970.980
NSA, %
 5–250.0050.0340.0050.567
 30–500.0600.5410.0510.292
 55–750.4830.9990.5440.5800.8220.8510.961
 80–100< 0.0010.435< 0.0010.014< 0.001< 0.0010.085
TPDV, %
 5–250.9280.9900.9670.923
 30–50< 0.001< 0.001< 0.0010.064
 55–75
 80–1000.7060.7530.9990.745
TPAP, %
 5–250.1600.1780.2680.960
 30–50< 0.001< 0.0010.133< 0.001
 55–75
 80–1000.9610.9840.9580.994
Centrum height (CH)

CH patterns closely mirror those of CL, with phocids having an almost exponential increase in CH along the thoracolumbar region, otariids having a relatively constant yet moderate CH, and Odobenus having a gradual increase in CH anteroposteriorly along the column (Fig. 2C). The CH profile in phocids is significantly different from that of otariids in all regions except the posterior thoracic region, being lower anteriorly and higher posteriorly. Odobenus has significantly taller centra than phocids in the anterior region of the column, but similar CH in the posterior thoracic and lumbar regions (Table 1). Odobenus also shows significantly taller centra than otariids throughout the column, except in the anterior thoracic region (Table 1). The vertebral profile of A. kernensis is almost parabolic in shape, with the anterior thoracic and lumbar centra being much taller than those mid-column (Fig. 2C). Visually, this pattern is most consistent with otariids in the anterior region and phocids in the posterior region of the column; statistically, the CH of A. kernensis is most similar to otariids through the thoracic region, but the lumbar region shows an intermediate CH with lower centra than phocids and Odobenus and taller centra than otariids (Table 1).

Centrum width (CW)

With respect to CW, phocids show a sigmoid pattern along the thoracolumbar region, with narrow centra through the anterior thoracic region, a steady increase in width throughout the middle to posterior thoracic region, and then a levelling off of CW for the remainder of the column (Fig. 2D). Otariids have very narrow centra that steadily decrease in width anteroposteriorly, whereas Odobenus has very wide centra that increase in width from the anterior to the posterior thoracic region and then decrease in width through the lumbar region (Fig. 2D). Statistically, phocids show significantly wider centra in the posterior region of the column when compared to otariids, but have significantly narrower centra in the anterior region of the column when compared to Odobenus. In addition, Odobenus has a significantly different CW pattern as compared to otariids, being wider throughout the column (Table 1). The profile of A. kernensis shows an almost constant centrum width throughout the thoracolumbar region, but with a slight decrease in width mid-column. Visually, the overall pattern is the inverse of that seen in Odobenus; statistically, CW in A. kernensis is most similar to Odobenus in the anterior thoracic region and phocids in the remainder of the column (Table 1).

Neural spine lever arm (NSLA)

Phocids have a fairly constant NSLA length along the thoracolumbar region, but they are slightly longer in the lumbar region (Fig. 2E). Both otariids and Odobenus show a similar NSLA profile, with NSLA starting off very long and decreasing in length towards the posterior thoracic region and then levelling off. However, the decrease in NSLA length is much more extreme in otariids, with very short NSLA in the lumbar region (Fig. 2E). The NSLA pattern in phocids is statistically different from that in otariids and the anterior region in Odobenus, but NSLA length in phocids and Odobenus is indistinguishable in the posterior region of the column (Table 1). As the profile suggests, otariids and Odobenus have similar NSLA lengths in the anterior thoracic region, but otariids have significantly shorter NSLA than Odobenus in the posterior thoracic and lumbar regions (Table 1). The NSLA profile in A. kernensis appears to decrease in length through the thoracic region similar to otariids and Odobenus, and increase in length in the lumbar region like phocids, but to a more extreme degree (Fig 2E). Statistically, A. kernensis has similar NSLA lengths to otariids in the thoracic region, but the pattern of lumbar NSLA lengths is significantly different from all modern pinnipeds (Table 1).

Transverse process lever arm (TPLA)

The TPLA profile is very similar between all groups, decreasing in lateral projection through the thoracic region and then increasing in lateral projection in the lumbar region. However, the TPLA projection is statistically much shorter in otariids than in both phocids and Odobenus (Fig. 2F; Table 1). The profile of A. kernensis matches the pattern seen in modern pinnipeds (Fig. 2F); however, the thoracic vertebrae have shorter TPLA similar to otariids, whereas the lumbar vertebrae have long TPLA like phocids and Odobenus (Table 1).

Inter-zygapophyseal length (I-ZL)

The I-ZL profiles in phocids and otariids are mirror images, with a decrease in I-ZL from the mid-thoracic to the lumbar region in phocids and an increase in I-ZL from the mid-thoracic to lumbar region in otariids (Fig. 2G). Conversely, Odobenus has relatively long I-ZL along the thoracolumbar region (Fig. 2G). Statistically, Odobenus has significantly longer I-ZL than phocids and otariids from the mid-thoracic region posteriorly (Table 1). In addition, phocids have significantly longer I-ZL than otariids in the mid-thoracic region, but shorter I-ZL in the lumbar region (Table 1). The profile of A. kernensis is visually very similar to that in otariids and statistically they are indistinguishable (Fig. 2G; Table 1). However, the I-ZL in A. kernensis are statistically shorter than those in Odobenus from the mid-thoracic region posteriorly and longer in the lumbar region than those in phocids (Table 1).

Laminar width (LW)

All three pinniped clades have similar LW profiles, with a gradual decrease in width anteroposteriorly; however, otariids have significantly narrower LW than both phocids and Odobenus (Fig 2H; Table 1). Allodesmus kernensis has a distinct profile, showing a decrease in LW throughout the thoracic region and then a sharp increase in LW in the lumbar region (Fig. 2H). LW in the middle to posterior thoracic region is significantly different from modern pinnipeds, but the lumbar region is similar in width to phocids and Odobenus (Table 1).

Angular functional profiles

Prezygapophyseal angle (PZA)

The PZA profiles are virtually identical in all three modern pinniped clades and A. kernensis (Fig. 3A). The first few thoracolumbar vertebrae start off near 90° and then dramatically leap to > 200° for the remainder of the anterior and mid-thoracic region. In all cases, thoracic vertebra 11 (55% of thoracolumbar length) is the diaphragmatic vertebra, except in Odobenus, where the diaphragmatic vertebra is T12 (60% of thoracolumbar length). After this point, the PZA become acute and maintain an angle of around 55° for the remainder of the column. Statistically, all groups have very similar PZA (Table 1).

image

Figure 3.  (A–D) Angular functional profiles plotted as a percentage of thoracolumbar length. Suggested functional implications of each measurement are depicted on the right-hand side of each graph. The dashed line indicates the transition between the thoracic and lumbar regions; this transition takes place one step/vertebra earlier in Odobenus rosmarus and Hydrurga leptonyx.

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Neural spine angle (NSA)

NSA follow the same pattern for all three modern pinniped clades and A. kernensis (Fig. 3B). The NSA are posteriorly directed in the thoracic region and become more vertically oriented in the lumbar region; however, none of the groups possess true anticlinal (i.e. anteriorly inclined) neural spines. Statistically, all three clades are very similar to each other, although phocids tend to have more posteriorly directed neural spines as compared to Odobenus in the anterior thoracic and lumbar vertebrae (Table 1). The NSA of A. kernensis are significantly more vertically oriented in the lumbar region compared to phocids; in pattern they are most similar to Odobenus in the posterior region of the vertebral column (Table 1), but appear more posteriorly directed in the anterior vertebrae (Fig. 3B).

Transverse process dorsoventral projection (TPDV)

The TPDV profiles are very similar across the three modern pinniped clades and A. kernensis. In each group the thoracic vertebrae have dorsally directed TPDV, whereas the lumbar vertebrae have ventrally deflected TPDV (Fig. 3C). Statistically there is very little difference in TPDV amongst the groups; however, phocids do tend to have less dorsally directed TPDV in the mid-thoracic region (Table 1). In pattern, A. kernensis is most similar to otariids and Odobenus in the thoracic region, but the TPDV in the lumbar region are less ventrally deflected than all modern pinniped groups, differing the most in degree from otariids (Fig 3C).

Transverse process anteroposterior projection (TPAP)

In all three modern pinniped clades and A. kernensis the TPAP project anteriorly (Fig. 3D). Again, statistically there is very little difference in TPAP amongst the groups; however, otariids tend to have statistically more anteriorly deflected TPAP in the mid-thoracic region (Table 1). In pattern, A. kernensis has the most anteriorly deflected TPAP in the mid-thoracic region, but the least anteriorly deflected TPAP in the lumbar region (Fig. 3D).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Author contributions
  10. References
  11. Supporting Information

Despite remarkable similarity in body plan, pinnipeds show clear differences in their axial anatomy which can be linked to variations in locomotory behaviour. In particular, our results have uncovered distinct linear functional profiles for each of the three modern pinniped clades and Allodesmus kernensis; however, we also have shown that there is little variation with respect to angular functional profiles. This indicates that biomechanical differences in locomotor style are to a greater extent determined by changes in the linear dimensions of the vertebrae rather than the angle of muscular/ligamentous attachments, although soft tissue differences not evident from the skeleton may still play a role (in addition to limb specialisations). Below, we discuss the functional implications of the vertebral morphometric parameters and how they may correlate with locomotory behaviour in phocids, otariids and Odobenus. Moreover, we examine which locomotor hypothesis best matches the vertebral functional profiles displayed by A. kernensis.

Functional implications of morphometrics

Centrum dimensions

The dimensions of the centra – CL, CH, CW – have a considerable impact on the degree of passive flexibility at inter-vertebral joints (Long et al. 1997); however, regional changes in the mechanics of vertebral bodies may be best discussed by examining the overall shape of the centra (e.g. Brown, 1981; Buchholtz, 1998, 2001a,b; O’Keefe & Hiller, 2006). Variation in centra shape or dimensional change along the vertebral column can be evaluated by calculating relative centrum length, which is equivalent to 2CL/(CH + CW). A constant relative centrum length along the vertebral column indicates a similar range of motion in all inter-vertebral joints, whereas a change in this dimension signifies regions of increased passive flexibility or stiffness. Long relative centrum lengths point towards more spool-shaped vertebrae and greater inter-vertebral flexibility due to reduced contact surface area and increased angular deflection between succeeding vertebrae. Short relative centrum lengths are indicative of disk-shaped vertebrae and increased inter-vertebral stiffness due to greater contact surface area and a minimal degree of deflection before adjacent vertebrae obstruct one another.

Calculating relative centrum length along the thoracolumbar region in modern pinnipeds and A. kernensis shows some interesting trends (Fig. 4). First, the vertebrae in all groups are spool-shaped (except for the first two vertebrae in Odobenus), meaning that centrum length is greater in dimension than the centrum endplate. In general, this result indicates that the thoracolumbar region in pinnipeds is adapted for increased passive inter-vertebral flexibility, unlike other secondarily aquatic tetrapods such as whales (Buchholtz, 2001b), sirenians (Buchholtz et al. 2007), ichthyosaurs (Buchholtz, 2001a) and mosasaurs (Lindgren et al. 2007), which show a tendency for disk-shaped vertebrae. Secondly, the patterns of relative centrum length in phocids and A. kernensis are roughly the mirror image of each other. Phocids show a steady increase in relative centrum length along the thoracolumbar region. This indicates that phocids likely have relatively stiff inter-vertebral joints in the anterior region of the column and more passively flexible inter-vertebral joints in the posterior region. In contrast, A. kernensis shows a decrease in relative centrum length along the column indicating potentially more flexible inter-vertebral joints in the anterior region of the column and relatively stiff inter-vertebral joints in the posterior region. Finally, in terms of the whole thoracolumbar region, otariids appear to have the greatest relative centrum length, whereas Odobenus has the shortest. As a result, otariids likely have the most passively flexible inter-vertebral joints and greatest range of movement along the length of the column compared to the other pinniped groups and Odobenus likely has the stiffest or most stable inter-vertebral joints.

image

Figure 4.  Centrum shape, as defined by relative centrum length [2CL/(CH+CW)], plotted as a percentage of thoracolumbar length. Direction of shape change is depicted on the right-hand side of the graph. The dashed line indicates the transition between the thoracic and lumbar regions; this transition takes place one step/vertebra earlier in Odobenus rosmarus and Hydrurga leptonyx.

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Vertebral processes

Vertebral process size and inclination have an important impact on the degree of muscular and ligamentous forces acting on them, and thus have a huge effect on the active (and passive, when muscles are stretched) mobility of the axial skeleton. Neural spines (NS) act as bony lever arms for the epaxial musculature, primarily for the back extensor muscles (e.g. m. spinalis); the longer the NS lever arm (or greater dorsal projection), the more powerful the extensor leverage of the muscles (Shapiro, 1995; Shapiro et al. 2005). Longer NS also indicate the presence of greater muscle mass, which in turn acts to increase the second moment of area (or cross-section) of the body, and overall passive inter-vertebral stiffness in the sagittal plane (Long et al. 1997). In pinnipeds, phocids display moderately sized NS lever arms along the length of the thoracolumbar region (Fig. 2E), which suggests that phocids can produce controlled, yet powerful extensor movements. Otariids show a decrease in NS lever arm length posteriorly such that they appear to have a very stiff anterior thoracic region and more sagittally flexible posterior thoracic and lumbar regions (Fig. 2E). Odobenus and A. kernensis also display a decrease in NS lever am length and inter-vertebral stability anteroposteriorly through the thoracic region; however, the lever arms in the lumbar region are of a similar length to phocids, implying a comparable degree of sagittal movement (Fig. 2E).

The angle of the NS from the horizontal provides a clue as to the direction the extensor musculature is acting. Slijper (1946) postulated that the orientation of the NS should be perpendicular to the most ‘important’ muscles acting on them; therefore, clear differences in the inclination of the NS would suggest a difference in the function of the vertebral column. Within this context, if mobility is more important than strength, the neural spines are cranially inclined to allow greater leverage and room for musculature, but if stability is more important, they are caudally directed (e.g. Shapiro, 1995, 2007). A caudally directed NS, when connected by a dorsal ligament, also could act as a spring by pulling a flexed vertebral column back towards the neutral position, potentially saving energy during dynamic bending movement (Videler, 1993; Pabst, 1996; Buchholtz, 2001a; Westneat & Wainwright, 2001). In all pinnipeds the NS are caudally directed (Fig. 3B), suggesting inter-vertebral stability and a general reduction in the potential for muscular leverage. Also, there does not appear to be any appreciable difference in NS angle between clades (Table 1), which implies that the epaxial musculature is oriented in the same way, irrespective of locomotory behaviour.

Transverse processes (TP) also act as bony levers for the epaxial (and other) musculature, but for movements in the dorsolateral (for muscles attaching to the dorsal aspect of the process, e.g. m. iliocostalis) and ventrolateral direction (for muscles attaching to the ventral aspect of the processes, e.g. m. quadratus lumborum) (Shapiro, 1995). In general, the longer the TP lever arm, the greater the muscular leverage but the stiffer the vertebral column becomes in the horizontal plane; again this passive stiffening is a consequence of a larger muscle mass, which increases the second moment of area (cross-section) of the body. The pattern of TP lever arm lengths is similar in all pinnipeds, with a decrease in length through the thoracic region and an increase in length in the lumbar region; however, the degree is different (Fig. 2F; Table 1). Phocids and Odobenus both have significantly longer TP lever arms than otariids along the thoracolumbar region, potentially indicating that these pinnipeds have stiffer columns but greater leverage for horizontal movements. The TP lever arms in A. kernensis appear to be shorter in the thoracic region than in the lumbar region (Fig. 2F). This pattern suggests that the thoracic region in A. kernensis is more flexible than the lumbar region but that the lumbar region has a greater propensity for active horizontal movements.

Determining the angles of the TP, both dorsoventrally and anteroposteriorly, makes it possible not only to compare the orientation of muscular attachments, but also to assess the propensity for movement (Gambaryan, 1974; Shapiro, 1995; Argot, 2003). For instance, a more ventrally oriented TP improves the mechanical advantage of the spinal flexors, increasing sagittal mobility. Furthermore, an anteriorly oriented TP improves the mechanical advantage for horizontal flexion by keeping the moment arm of the muscles large at all angles of flexion. In modern pinnipeds and A. kernensis, the pattern of TP angles is similar for each group (Table 1), being anterodorsally oriented in the thoracic region and anteroventrally oriented in the lumbar region (Figs. 3C,D). This similarity again suggests that all pinnipeds have the same orientation of epaxial muscular attachments, irrespective of locomotory behaviour. However, the change in direction also indicates that the TP in the lumbar region of pinnipeds effectively increase the mechanical advantage of the epaxial musculature for greater mobility in both the sagittal and horizontal planes. Such speculations about muscle orientations, of course, deserve direct investigation via dissection in future studies.

Zygapophyseal joints

Zygapophyseal joints control the range of movement along the vertebral column, giving an indication not only of the direction of movement, but also the degree of movement. A more acute (< 90° between prezygapophyses) prezygapophyseal angle (PZA) restricts movement to the sagittal plane and helps to resist torsional loads, whereas an obtuse PZA angle (> 90° between zygapophyses) restricts movements to the horizontal plane and helps to resist ventral shear (Slijper, 1946; Boszczyk et al. 2001; Hua, 2003). In addition, the anteroposterior projection of the zygapophyses with respect to the centrum body (i.e. the inter-zygapophyseal length, I-ZL) has been shown to be positively correlated with the degree of movement at the joint, such that a longer distance permits a greater range of motion (Jenkins, 1974). The patterns of PZA along the thoracolumbar region in all pinnipeds are virtually identical (Fig. 3A; Table 1), with movements restricted to the horizontal plane in the anterior and mid-thoracic regions and the sagittal plane in the posterior thoracic and lumbar regions. However, the I-ZL do show variation (Fig. 2G; Table 1). Odobenus displays the greatest I-ZL anteroposteriorly, indicating a potentially high degree of zygapophyseal joint mobility throughout the thoracolumbar region. Phocids, however, show a steady decrease in I-ZL posteriorly, suggesting reduced zygapophyseal joint mobility towards the lumbar region. In contrast, otariids and A. kernensis show a steady increase in I-ZL posteriorly and, in turn, an increase in zygapophyseal joint mobility towards the lumbar region (Fig. 2G).

Lamina width

It has been suggested that wide laminae increase the attachment area for the ligamenta flava – ligaments which connect the laminae of adjacent vertebrae from the axis to the sacrum – increasing passive resistance to hyperflexion (Godfrey & Jungers, 2003; Shapiro, 2007). Modern pinnipeds all show the same pattern of lamina widths along the thoracolumbar region, with a slight decrease in width anteroposteriorly; however, phocids and Odobenus have much wider laminae than otariids, suggesting a greater resistance to hyperflexion. Alternatively, A. kernensis has narrow, low-resistant otariid-like laminae in the thoracic region and wide, high-resistant phocid-like laminae in the lumbar region (Fig. 2H; Table 1).

Correlation with locomotory behaviour

Phocids

As phocids are pelvic oscillators, most of the inter-vertebral flexibility should be restricted to the posterior region of the axial skeleton and this is indeed the case. The short relative centrum lengths in the anterior region of the column would potentially create a rigid torso, which acts to anchor the more flexible posterior region, helping to generate movements of high amplitude and low wavelength just anterior to the pelvic girdle. This pattern is analogous to that seen in modern whales, where there is a decrease in relative centrum length (inter-vertebral flexibility) anterior to the fluke in order to enhance sagittal displacement of the caudal tail stock through the water (Buchholtz, 2001b). Focused pelvic oscillation in phocids is also supported by large epaxial muscles attached to long lever arms. In particular, the long transverse process lever arms provide the necessary leverage for horizontal movements of the lumbar region and this is further enhanced by more loosely fitting zygapophyses. In fact, the monk seal (Monachus monachus) has greatly reduced splint-like postzygapophyses in the lumbar region which do not contact the prezygapophyses of the succeeding vertebrae (S. E. Pierce, personal observation). This in effect eliminates the sagittal restriction of movement caused by the acutely angled prezygapophyses and counteracts the reduced mobility implied by the short inter-zyapophyseal lengths, allowing phocids to move the spine and hindflippers in the horizontal plane (Fish et al. 1988).

Otariids

The thoracolumbar region in the pectoral oscillating otariids reveals less evidence of active axial movement. As a whole, the axial skeleton is much more flexible than that of phocid seals, with long, spool-shaped centra along the column and an increase in inter-zygapophyseal length towards the lumbar region. In addition, the epaxial musculature is less well developed, especially in the posterior region of the column, with the lumbar vertebrae displaying short lever arms. This increased inter-vertebral flexibility is consistent with the high degree of agility and manoeuvrability observed during otariid swimming. In fact, the extremely pliable body permits otariids to literally bend over backwards, reaching their pelvic flippers during turning (Riedman, 1990). Bending of the spine allows the body to curve smoothly, maintaining a streamlined appearance throughout the turn and minimising deceleration during directional changes (Godfrey, 1985; Fish et al. 2003). The enhanced turning performance seen in otariids allows these seals to forage after highly elusive prey in structurally complex environments. Another notable characteristic of the otariid thoracolumbar region is the presence of long neural spine lever arms in the anterior thoracic region, which is the area of the spine suspending the scapulae. As the foreflippers are the main propulsive unit in otariids, these longer neural spines expand the area of muscular attachment for the pectoral girdle (English, 1977), potentially providing greater capacity to generate thrust and lift.

Odobenus

The modern walrus shows vertebral characteristics most similar to phocids, but with some otariid qualities, consistent with an intermediate or mixed form of aquatic locomotion. For instance, long lever arms suggest that the epaxial musculature is likely well developed around both girdles, providing the necessary leverage for both pectoral and pelvic oscillation; however, this needs to be quantified through dissection. Expanded pectoral musculature should also help to support the body on land (Gordon, 1983) and during feeding on the ocean floor (see below). However, the implied inter-vertebral stability of the thoracolumbar region in Odobenus, based on short relative centra lengths, does not appear to be consistent with pelvic oscillatory movements of the spine and thus might be a reflection of large body size and/or feeding behaviour. Odobenus is the second largest pinniped after the elephant seal and thus body mass might place constraints on the thoracolumbar region to ensure the distribution of load. Moreover, in the wild, Odobenus primarily feeds on molluscs buried beneath the ocean sediment. During foraging the animals position themselves with their front flippers on the sand and their body at an angle of 30–90° from the ocean floor; the snout and foreflippers are then used to locate the food (Kastelein & Mosterd, 1989; Levermann et al. 2003). Having a passively rigid spine might help to maintain this almost vertical position in the water column for long periods of time. Nonetheless, the seemingly stiff inter-vertebral joints of Odobenus do not appear to preclude it from performing pelvic oscillatory movements. Perhaps the long, overhanging zygapophyses allow the necessary range of movement to perform locomotory behaviours; however, this would need to be determined through mechanical testing of cadaveric material.

Allodesmus

Results from this study reveal that the thoracolumbar region of A. kernensis displays a mixture of morpho-functional characteristics. In particular, the thoracic region is highly flexible and shows evidence of long neural spine lever arms, a pattern consistent with pectoral oscillation. Conversely, the lumbar region is short and stiff, the vertebral processes display long lever arms for both sagittal and horizontal movements, and there is evidence of increased resistance to hyperflexion. All of these morpho-functional features are consistent with pelvic oscillation. Consequently, this study supports Giffin’s (1992) interpretation that A. kernensis used a combination of fore- and hindlimb movements during aquatic locomotion. Considering the limbs in A. kernensis suggest an otariid-like swimming movement (Mitchell, 1966; Bebej, 2009) and the vertebral column points towards a mixed pattern (Giffin, 1992; this study), we propose that the locomotor style of A. kernensis was most likely the opposite to that found in Odobenus, with the large foreflippers as the primary propulsive force and the smaller hindflippers and mechanically active lumber region being used secondarily to drive the animal through the water column.

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Author contributions
  10. References
  11. Supporting Information

Although often overlooked, the axial skeleton plays a key role in providing structural support and mobility during locomotion in all tetrapods, even (or particularly) in those with reduced or highly specialised limbs. Thus, when analysing the linkages between form, function and movement, one must consider the mechanical behaviour of the vertebral column. In this study, we have analysed the functional implications of regional variation in the thoracolumbar vertebrae of modern pinnipeds and the fossil taxon Allodesmus kernensis. Our results demonstrate a clear distinction in the axial column of modern pinniped clades and a strong correlation between vertebral mechanics and aquatic locomotory behaviour. From this comparative dataset and knowledge of limb morphology and neural canal anatomy, we are able to infer confidently that A. kernensis used a combination of pectoral and pelvic oscillation during swimming. As A. kernensis belongs to the Desmatophocidae, an extinct pinniped lineage considered the sister group to the Phocidae (Berta & Adam, 2001; Demere et al. 2003; Berta et al. 2006), this hypothesised mode of locomotion brings into question the sequence of evolutionary events that led to the diversification of pinniped locomotory behaviours. For example, it raises speculation about the locomotor style in other desmatophocids and ultimately the acquisition of phocid pelvic oscillation, as well as the interpretation of swimming mode in more basal pinnipedimorphs such as Enaliarctos (Berta & Adam, 2001; Bebej, 2009) and the newly discovered Puijila darwini (Rybcznski et al. 2009). However, this study also provides the necessary framework to begin to examine the evolution of axial mechanics and locomotion stages in other fossil pinnipedimorphs and their relatives in more detail, with which broader scenarios of locomotor evolution could be tested.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Author contributions
  10. References
  11. Supporting Information

For providing access to specimens in their care, we thank: M. Lowe (UMZC), R. Miguez (BMNH) and S. McLeod (LACM). For help and advice during data collection and manuscript construction we thank: D. Haine, M. Llyod, L. Hautier, K. Richards, A. Charlton, S. Turner, A. Friday and J. Molnar. For enhancing the clarity of the manuscript, we also thank two anonymous reviewers. This research was supported by NERC grant NE/G005877/1 and NE/G00711X/1.

Author contributions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Author contributions
  10. References
  11. Supporting Information

S.E.P.: Concept and design, data collection and analysis, draft of manuscript; J.R.H. and J.A.C.: critical review and approval of manuscript.

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  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Author contributions
  10. References
  11. Supporting Information
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Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. Author contributions
  10. References
  11. Supporting Information

Table S1. Raw data and specimens. T = thoracic; L = lumbar. BMNH, Natural History Museum London; LACM, Natural History Museum of Los Angeles County; UMZC, University Museum of Zoology Cambridge. Linear measurements in mm and angular measurements in degrees. (M) = male; (F) = female; (–) = unknown gender.

Table S2. PC loadings per vertebra for each measurement on PC1 and PC2. Bold indicates high loading (> 0.6) and italics indicates moderate loading (0.4 ≥ to < 0.6). T = thoracic; L = lumbar; CL = centrum length; CH = centrum height; CW = centrum width; TPLA = transverse process lever arm; NSLA = neural spine lever arm; I-ZL = inter-zygapophyseal length; LW = lamina width.

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