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Tail Architecture and Function of Cebupithecia sarmientoi a Middle Miocene Platyrrhine from La Venta Colombia.

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THE ANATOMICAL RECORD 294:2013–2023 (2011)
Tail Architecture and Function of
Cebupithecia sarmientoi, a Middle
Miocene Platyrrhine From
La Venta, Colombia
JASON M. ORGAN1,2* AND PIERRE LEMELIN3
Department of Surgery, Saint Louis University School of Medicine, St. Louis, Missouri
2
Center for Anatomical Science and Education, Saint Louis University School of Medicine,
St. Louis, Missouri
3
Division of Anatomy, Faculty of Medicine and Dentistry, University of Alberta, Edmonton,
AB, Canada T6G 2H7
1
ABSTRACT
Cebupithecia sarmientoi, an early pitheciine from the Middle Miocene
of La Venta, Colombia, preserves an almost complete caudal vertebral
sequence (18 vertebrae). Behavioral reconstructions for this taxon based
on appendicular elements suggest a locomotor profile similar to that of
Pithecia for which vertical clinging postures and leaping behavior are frequently adopted. General tail morphology suggests some similarity with
prehensile-tailed Cebus in the proximal tail region, although overwhelming similarity with nonprehensile-tailed Pithecia is evident in the distal
tail region. Indices of caudal muscle attachment sites show marked similarities to nonprehensile-tailed platyrrhines, especially Pithecia. However,
the cortices of Cebupithecia caudal vertebral bodies are thicker than those
of most other nonprehensile-tailed New World primates. Mechanically,
this would provide high resistance to bending and torsional stresses, falling within the range exhibited by prehensile-tailed monkeys. These
results suggest that Cebupithecia may have employed its tail differently
than most nonprehensile-tailed platyrrhines living today, behaviors that
possibly involved tail-bracing or twisting during hindlimb (pedal grasping) suspensory behaviors. Such behaviors may serve as a preadaptive
model for the full-fledged evolution of below-branch tail suspension and
prehensility seen in other New World primates. Anat Rec, 294:2013–2023,
C 2011 Wiley Periodicals, Inc.
2011. V
Key words: prehensile tail; caudal vertebrae; cross-sectional
geometry; section modulus; pQCT; Platyrrhini;
New World monkeys; primate evolution
INTRODUCTION
The holotype specimen of Cebupithecia sarmientoi
(UCMP 38762)—an early pitheciine from the Middle
Miocene deposits of the Villavieja Formation (Honda
Group), La Venta, Colombia (12.5 ma) (Stirton, 1951;
Stirton and Savage, 1951)—is 70% complete (Fig. 1)
and preserves a nearly complete caudal vertebral
sequence (18 vertebrae), affording the rare opportunity
to examine tail architecture and function in a fossil New
World monkey (Meldrum and Lemelin, 1991). Locomotor
reconstructions of Cebupithecia based on limb evidence
C 2011 WILEY PERIODICALS, INC.
V
Grant sponsor: National Science Foundation; Grant number:
BCS-0550676; Grant sponsors: Johns Hopkins University, Saint
Louis University.
*Correspondence to: Jason M. Organ, Center for Anatomical
Science and Education, Department of Surgery, Saint Louis
University School of Medicine, 1402 S. Grand Blvd., M306, St.
Louis, MO 63104. Fax: 314-977-5127. E-mail: jorgan1@slu.edu
Received 15 September 2011; Accepted 16 September 2011
DOI 10.1002/ar.21504
Published online 1 November 2011 in Wiley Online Library
(wileyonlinelibrary.com).
2014
ORGAN AND LEMELIN
Fig. 1. The composite postcranial skeleton of Cebupithecia sarmientoi (UMCP 38762), modified from
photo courtesy of Jeff Meldrum and John Fleagle.
2015
CEBUPITHECIA TAIL MORPHOLOGY
suggest a combination of frequent clinging postures and
leaping, similar to that observed for Pithecia (e.g., Davis,
1987; Fleagle and Meldrum, 1988; Ford, 1990; Meldrum
et al., 1990; Meldrum and Lemelin, 1991; Meldrum,
1993), but without tarsal specializations indicative of
hindlimb suspension typical of Chiropotes (Fleagle and
Meldrum, 1988; Meldrum, 1993, 1998; but see Ford,
1990). Tail anatomy shows some similarity with prehensile-tailed Cebus1 more proximally; more distally, the tail
exhibits overwhelming resemblance with nonprehensiletailed Pithecia (Meldrum and Lemelin, 1991). Ultimately, the tail of Cebupithecia was diagnosed as nonprehensile (Meldrum and Lemelin, 1991).
These inferences about tail function in Cebupithecia
are based on external dimensions without consideration
of the internal architecture of the caudal vertebrae.
Recent analysis of caudal vertebral structure among
extant platyrrhines indicates that caudal vertebrae with
relatively higher resistance to torsional and bending
moments are found in prehensile-tailed species (Organ,
2010). The cortices of the caudal vertebrae of Cebupithecia appear thicker than most other nonprehensile-tailed
platyrrhines (pers. obs.), suggesting they may be capable
of resisting higher torsional and bending stresses. In
light of the similarities to the Cebus tail in the proximal
region and the apparently thicker cortices of the caudal
vertebral bodies, the overall mechanical structure of
the Cebupithecia tail requires re-examination. More
specifically, this study tests the hypothesis that the
thicker cortices of the Cebupithecia caudal vertebrae
translate into stronger vertebrae. If the caudal vertebrae
of Cebupithecia are indeed stronger in bending and torsion than their external dimensions would predict, it
might suggest this taxon employed its tail in some form
of bracing and/or suspensory (bending) behavior.
MATERIALS AND METHODS
Sample
The caudal vertebrae of Cebupithecia were compared
with a sample of extant platyrrhines from nine genera
(four prehensile-tailed and five nonprehensile-tailed)
totaling 70 individuals (Table 1). Much of this comparative sample is described in detail in Organ (2010). In
1
The tail of Cebus has been called ‘‘semiprehensile’’ by some
authors (e.g., Napier and Napier, 1967; Emmons and Gentry, 1983)
in order to distinguish it from the more derived prehensile tail
found in atelines. Like the term ‘‘semibrachiation’’ (Napier and
Napier, 1967), ‘‘semiprehensile’’ is uninformative and misleading as
it may imply that the tail of Cebus represents an intermediate condition between a nonprehensile tail found in most primates and the
prehensile tail of atelines. Although there are clear behavioral and
morphological differences between the prehensile tails of atelines
and Cebus (Rosenberger, 1983; Rosenberger and Strier, 1989;
Lemelin, 1995; Bergeson, 1996; Organ, 2007, 2010; Organ et al.,
2009, 2011), these lines of evidence support the contention of parallel evolution of this remarkable organ (i.e., tail prehensility evolved
independently at least twice in New World primates). Moreover,
mechanical demands placed upon the musculoskeletal elements of
the ateline and Cebus tails result in strong structural similarities in
caudal vertebrae and musculature (Organ, 2007, 2010; Organ et al.,
2009), and both types of tails are capable of suspending the entire
body weight of the animal (Bergeson, 1996). Thus, in the present
mechanical analysis, the tail of Cebus is categorized and treated as
being prehensile.
TABLE 1. Comparative sample of extant
platyrrhines
Species
Ateles fusciceps (N ¼ 6)
Lagothrix lagotricha (N ¼ 8)
Alouatta palliata (N ¼ 8)
Cebus apella (N ¼ 8)
Saimiri sciureus (N ¼ 8)
Pithecia pithecia (N ¼ 7)
Pithecia monachus (N ¼ 5)
Chiropotes satanas (N ¼ 5)
Aotus trivirgatus (N ¼ 7)
Saguinus oedipus (N ¼ 7)
Body Massa (g)
Tail Type
M: 8,890
F: 9,160
M: 7,280
F: 7,020
M: 5,959
F: 4,619
M: 3,650
F: 2,520
M: 779
F: 662
M: 1,940
F: 1,580
M: 2,610
F: 2,110
M: 3,100
F: 2,960
M: 813
F: 736
M: 418
F: 404
Prehensile
Prehensile
Prehensile
Prehensile
Nonprehensile
Nonprehensile
Nonprehensile
Nonprehensile
Nonprehensile
Nonprehensile
a
All body masses taken from Smith and Jungers (1997)
except Alouatta, taken from Organ (2010).
that study, structural differences in the proximal caudal
vertebrae were found between species of Pithecia, which
may be associated with differences in tail-use behavior.
However, the morphologic differences were based on
small sample sizes for each Pithecia species. To this end,
the present analysis adds nine individuals to the previous dataset, expanding the number of Pithecia pithecia
and Pithecia monachus individuals in the sample, while
also adding individuals of Chiropotes. The inclusion of
Chiropotes in particular is important because this taxon
may spend a significant proportion of time in hindlimb
suspension with the middle section of the tail draped
over the substrate (i.e., tail-bracing) (Fleagle and Meldrum, 1988; van Roosmalen et al., 1988; Walker, 1993,
1996; Meldrum, 1998).
Mechanical Structure of the Tail
General tail morphology. The overall structural
morphology of the tail of Cebupithecia was assessed first
by recording the total number of caudal vertebrae in
each of the three regions of the tail: proximal, transitional, and distal (Fig. 2; see Organ (2010) for a complete
review of tail osteology). Caudal vertebrae from the
proximal tail region differ dramatically in morphology
from those of the transitional and distal tail regions. In
particular, these caudal vertebrae bear ventral and neural arches and a single pair of transverse processes and
articulate with one another by zygapophyseal and intervertebral disc joints (in a fashion similar to lumbar vertebrae). Caudal vertebrae from transitional and distal
tail regions are distinct from proximal ones by possessing two pair of transverse processes and only intervertebral disc articulations. Differences in intervertebral
articular morphology contribute to differences in tail
movements and flexibility. In short, movements of the
proximal region of the tail are primarily limited to flexion-extension in a sagittal plane with more limited
movements in other planes (Organ, 2010; see also Wada
2016
ORGAN AND LEMELIN
Fig. 2. Schematic representations of the primate tail, showing distinctions between the prehensile tail of an ateline (A); prehensile tail of Cebus
(B); and, a nonprehensile-tailed platyrhrine (C). Blue, proximal region;
green, transitional region; tan, distal region; TV, transition vertebra; LV, longest caudal vertebra; MDV, mid-distal vertebra. See text for description of
TV, LV, and MDV. (Reproduced with permission from Organ et al., 2009).
et al., 1993), while the planes of motion between the
transitional and distal region vertebrae are more varied.
Prehensile-tailed platyrrhines tend to have longer proximal tail regions with more numerous vertebral elements
than nonprehensile-tailed platyrrhines (Ankel, 1962,
1972; German, 1982; Schmitt et al., 2005; Organ, 2010),
which increases movement and flexibility of the proximal tail region (i.e., more zygapophyseal joints in series;
see Ward, 1991, 1993; Shapiro, 1993, 1995).
Once the relative number of vertebrae in each tail section was compiled, a single vertebra from each region
was chosen for external dimensional (process expansion
indices) and internal architectural (cross-sectional geometry) analyses: transition vertebra (TV) from the proximal
region, longest caudal vertebra (LV) from the transitional
region, and mid-distal vertebra (MDV) from the distal
region of the tail. These vertebrae represent functionally
analogous points within each tail that can be compared
across taxa (Organ et al., 2009; Organ, 2010). These vertebrae were chosen because they likely experience different mechanical loads in prehensile and nonprehensile
activities. The TV was chosen because it represents the
vertebral element where possible movements of the tail
change from being oriented primarily in flexion/extension
in a sagittal plane to being more multidirectional (including flexion, extension, and axial rotation) (Organ, 2010;
see also Wada et al., 1993). The LV is the longest vertebra
in the caudal sequence and, therefore, is likely to experience higher bending moments than other caudal vertebrae; the MDV is located in the area where tail-wrapping
around a substrate most likely occurs in most prehensiletailed platyrrhines (Organ, 2010).
vertebrae in the distal region of the tail. If the total number of vertebrae is unknown, the placement of the MDV
is less certain. Therefore, to analyze the structure of the
MDV in Cebupithecia, it was necessary to estimate the
total number of caudal vertebrae that would have been
present in the living individual. Three reconstructions of
total caudal vertebral number were used in this analysis.
First, the tail of Cebupithecia was reconstructed to
include 25 total caudal vertebrae, the purported primitive
condition for primates (Schultz and Straus, 1945; Stirton,
1951). Next, because of its numerous postcranial similarities to Pithecia, the tail of Cebupithecia was reconstructed to a total of 23 caudal vertebrae, representing
the average number of vertebrae in Pithecia (Organ,
2010). Finally, a prehensile tail model of 27 total caudal
vertebrae was used, as it represents the average number
of caudal vertebrae among all ateline and Cebus individuals in the sample (Organ, 2010).
It is important, again, to note that only the distalmost vertebrae are missing from the Cebupithecia material. Therefore, choice of reconstruction method did not
affect the position of the morphologically defined TV and
LV. Only the location of the MDV was affected by the
choice of reconstruction method, and even then, only by
a small margin.
Cebupithecia Tail Reconstruction Methods
The initial descriptions of the Cebupithecia axial skeleton identified 17 caudal vertebrae (Stirton, 1951; Stirton and Savage, 1951). A full analysis of the axial
skeleton conducted by Meldrum and Lemelin (1991)
identified an additional caudal vertebra, bringing the
number to 18. However, the total number of caudal vertebrae for this taxon is still unknown, as the distal-most
elements were not recovered.
Missing distal elements of the tail does not present
challenges to analyzing the TV and LV, as they are morphologically defined based on articular morphology and
length. However, the placement of the MDV within the
vertebral sequence is determined by the total number of
Indices of Caudal Muscle Attachments
Caudal musculature of platyrrhine prehensile tails is
more robust than that of nonprehensile tails, particularly
in the ventral (flexor) and lateral muscle compartments
(Lemelin, 1995; Organ et al., 2009). Therefore, previous
morphometric analyses of the external geometry of caudal
vertebrae focused on the relative expansion of muscle
attachment sites (especially transverse processes) as a
generally successful means of discriminating between prehensile and nonprehensile vertebrae (German, 1982; Meldrum and Lemelin, 1991; Youlatos, 2003; Schmitt et al.,
2005; Organ, 2010). Transverse processes serve as the
sites of origin and insertion of mm. intertransversarii caudae, the prime lateral flexors and rotators of the tail (Dor,
1937; Lemelin, 1995; Organ et al., 2009; Organ, 2010), as
well as the fleshy origins (in the proximal tail) of mm.
flexor caudae longus et brevis, the primary flexors of the
tail. An index of relative transverse process expansion
was calculated to reflect the moment arm of lateral flexion of mm. intertransversarii caudae and the robustness
of mm. flexor caudae longus et brevis (Organ, 2010).
CEBUPITHECIA TAIL MORPHOLOGY
The distal (tendinous) attachment site for mm. flexor
caudae longus et brevis on the hemal arch (which articulates with the hemal process on the proximoventral aspect of the caudal vertebra) is not shared with other
muscles. The relative expansion of the hemal process
discriminates prehensile from nonprehensile vertebrae
better than indices of transverse process expansion, in
part because transverse processes are inherently tied to
muscle belly size in addition to mechanical advantage
(Organ, 2010). Therefore, an index of hemal process
expansion was also calculated to reflect the dorsoventral
bending moment arm of mm. flexor caudae longus et brevis, without the potentially confounding influence of
muscle size (Organ, 2010).
Three linear measurements of the TV, LV, and MDV
were collected with Mitutoyo 15-cm sliding digital calipers (Mitutoyo Corp. USA, Aurora, IL) to the nearest 0.1
mm (Organ, 2010):
a. Craniocaudal length (CCL): maximum craniocaudal length of the vertebra, measured in lateral
view.
b. Proximal transverse process breadth (PTPB): maximum breadth of the proximal transverse process,
measured in superior view.
c. Hemal process height (HPH): maximum height of
the hemal process, measured from proximal transverse process to hemal process, in proximal view.
These measurements were used to calculate transverse process expansion (TPE) and hemal process expansion (HPE) indices, following Organ (2010):
a. TPE ¼ PTPB/CCL 100
b. HPE ¼ HPH/CCL 100
Cross-Sectional Geometric Methods
All cross-sectional properties of caudal vertebrae exhibit similar patterns of variation across taxa (e.g.,
cross-sectional areas, second moments of area, section
moduli) (Organ, 2007; Organ and Lemelin, 2009). This
study focuses on the polar section modulus (Zp)—a
direct measure of torsional strength and a proximate
measure of (twice) average bending strength (Ruff, 2002;
Organ, 2010)—because previous studies suggest it is the
most appropriate singular measure of overall mechanical
strength of a bony element (Ruff, 2002; Organ, 2010).
Cross-sectional images of the TV, LV, and MDV of 61
individual monkeys were obtained at 50% of vertebral
craniocaudal length with a Norland-Stratec XCT
Research SAþ peripheral quantitative computed tomography (pQCT) scanner (Stratec Medizintechnik GmbH,
Pforzheim, Germany) using the following parameters:
pixel size ¼ 0.1 mm2, slice thickness ¼ 1 mm, scan speed
¼ 3 mm/sec. Polar section moduli were calculated from
pQCT scans using native scanner software (XCT software 5.40), with a density threshold of 500 mg/cm3 to
isolate cortical from cancellous bone and an internal
software algorithm designed to segment bone types
(described in detail in Organ, 2010).
The Ellipse Model Method (EMM) of reconstructing
cross-sectional geometry with biplanar radiographs
(Ohman, 1993; Runestad et al., 1993; Lazenby, 1997,
2017
Fig. 3. Diagrams of measurements used to reconstruct vertebral
cross-sectional properties using the Ellipse Model Method (EMM).
Total subperiosteal and medullary breadths were measured from anteroposterior and mediolateral projection radiographs and used to calculate section properties using formulae found in the text. Only the AP
projection is illustrated here.
1998; O’Neill and Ruff, 2004) was used instead of pQCT
to estimate the polar section modulus of the caudal vertebrae of Cebupithecia and the nine pitheciine individuals added to the comparative dataset. In brief, this
method uses cortical thickness of the vertebrae measured from orthogonal radiographs (posteroanterior and
lateral projections) to geometrically derive cross-sectional geometric properties for a hollow ellipse using
standard equations (Fig. 3) (O’Neill and Ruff, 2004):
a. Second moment of area about mediolateral axis:
Ix ¼ p/64[(AP3ML) – (ap3ml)].
b. Second moment of area about anteroposterior
axis: Iy ¼ p/64[(APML3) – (apml3)].
c. Polar second moment of area: J ¼ Ix þ Iy.
d. Polar section modulus: Zp ¼ J/(average diameter/
2).
Biplanar radiographs of the nine specimens of Pithecia
and Chiropotes were captured at the Field Museum of
Natural History (Chicago, IL) with a Philips Electronic
Instruments, Radifluor 120 (TORR X-Ray Corp., East
Sussex, UK) x-ray source onto Kodak MX125 Ready
Pack Film using a voltage of 50 kV and a current of 3.0
mA. The caudal vertebrae of Cebupithecia were radiographed with a Thermo Scientific Kevex PXS5-724EA
MicroFocus (Thermo Fisher Scientific, Inc., Waltham,
MA) portable x-ray source mounted above a PaxScan
4030 (Varian Medical Systems, Palo Alto, CA) amorphous-silicon digital imaging panel at the Division of
Fishes, National Museum of Natural History, Smithsonian Institution (Washington, DC) using a voltage of 68
kV and a current of 0.098 mA.
One disadvantage of EMM in reconstructing cross-sectional geometry is it tends to overestimate section properties compared with other noninvasive methods (O’Neill
and Ruff, 2004). Therefore, in order to compare data collected with pQCT and EMM, a small subset (N ¼ 17) of
the pQCT-scanned vertebrae was also examined using
EMM in order to validate the pooling of data collected
with different methods.
2018
ORGAN AND LEMELIN
Fig. 4. Contributions from each tail region as a percentage (%) of total tail length in extant platyrrhines
and in Cebupithecia sarmientoi. The values for Cebupithecia are based on two reconstruction models of
total vertebral number: (A) primitive reconstruction model of 25 total caudal vertebrae and (B) Pithecia
reconstruction model of 23 total caudal vertebrae.
Comparison of Cebupithecia to Extant Sample
Caudal Muscle Development Indices
Statistical evaluation of caudal vertebral metrics for
61 individuals of the extant sample are presented in
detail elsewhere (Organ, 2010). The additional specimens of extant piithecines included in this study do not
change the overall patterns of species distributions or
conclusions of the earlier analysis. Thus, because the
purpose of the present study is to evaluate the Cebupithecia tail against the backdrop of the extant sample,
this study does not rehash the statistical particulars of
the Organ (2010) study. Instead, data for Cebupithecia
caudal vertebrae are presented in the context of the
extant data previously analyzed.
Indices for three caudal vertebrae (TV, LV, and MDV)
that can be used as proxies for caudal muscle development are presented in Figure 5. As previously reported
(German, 1982; Youlatos, 2003; Organ, 2010), prehensiletailed taxa have generally more expanded transverse and
hemal processes than nonprehensile-tailed taxa, with the
differences becoming more drastic further distally within
the vertebral sequence. Hemal process expansion of the
TV, LV, and the three reconstructions of the MDV of
Cebupithecia all fall within the nonprehensile tail range
(Fig. 5a–c). Relative transverse process expansion also
places Cebupithecia within the nonprehensile tail range
for the LV and MDVs (Fig. 5d–e). In particular, Cebupithecia consistently resembles Pithecia in terms of relative
expansion of transverse and hemal processes, and does
not have muscle development indices anywhere near the
ranges of prehensile-tailed species (Fig. 5).
RESULTS
General Tail Morphology
Relative lengths of the three regions of the Cebupithecia
tail are presented in Figure 4 based on two reconstructions of total vertebral number: primitive model of 25 caudal vertebrae (Fig. 4a) and a Pithecia model of 23 caudal
vertebrae (Fig. 4b). In general, prehensile-tailed taxa
tend to have a longer proximal region of the tail. As the
reconstructed total number of caudal vertebrae for Cebupithecia increases (i.e., from 23 to 25), the relative length
of the proximal region of the specimen decreases. In both
reconstructions, the proximal region of the tail is relatively short, as in nonprehensile-tailed taxa. However, the
reconstruction of the Cebupithecia tail based on a Pithecia
model shows a proximal tail region that is relatively longer than nonprehensile-tailed Saimiri, and encroaching
on the relative length seen in prehensile-tailed Cebus.
Cross-Sectional Geometry of Caudal Vertebrae
The natural logarithms (ln) of polar section moduli
derived from pQCT were compared with those derived
from EMM using the least-squares regression method.
The regression coefficient was compared to an isometric
slope of 1.0 using a student’s t-test (Zar, 2010). Data
from both methods are highly correlated (r ¼ 0.99) and
the relationship is positively allometric (y ¼ 1.11 þ
0.05, p[isometry]<0.05), but with an intercept not different from zero (P[intercept]>0.05) (Fig. 6). Because of the
high correlation between measures, data were pooled for
the complete analysis, even though the relationship
CEBUPITHECIA TAIL MORPHOLOGY
2019
Fig. 5. Notched box plots of caudal muscle attachment indices for
the transition vertebra (TV), longest caudal vertebra (LV), and mid-distal vertebra (MDV). The middle horizontal waist of the box represents
the median, the outer horizontal limits of the boxes are the hinges
encompassing the interquartile range, and the whiskers represent all
other data points except outliers more than 1.5 times the interquartile
range. Notches extending out from the median represent 95% confidence intervals around the median (McGill et al., 1978). Hemal process expansion index (A–C) and transverse process expansion index
(D, E). Red boxes, prehensile-tailed taxa; blue boxes, nonprehensiletailed taxa. Cebupithecia is indicated by a single solid line for TV and
LV indices, and by three solid lines for MDV indices: Pithecia reconstruction model of 23 caudal vertebrae (top line); primitive reconstruction model of 25 caudal vertebrae (middle line); prehensile-tailed
monkey reconstruction model of 27 caudal vertebrae (bottom line).
Cp, Cebupithecia; At, Ateles; Lg, Lagothrix; Al, Alouatta; Cb, Cebus;
Sm, Saimiri; Pp, Pithecia pithecia; Pm, Pithecia monachus; Ch, Chiropotes; Ao, Aotus; Sg, Saguinus.
between variables is positively allometric. The intercept
of the regression equation is not different from zero,
meaning no correction factors are needed to correct overestimated EMM-derived section moduli to their pQCTderived equivalence. However, the positively allometric
relationship of the variables does imply an overestimation of polar section modulus in EMM-derived data compared to pQCT-derived data at the higher end of the
body size range for the sample, and an underestimation
of polar section modulus at the lower end of the size
range. This is not problematic for the present analysis
because the EMM-derived data included are for animals
in the middle and lower end of the body size range.
Therefore, it is possible that the EMM-derived data
obtained for Cebupithecia (2.2 kg, Fleagle, 1999) represent a ‘‘minimum’’ polar section modulus, and results
should be interpreted in this context.
Figure 7 illustrates size-adjusted polar section moduli
for three caudal vertebrae (TV, LV, and MDV) of the
extant platyrrhine sample and Cebupithecia. All three
caudal vertebrae are relatively stronger in torsion and
bending in prehensile-tailed platyrrhines compared to
most other taxa (Fig. 7a–c). The tails of Cebupithecia
and Pithecia monachus have stronger TV and LV compared with all other nonprehensile-tailed taxa, with
cross-sectional property values of these two caudal vertebrae falling within the range of Cebus (Fig. 7a–b).
Depending on which reconstruction of total vertebral
number is used for Cebupithecia, the strength of the
MDV varies, however. If 23 caudal vertebrae are used
to reconstruct the tail of Cebupithecia, the MDV
appears as strong as that of Cebus (Fig. 7c, top line).
With 25 caudal vertebrae, MDV strength of Cebupithecia falls between prehensile- and nonprehensile-tailed
taxa (Fig. 7c, middle line); at 27 caudal vertebrae,
MDV strength falls within the range of all nonprehensile-tailed platyrrhines, including both species of Pithecia (Fig. 7c, bottom line). It should be pointed out that
2020
ORGAN AND LEMELIN
unlike the TV and LV, cross-sectional properties of the
MDV of P. monachus do not differ from those of Pithecia pithecia (Fig. 7c).
DISCUSSION
Fig. 6. Bivariate plot comparing natural logarithms of polar section modulus measurements of 17 individuals (open circles) from the
sample obtained through peripheral quantitative computed tomography (pQCT) and the Ellipse Model Method (EMM). Data are highly
correlated (r ¼ 0.99) and the relationship between variables is positively allometric (y ¼ 1.11 þ 0.05, P[isometry]<0.05), but with an
intercept not different from zero (P[intercept]>0.05). See text for
more detail.
Reconstructions of the positional behavior of Cebupithecia sarmientoi (UMCP 38762) include a significant
amount of clinging postures and leaping behavior (Davis,
1987; Fleagle and Meldrum, 1988; Meldrum and Fleagle,
1988; Ford, 1990; Meldrum and Lemelin, 1991; Meldrum, 1993). The degree of hindlimb suspension
employed by Cebupithecia is equivocal, however, as some
researchers pointed out the absence of anatomical correlates of such behavior in the foot (e.g., Fleagle and Meldrum, 1988; Meldrum and Lemelin, 1991; Meldrum,
1993), while others have stressed morphological aspects
of the hindlimb consistent with suspensory and climbing
behaviors (e.g., Davis, 1987; Ford, 1990). Yet, nearly all
studies have agreed that Cebupithecia relied heavily on
vertical and nonhorizontal supports.
Previous analyses of the external morphology of the
caudal vertebrae of Cebupithecia indicated a distinct resemblance to Cebus in the proximal region of the tail,
and marked similarities to Pithecia in more distal region
of the tail (Meldrum and Lemelin, 1991). The previous
work by Meldrum and Lemelin (1991) also noted the
stronger resemblance of Cebupithecia in many aspects of
the axial skeleton (including caudal vertebral morphology) to Pithecia monachus over Pithecia pithecia. The
data reported here confirm that the caudal vertebrae of
Cebupithecia resemble those found in the nonprehensile
tail of Pithecia to the greatest degree, with closer resemblance to P. pithecia rather than P. monachus in terms
of caudal muscle development.
Novel analysis of the internal morphology of the Cebupithecia caudal vertebrae presented here also suggests distinct similarities to Cebus in the proximal (and
transitional) tail region. As predicted, the thicker cortices
of the caudal vertebrae of Cebupithecia translate to
increased resistance to bending and torsion at the locations
Fig. 7. Notched box plots of size-adjusted torsional strength of the
transition vertebra (TV), longest caudal vertebra (LV), and mid-distal
vertebra (MDV). The middle horizontal waist of the box represents the
median, the outer horizontal limits of the boxes are the hinges encompassing the interquartile range, and the whiskers represent all other
data points except outliers more than 1.5 times the interquartile range.
Notches extending out from the median represent 95% confidence
intervals around the median (McGill et al., 1978). Red boxes, prehen-
sile-tailed taxa; blue boxes, nonprehensile-tailed taxa. Cebupithecia is
indicated by a single solid line for TV and LV indices, and by three
solid lines for MDV indices: Pithecia reconstruction model of 23 caudal
vertebrae (top line), primitive reconstruction model of 25 caudal vertebrae (middle line), prehensile-tailed monkey reconstruction model of
27 caudal vertebrae (bottom line). Cp, Cebupithecia; At, Ateles; Lg,
Lagothrix; Al, Alouatta; Cb, Cebus; Sm, Saimiri; Pp, Pithecia pithecia;
Pm, Pithecia monachus; Ch, Chiropotes; Ao, Aotus; Sg, Saguinus.
CEBUPITHECIA TAIL MORPHOLOGY
of the transition vertebra (proximal tail region) and longest
caudal vertebra (transitional tail region). The transition
and longest caudal vertebrae of P. monachus are stronger
in torsion and bending than those of P. pithecia (Organ,
2010, and confirmed here). As a matter of fact, the section
moduli of the caudal vertebrae of P. monachus and Cebupithecia fall within the range of those of Cebus (Fig. 7a–b).
Depending on the tail reconstruction model used, the
caudal vertebra of Cebupithecia at mid-point of the distal tail region is either: (1) as strong as that of the prehensile-tailed Cebus (23 caudal vertebrae model); (2)
intermediate in strength between that of prehensile and
nonprehensile-tailed platyrrhines (25 caudal vertebrae
model); (3) similar in strength to that of nonprehensiletailed taxa (27 caudal vertebrae model) (Fig. 7c). Thus,
the internal architecture of the TV, LV, and MDV caudal
vertebrae of Cebupithecia suggests functional adaptation
to elevated stress levels that may be related to positional
behaviors.
Analyses of the postcranial elements of Cebupithecia
aligned this fossil platyrrhine most closely with Pithecia
(Davis, 1987; Ford, 1990; Fleagle and Meldrum, 1988;
Meldrum and Lemelin, 1991; Meldrum, 1993), emphasizing the marked adaptation for powerful leaping typical
of pitheciines (Pithecia and Chiropotes). However, as
Ford (1990: 170) pointed out: ‘‘the particular mix of anatomical features seen in Cebupithecia is unlike that
found in any living platyrrhine.’’ The data presented in
this study show that the increased cortical thickness of
the caudal vertebral bodies of Cebupithecia translates
into higher section moduli (i.e., higher torsional and
bending strength) compared to extant pitheciines. The
relatively thickened cortices of the caudal vertebrae
(which do not characterize the limb bones) suggest that
the tail of this fossil pitheciine may have been used differently than that of Pithecia. Instead, Cebupithecia
may have used its tail as a brace on nonhorizontal substrates during hindlimb suspensory behavior, in a manner similar to that observed in Chiropotes. This
hypothesis can only be tested further directly with recovery of additional caudal vertebral material.
Platyrrhine Tail Evolution
A growing body of evidence suggests that the prehensile tail evolved twice in parallel among platyrrhine primates: once among the atelines (Ateles, Lagothrix,
Brachyteles, and Alouatta) and once within the genus
Cebus (Rosenberger, 1983; Rosenberger and Strier, 1989;
Lemelin, 1995; Organ, 2007, 2010; Organ et al., 2009,
2011). Differences in tail-use behavior and morphology
are the primary lines of evidence of this parallel evolution. During feeding, atelines regularly use tail suspension (with or without assistance from the hindlimbs),
while Cebus primarily uses its tail to form a tripod with
its hindlimbs (Bergeson, 1996; Garber and Rehg, 1999;
Garber, 2011). During suspensory locomotion, Lagothrix
and Ateles show extensive use of the prehensile tail,
which is best characterized as a ‘‘fifth limb’’ (Jenkins
et al., 1978; Turnquist et al., 1999; Schmitt et al., 2005).
These behavioral differences likely account for a number
of morphological differences between ateline and Cebus
prehensile tails (Organ, 2010). Atelines have relatively
longer tails than Cebus (Rosenberger, 1983; Organ,
2007; Garber, 2011), which account for a higher percent-
2021
age of total body mass (Grand, 1977). At its distal end,
the tail of atelines has much greater flexor muscle mass
relative to the extensors compared with Cebus and especially nonprehensile-tailed platyrrhines (Grand, 1977;
Lemelin, 1995). And finally, the ateline prehensile tail
possesses a glabrous friction pad on the ventrodistal surface of the tail with abundant mechanoreceptors sensitive to touch (Hill, 1962; Organ et al., 2011). The Cebus
prehensile tail is completely covered in hair, and does
not experience the same degree of tactile sensitivity
(Organ et al., 2011).
Hypothesized proximate causes to the evolution of platyrrhine prehensile tails have included accommodation
of larger body sizes in the forest canopy (e.g., Napier
and Napier, 1967; Grand, 1972, 1977), assistance in feeding behaviors (e.g., Mittermeier and Fleagle, 1976;
Grand, 1972, 1984; Cant, 1986; Rosenberger, 1992; Bergeson, 1996, 1998), or response to mechanically compliant substrates in the forest canopy (Emmons and
Gentry, 1983; Organ, 2010). Many of these proximate
causes are also compatible with the tail-bracing behavior
seen among pitheciines. There is compelling evidence
that Chiropotes engages in tail-bracing during hindlimb
suspension (Fleagle and Meldrum, 1988; van Roosmalen
et al., 1988; Walker, 1993, 1996; Meldrum, 1998). If such
behavior is also present in Pithecia monachus (see
Organ, 2010), then it may explain some of the stronger
caudal vertebrae (transition and longest) of this species
compared with Pithecia pithecia. By the same token,
similarities in cross-sectional properties of the caudal
vertebrae between P. monachus and Cebupithecia suggest that tail-bracing behavior may be primitive for the
pitheciine clade, with an ensuing loss in P. pithecia.
The distribution of tail-bracing behaviors within the
pitheciine clade is of interest in light of the hypothesis
that this behavior may have been transitional from nonprehensile to ateline prehensile tails (Meldrum, 1998).
In particular, Meldrum (1998: 151) argues ‘‘that hindlimb suspension, assisted by tail-bracing and/or twining,
served as a transitional positional behavior in the evolution of the highly derived platyrrhine [ateline] prehensile tail.’’ Hindlimb suspensory behaviors are employed
by a large number of primate and nonprimate mammals,
and some of the skeletal correlates of these behaviors
are well-established. In particular, mammals that suspend from their hindlimbs often have tarsal morphology
indicative of enhanced plantarflexion and supination of
the hindfoot, which together enable hindfoot reversal
and/or hindlimb suspension (e.g., Jenkins and McClearn,
1984; Fleagle and Meldrum, 1988; Meldrum et al.,
1997). It is important to point out that such specializations of the hindfoot are not present in Cebupithecia
(Fleagle and Meldrum, 1988; Meldrum, 1993, 1998; but
see Ford, 1990). Therefore, the tail-bracing behavior of
Cebupithecia was probably different from that observed
in Chiropotes in the sense that it was rarely or never
used in the context of hindlimb suspension. The present
analysis does not bring evidence to support or disprove
the hypothesis that hindlimb suspension with assistance
of the tail was a transitional behavior for the evolution
of ateline prehensile tails. However, the presence of possible tail-bracing behavior in an early pitheciine is an
important step toward understanding the evolution of
tail-use behaviors in extant pitheciines—including Chiropotes and possibly Pithecia monachus.
2022
ORGAN AND LEMELIN
ACKNOWLEDGEMENTS
The authors thank A. Rosenberger for inviting them
to contribute to this special issue on evolutionary morphology of the New World monkeys, and to L. Halenar
for comments that significantly improved this manuscript. They are grateful to P. Holroyd at the University
of California Museum of Paleontology for access to the
Cebupithecia specimen. For access to extant comparative
material, they thank: R. Thorington, J. Mead, L. Gordon, and J. Jacobs of the Smithsonian National Museum
of Natural History; R. MacPhee and E. Westwig of the
American Museum of Natural History; R. Martin, W.
Stanley, and T. Damitz of the Field Museum of Natural
History; and K. Glander of Duke University. Finally,
they thank M. Teaford and C. Ruff for access to research
equipment, and K. Rose, A. Taylor and R. German for
early discussions of this work. Dedicated to M.E. Organ.
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