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2Morphology and evolution of the
spider monkey, genus Ateles
ALFRED L.ROSENBERGER,LAUREN HALENAR,
SIOBH ´
A N B .COOKE AND WALTER C.HARTWIG
Introduction
Spider monkeys cast a distinct morphological silhouette – long scrawny arms
and a snaky prehensile tail arching from a narrow pot-belly torso, topped by
a small round head and blunt face. The commitment of this relatively large-
bodied platyrrhine to a large-tree, upper canopy milieu and to ripe fruit foraging
is seen throughout its skeletal and craniodental morphology. Spider monkeys
are the signature New World suspensory-postured brachiators. Bodily, they
are the closest thing to a gibbon that has evolved anywhere else within the
Order Primates. Less obvious may be the fact that they are also gibbonesque
craniodentally. But in the context of the adaptive array of Latin America’s four
ateline genera, Alouatta,Lagothrix,Brachyteles and Ateles, spider monkeys
are not simply the polar end of an adaptive morphocline, standing opposite
howlers or even opposite Lagothrix if we draw our comparison more narrowly,
to encompass only atelins. Spider monkeys are different by far. For example,
as close as Brachyteles is to the visage of a spider monkey with its ungainly
limbs and shortness of face, it does not match Ateles in the high-energy lifestyle
that goes along with eating quickly metabolized fruit and little else. Nor can
Brachyteles deftly fly and lope through the trees as if gravity and substrate
did not matter and hands, feet and tail were octopus tentacles. How ironic
that Geoffroy Saint-Hilaire was so impressed with the spider monkey’s lone
anatomical “deficiency,” its missing thumb, that in 1806 he named the genus
Ateles, meaning imperfect.
General morphology
Spider monkeys are built to roam for ripe fruit in the upper canopy of a stratified
tropical rain forest. Their lithe skeleton is designed to suspend and hurl their
Spider Monkeys: Behavior, Ecology and Evolution of the Genus Ateles ed. Christina J. Campbell
Published by Cambridge University Press. C!Cambridge University Press 2008
19
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20 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
Figure 2.1 Ateles skeleton (Encyclopedia Britannica, 1893).
body weight, rather than strut it against gravity quadrupedally (Figure 2.1).
When dealing with the minimally resistant pulp of a choice fruit, spider monkey
anatomy abides as well – in the form of an impressive incisor battery and
undistinguished, open-basin molar occlusal surfaces. Additionally,their energy-
rich diet allows the spider monkey anatomy to afford modestly enlarged brains.
Historically, spider monkey anatomy, in the context of its membership in
the ateline group, has been compared most frequently and favorably to that
of hominoids (Erikson, 1963; Rosenberger and Strier, 1989). A more pointed
comparison might emphasize resemblances with gibbons, but less empirical
work has been done to examine that aspect. Field, museum and genetics studies
have progressed from broad inter generic surveys to focused and single ques-
tion, intra specific projects (e.g. Norconk et al., 1996). These investigations
have expanded our sense of the uniqueness of Ateles and challenged long-held
phylogenetic interpretations (Jones, 2004; Hartwig, 2005), but they have not
altered the fundamental ecomorphological depiction of Ateles as a ripe-fruit
driven, upper canopy suspensory brachiator.
Body size and sexual dimorphism
It has been difficult to develop a clear, consistent assessment of body size and
sexual dimorphism in Ateles. Some studies of male and female body weight in
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Morphology and evolution 21
Table 2.1 Body weight and sexual dimorphism in Ateles
Species Dimorphism index Male weight (g) Female weight (g)
A. belzebuth 1.052 8532 8112
A. fusciceps 1.010 8890 8800
A. geoffroyi 1.101 8210 7456
A. paniscus 0.853 7460 8750
Dimorphism index =male weight/female weight
Sources: Ford (1994); Ford and Davis (1992).
the various species conclude that this genus is most often monomorphic, with
one species, A. paniscus, showing negative sexual dimorphism in which the
females are actually larger than the males (see Table 2.1; Ford and Davis, 1992;
Ford, 1994). The most recent survey by Di Fiore and Campbell (2007) obtained
similar results using a sample restricted to free-ranging individuals. Their mean
values were comparable to those of Ford and Davis (1992) for all species except
A. paniscus. Di Fiore and Campbell (2007) also summarized published assess-
ments, noting that Smith and Jungers (1997) provided a dimorphism index of
1.08 for A. paniscus as compared with the 0.853 value reported by Ford and
Davis (1992). The discrepancy represents the difference between categorizing
A. paniscus as monomorphic or negatively dimorphic. For comparison with the
other ateline primates, the dimorphism indices given by Di Fiore and Campbell
(2007) for Alouatta ranged from 1.2 (A. seniculus) to 1.76 (A. pigra); Brachyte-
les ranged from 1.13 to 1.2; and Lagothrix from 1.24 to 1.57. When these data
are taken into consideration, Ateles is the closest genus to being monomorphic
among the atelines, but it must be noted that comparable data on a variety of
other atelin species or populations is not really available.
Cranial morphology
The Ateles cranium has a gracile build, characterized by large rounded orbits, a
globular braincase, a narrow face ending in a fairly prominent but narrow snout,
and a shallow mandible (Figure 2.2). This pattern, especially in the shape of the
face, makes spider monkeys easily recognizable and quite distinct from other
ateline genera. Alouatta skulls have a relatively large uptilted face and relatively
small braincase, a lower jaw in which the angle of the mandible is deep and
flared posteriorly, and a tall ramus. Lagothrix and Brachyteles skulls share more
general resemblances. They have moderately large, broad faces and braincases
that are less rounded in shape than in Ateles. The mandible of Lagothrix is
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22 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
Figure 2.2 Ateles paniscus skull. (From Hershkovitz, 1977.)
moderately developed and not very deep and Brachyteles has a lower jaw that
is inflated postero-inferiorly and carries a ramus that is also quite tall.
In terms of overall size, spider monkey crania show no obvious sexual
dimorphism (Masterson and Hartwig, 1998), but there is evidence of differ-
ences in growth patterns between males and females. According to Corner and
Richtsmeier (1993), in their study of Ateles geoffroyi, females in the oldest
subadult age groups appeared to be larger because of an earlier onset of matu-
rity. Schultz (1960) also pointed out that even though the male and female crania
were of similar overall size in his study sample, the sexes differed somewhat
in specific cranial dimensions, including having a shorter postcanine length,
longer facial breadth and taller facial height in males than females.
The overall shape of the Ateles skull is strongly influenced by regional growth
patterns and the packaging requirements of the face and braincase, especially
compared with other atelines (Hartwig, 1993). Inside the globular neurocranium
of Ateles is a brain typically over 100 grams (Armstrong and Shea, 1997). When
compared with body size, the brain is slightly above regression lines based
on other genera (Hartwig, 1993, 1996). In general, dimensions of the spider
monkey facial skeleton scale with other relatively “unspecialized’ New World
monkey genera, but as the neurocranium becomes more globular and frontally
disposed, the facial skeleton develops more orthognathically. Ateles crania thus
display the relatively frontated orbital alignment and facial recession typical of
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Morphology and evolution 23
small-snouted, orthognathic primates, with the emphasis here on relative within
New World monkeys (Hartwig, 1993).
The external morphology of the Ateles brain has been studied, with special
attention given to features related to innervating the prehensile tail. Hershkovitz
(1970, 1977) provides comparative schematic figures of the cerebral cortex and
volumetric measurements. The regions of the brain that have both sensory and
motor control of tail function are larger in Ateles than in other species, reflecting
the remarkably sensitive, flexible prehensile tail (see below) and altering the
spatial arrangement of sulci and gyri of the brain’s lateral surface. This special-
ization also leads to more direct and efficient nerve endings in the lower levels
of the spinal cord itself that are related to tail function (Armstrong and Shea,
1997).
The cranial anatomy of Ateles is also notable for what it does not display. The
narrow facial skeleton is relatively shallow, gracile and unremarkable, in keep-
ing with the general expectations of a highly frugivorous taxon. The braincase
is also relatively simple in design, rounded as might be expected in a mod-
estly encephalized form and lacking marked temporal and nuchal lines, crests,
or rugosities on the outer table. This simplistic picture is not meant, however,
to imply that the Ateles head is also primitive in design. To the contrary –
it combines a variety of traits not expected in the ancestral morphotype of
atelins or atelines, which we believe more closely resembled a more robust
architecture similar to Lagothrix.
Dental morphology
The overall morphology of the Ateles dentition is consistent with its relatively
small face, but blunt snout tip. The cheek teeth are unimpressive in size, but the
incisor teeth are well developed (Figure 2.3a). This pattern stands in contrast
to Alouatta, with large cheek teeth and small incisors; Brachyteles, also with
larger cheek teeth and small incisors (Figure 2.3b); and Lagothrix, with large
cheek teeth and proportionately large incisors (Figure 2.3a). All three of these
latter taxa have larger faces, although each is built somewhat differently.
The upper dental arcade of the spider monkey is parabolic with the palate
broadening posteriorly and the molars set farther apart than the canines. The
lower dental arcade is more U-shaped, with the cheek teeth rows set closer
together and running more parallel to one another anteroposteriorly. Kinzey
(1970) attempted to quantify the length:breadth proportions of primate lower
jaws, given the purported importance of this measure for diagnosing hominins.
He developed an index, the “basic rectangle of the mandible.” The mean value
for Ateles fusciceps (a.k.a. A. geoffroyi fusciceps) was 140.5 ±1.5, placing its
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24 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
Figure 2.3 Comparative craniodental anatomy of Ateles and Lagothrix (a) and
Brachyteles and Alouatta (b). Skulls drawn to approximately the same cranial length.
Maxillary (occlusal and 3
/4lingual views) and mandibular (occlusal and 3
/4buccal
views) dentitions each drawn to approximately the same length. (From Rosenberger
and Strier, 1989, with permission of the authors.)
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Morphology and evolution 25
Figure 2.3 (cont.)
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26 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
Figure 2.4 Ratio of lower first incisor area relative to lower first molar area in Ateles
compared with both extant and extinct atelines. (Data augmented from Rosenberger,
1992.)
shape between the extreme parabola of Homo sapiens and the extreme U-shape
of some other primates.
The incisor teeth are an impressive feature of the Ateles dentition. Upper
and lower incisors are relatively wide and high-crowned. The incisors do not
appear to be disproportionately large relative to molar size (Rosenberger, 1992;
Figure 2.4). Upper central incisors are much larger than the lateral incisors and
are spatulate in shape, while the upper lateral incisors are more conical. All
lower incisors are more or less equal in size and homomorphically spatulate.
The upper canines are long, slender, and recurved in males and slightly
shorter, stouter and less projecting in females. The lower canines occlude into
a sizable diastema between the upper second incisors and the upper canines.
The maxillary canines occlude with an enlarged mesiobuccal surface of the
lower second premolars, resembling the canine–P3honing complex seen in
catarrhines. However, the canines of Ateles appear not to be particularly large.
Harvey et al. (1978) calculated relative canine size for primates, irrespective
of sex differences. They determined that canines in A. geoffroyi are about 90%
of the size expected based on a regression model that sampled 39 species,
including nonplatyrrhines.
Sexual dimorphism in canine size has been documented and assessed in dif-
ferent ways. Orlosky (1973) provided useful descriptive statistics for canine
length and breadth dimensions in A. geoffroyi and A. belzebuth, and concluded
that metric sexual dimorphism was minimal but varied in its expression in the
two. Kay et al. (1988), examining A. geoffroyi,A. fusiceps (including specimens
now known as A. geoffroyi fusciceps and A. g. robustus) and A. paniscus found
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Morphology and evolution 27
consistent degrees of dimorphism in each taxa. Using multivariate analysis, they
developed a combined measure of tooth diameters, which effectively showed
that males were about 10% larger than females. Plavcan and Kay (1988) and
Plavcan and van Schaik (1997) found the degrees of canine height dimorphism
in Ateles consistent with that of other atelines, despite perceived lower lev-
els of male–male competition (see also Masterson and Hartwig, 1998). These
interpretations should not be construed with other studies that may empha-
size monomorphism, dimorphism or negative dimorphism in Ateles species
based on other anatomical systems. For example, for A. geoffroyi, Corner and
Richtsemeier (1993) determined that skulls were monomorphic in overall mor-
phology, but noted that male and females matured at different rates. Schultz
(1960) identified negative dimorphism in some cranial dimensions but not in
others. Masterson and Hartwig (1998) noted that A. paniscus was monomor-
phic for most cranial metrics. Chapman and Chapman (1990) found negative
dimorphism in body weight.
The upper premolars are typical bicuspid teeth, wider buccolingually than
they are mesiodistally. The buccal cusp is taller than the lingual cusp and there
is a wide deep basin in the center of the tooth. P2is slightly smaller than P3
and P4, which are equal in size. Generally, crowns of the cheek teeth are of
a nonshearing design. The first and second upper molars are relatively square
and have relatively low relief, with a prominent ridge-like crista obliqua and
marginal crests that are not strongly beveled. The low cusps are spaced far apart
on the corners of the crown, creating a wide central basin. The hypocone is well
developed and tends to be separated from the central basin by a distinct groove.
Upper M3s are greatly reduced in size and complexity as compared with M1
or M2.
The lower premolars are rounded in shape with cusps that are more equal
in height. Due to its participation in occlusion and wear of the upper canine,
P2is somewhat larger than P3and P4, especially in males with larger canines.
This creates a sloping wear facet on the buccal surface and a dominant buccal
cusp that makes the tooth almost caniniform. All three premolars have a rela-
tively large bulbous buccal surface. The first two lower molars are smaller and
narrower buccolingually than the uppers. They also show a lack of shearing
crests in favor of deep basins between widely spaced, low-relief cusps. M3s are
reduced but not to the same degree as the other molars, although this could be a
variable trait among species and individuals. Both upper and lower molars lack
cingula and structures such as accessory cuspules.
Functionally, the Ateles dentition is considered well suited for a classically
frugivorous diet (Kay, 1975; Hylander, 1979; Rosenberger, 1992) with rela-
tively broad incisors and proportionately small molars (Anthony and Kay, 1993;
Anapol and Lee, 1994). The extreme reduction of third molars is connected
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28 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
with the general reduction of the masticatory apparatus (Rosenberger and Strier,
1989), as is common in frugivores. Smith (1978) concluded much the same
about Ateles in his biomechanical study of the temporomandibular joint in pri-
mates. Dental microwear studies of Ateles show a scratch-dominated pattern
related to the consumption of seeds and pulp of mature fleshy fruits (Kay, 1987).
Other pertinent functional studies are Wall (1999), who examined movements
of the mandibular condyle in A. geoffroyi cineradiographically. Additionally,
in a series of classic studies on the dynamics of the chewing cycle of primates,
Kay and Hiiemae (1974 et seq.) described the dynamics of Ateles mastication
in relation to molar morphology.
The shoulder girdle
The shoulder girdle of Ateles has been of particular interest to many researchers
(e.g., Campbell, 1937; Erikson, 1963; Ashton and Oxnard, 1963, 1964; Oxnard,
1963, 1967; Jenkins et al., 1978; Konstant et al., 1982; Turnquist, 1983;
Takahashi, 1990; Young, 2003; Jones, 2004), particularly in connection with the
comparative anatomy of gibbons and great apes and the functional morphology
of suspensory positional behaviors. Spider monkeys do exhibit many resem-
blances to hominoids, as outlined by Erikson (1963), and Ateles and the hylo-
batids are the most acrobatic arm-swingers among platyrrhines and catarrhines,
respectively. So, within the atelins, Ateles tends to present the most exaggerated
morphologies relating to brachiation-style positional behaviors and Lagothrix
the least, with Brachyteles resembling a bulked-up anatomical personification
of Ateles.Alouatta, which is quite different in its positional behavior, also differs
substantially from atelins in many anatomical details.
In Ateles, the scapula is positioned dorsally rather than on the lateral aspect
of the thorax, as is common among nonateline platyrrhines, and it is greatly
elongated craniocaudally (Figure 2.5). The glenoid fossa points cranially, even
when the arms are at rest. The scapular spine of Ateles is obliquely oriented
relative to the blade’s medial border. This has been interpreted as a facilitator
of arm-raising and an adaptation to suspensory behaviors aided by the action of
the cranial portion of the trapezius, which attaches along the scapular spine and
may assist in scapular rotation (Inman et al., 1944; Ashton and Oxnard, 1964).
A strongly angled line of attachment would add to the mechanical advantage of
the trapezius when the arm is raised. It should be noted, however, that it remains
possible that the infraspinatus, which originates on the infraspinous fossa, may
be more important for scapular rotation (Larson and Stern, 1986; Larson, 1995).
Specialization of the trapezius is also implicated by the morphology of the
acromion process, which projects past the glenoid fossa and is generally longer
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Morphology and evolution 29
Figure 2.5 Primate scapulae. Top row, left to right: Cebus,Colobus, Macaca; middle
row, left to right: Alouatta,Lagothrix,Brachyteles,Ateles,Hylobates; bottom row, left
to right: Pan,Pongo,Homo,Gorilla. (From Erikson, 1963, with permission from the
publisher.)
than in most other primates (Young, 2003). This feature may provide better
mechanical advantage for either the cranial portion of the trapezius during
scapular rotation and arm elevation (Jungers and Stern, 1984; Young, 2003),
or it may increase the length of the lever arm of the deltoid, which would be
advantageous during the elevation of the arm (Larson and Stern, 1986; Young,
2003).
Since the clavicle of Ateles spans between the manubrium on the chest and the
dorsally positioned scapula, it is obliquely oriented and relatively long (Ashton
and Oxnard, 1964; Jenkins et al., 1978). While Ashton and Oxnard (1964)
suggest that this morphology enhances the range of motion of the shoulder
joint, Erikson (1963) explains it as a correlate of the widening of the thorax
and the ventral shift of the vertebral column into the thoracic cavity, a pattern
that is typical of atelines and is also hominoid-like. Other details of clavicular
morphology that are well developed in Ateles involve its torsion and sigmoid
shape.
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30 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
Clavicular torsion occurs when the distal end of the clavicle is directed more
cranially than the proximal end. It might be related to the cranial orientation of
the glenoid fossa and the dorsal position of the scapula (Ashton and Oxnard,
1964). A sigmoidal shape occurs when the proximal portion of the clavicle
curves ventrally while the distal portion curves dorsally. The functional signifi-
cance of this pattern is unclear. Jenkins et al. (1978) suggest that it might allow
greater freedom of movement for the humerus in the glenoid fossa, while Voisin
(2006) proposes that the proximal curvature may act as a “crank” for the clav-
icular insertion of the deltoid muscle, to help rotate the glenoid cavity cranially
during the elevation of the arm. While such a function has also been empha-
sized for other mammals, Oxnard (1968) suggests that it is unlikely to serve as
a crank in primates. Konstant et al. (1982) provide additional information per-
tinent to the clavicle and shoulder. They give comparative, electromyographic
and kinematic information on the subclavius muscle of Ateles and other atelines
in connection with climbing and arm swinging.
The forelimb
Intermembral indices of the forelimb (humerus +radius/femur +tibia ×100)
have established that the upper limb as a whole is relatively longer in Ateles
than in a variety of other platyrrhine primates (Erikson, 1963). In Aotus and
Cebus the indices are 74 and 80, respectively, falling well outside the range of
Ateles, which has an index of 105. Among the other atelines, Brachyteles also
has an index 105, and the two other genera each have an index of 98. Another
measure developed by Erikson compares limb length with trunk length, and
this further emphasizes the unique proportions of Ateles. He shows that the
humerus and radius of Ateles is 150% of the length of the trunk. This compares
with Brachyteles at 140% trunk length, and with Lagothrix and Alouatta at 91%
and 109%, respectively.
More modern efforts to capture limb proportions have examined scaling.
With few exceptions, in primates the intermembral index tends to increase
with increasing body size, and in most platyrrhines the forelimbs show positive
allometry while the hindlimbs show negative allometry (Jungers, 1985). This
pattern has been explained as an adaptation to maintaining balance while climb-
ing and traveling on arboreal supports. The increased length of the forelimbs
allows an animal to lean away from a support and thus maintain a high level
of pedal friction without raising the center of gravity and decreasing overall
stability (Cartmill, 1974; Jungers, 1985). Still, Ateles has forelimbs that are
approximately 36–38% longer than expected for its body size (Jungers, 1985),
suggesting a complex functional explanation relating to an acrobatic locomotor
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Morphology and evolution 31
Figure 2.6 Primate forelimb. Left, Alouatta; right, Ateles. Proximal humeri and radii
are on the right. (After Gebo, 1996, with permission from the publisher.)
style that includes significant amounts of below-branch suspension, arboreal
climbing and quadrupedalism, as well as rapid brachiation (e.g., Mittermeier,
1978; Fontaine, 1990; Defler, 1999; Youlatos, 2002, this volume).
The shaft of the humerus of Ateles is fairly long, straight and slender, resem-
bling the upper arm of Brachyteles and, to a lesser degree, Alouatta and
Lagothrix (Figure 2.6). It has a large globular head with a small degree of
medial torsion at the humeral neck. Overall humeral shape is also a similarity
shared by Ateles and Hylobates. It has been interpreted as an adaptation that
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32 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
minimizes bending and shear stresses under torsion, which would be prevalent
during suspensory locomotion (Swartz, 1990). Another osteological correlate
to suspension is the relatively distal location of the deltoid tuberosity on the
humerus shaft. This more distal insertion of the deltoid muscle provides a greater
mechanical advantage for the deltoid when the arm is abducted (Ashton and
Oxnard, 1964).
The distal end of the Ateles humerus has an enlarged projection of the medial
epicondyle, a trait also associated with arm-swinging behavior as it relates to the
origin of most of the flexor muscles of the forearm. Takahashi (1990) suggests
that strong forearm flexors might also be a key muscle group during climb-
ing, which is extremely important in the behavioral repertoire of Ateles. While
Ateles is known for its dramatic brachiating locomotion, clambering, climbing
and quadrupedal walking and running make up roughly 50% of its locomo-
tor repertoire; 23% of locomotion is suspensory (Cant et al., 2001; see also
Youlatos, this volume). Overall the flexors are quite well developed in Ateles,
and all four digits are generally flexed at once to provide a strong grip during
suspensory postures (Youlatos, 2000). Unlike the lumbering quadrupedalist
Alouatta, which has a well-developed olecranon on the proximal ulna, the pro-
cess is reduced in Ateles.
The Ateles elbow shows several other features that are convergent on homi-
noids and contribute to an increased ability to pronate and supinate the forearm,
motions which are extensively employed during suspensory activities (Rose,
1988). The radial head is relatively round with a small lateral lip, and the area
for articulation with the radial notch of the ulna extends far around the radial
head. This results in much less restricted axial rotation of the radius than is seen
in other platyrrhine primates that have more flattening along the posterolateral
side of the radial head (Rose, 1988).
The wrist shows several unique features also correlated with the Ateles loco-
motor profile. First, the carpal tunnel is quite deep to accommodate the large
tendons of the flexors of the forearm (Napier, 1961). Napier (1961) notes that
the deep tunnel affects the position of the first metacarpal, which is largely ves-
tigial in Ateles and articulates with a trapezium that is steeply angled in toward
the palm of the hand. Second, the carpals of Ateles allow a large range of motion
across the wrist joint. A ball and socket joint is formed between the proximal
and distal carpal rows; the capitate and hamate move in the socket formed by
the proximal carpal row. This arrangement of the bones of the wrist allows mid-
carpal supination which permits increased mobility in the midcarpal region. As
a result, Ateles can rotate the wrist at both the junction between the radius and
proximal carpals and between the proximal and distal carpal rows, summing
to almost 90 degrees of axial swivel (Jenkins, 1981). This wrist morphology
also allows significantly more ulnar deviation of the hand during pronation as
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Morphology and evolution 33
well as during suspensory locomotion (Lemelin and Schmitt, 1998). Despite
the ball and socket joint, other aspects of the wrist joint remain fairly primitive
and Ateles retains the primitive synovial septum which separates the ulnar and
radial compartments of the joint (Lewis, 1971, 1972).
While the hands of spider monkeys appear superficially to be very long
and hook-like, according to Jouffroy et al. (1991) spider monkey hands are
not disproportionately longer than the hands of other platyrrhine primates in
relation to the length of the entire forelimb. Jouffroy et al. (1991) show that the
hands are approximately 27% of forelimb length; 26–32% is the range for other
platyrrhines. Relatively, Leontopithecus has the longest hands of all New World
monkeys. Regarding the functional axis and grasping pattern of the hand, Ateles
is paraxonic, with the third and the fourth digits being of equal length. Paraxonic
hands are also found in Lagothrix, but mesaxonic hands, with the middle digit
being best developed, are the norm in the other platyrrhines (Jouffroy et al.,
1991; Lemelin and Schmitt, 1998).
Of course, the most notable feature of the Ateles hand is the absence or
great reduction of the pollex (Figure 2.7), a feature shared with Brachyteles
and Colobus. In Ateles, the first metacarpal is present but, as in Colobus, the
proximal phalanx is variably present and it is very variable in size when it
does occur (Tague, 1997). We are not aware of a cogent functional argument
explaining why the external thumb is lost in these cases. Historically, while
convergence is surely behind its joint absence in platyrrhines and catarrhines,
we think the loss in Ateles and Brachyteles is more likely to be homologous.
The hindlimb
Less attention has been given to the Ateles hindlimb. Descriptions liken it to
hominoids, relating the similarities to comparable suspensory locomotor adap-
tations and somewhat orthograde body orientations (Stern, 1971; Larson, 1995,
1998; Johnson and Shapiro, 1998). Stern (1971) and Stern and Larson (1993)
give detailed descriptions of the muscles of the hip and thigh and their possible
relevance to questions related to the evolution of human bipedality. This short
list of papers forms the basis of our account.
The femoral head is very round and globular and maintains a distinct articular
surface that does not run down onto the femoral neck. The greater trochanter
is highly elevated, coming up slightly below the level of the head, with a deep
fossa behind it. Posteriorly, the proximal femur exhibits a large knob-like lesser
trochanter. Together, this morphology is indicative of a mobile hip joint, which
is consistent with the important role played by hindlimb suspension in the
positional repertoire of spider monkeys (see Youlatos, this volume).
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34 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
Figure 2.7 The hands of Hylobates (bottom) and Ateles (top). (Modified from Jouffroy
and Lessertisseur, 1977.)
The femoral shaft is slender, long, and mostly straight except for a slight
medial bowing towards the distal end. The knee joint is shallow, as expected
in a nonleaping taxon, with the medial condyle slightly larger than the lateral
condyle and a larger area for articulation with the patella. The articular surface
of the proximal tibia matches the femoral condyles; that is, the medial surface
is slightly larger than the lateral. The tibial tuberosity is broad and flat and
leads onto a tibial shaft that is strongly compressed mediolaterally. Distally,
the medial malleolus is robust and knob-like but not very long. The articular
surface on the lateral side runs up onto the shaft and the ankle joint is built to
be very mobile while being used in quadrumanous climbing and suspension.
Several studies have been done on the interior trabecular bone structure of
the Ateles postcranial skeleton. The proximal humerus and femur of A. paniscus
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Morphology and evolution 35
show the expected low degree of structural anisotropy for a suspensory taxon
whose bones are under variable, nonrepetitive loading. However, the anisotropy
values for Ateles and Hylobates, another highly suspensory taxon, overlap with
those of the more terrestrial Macaca and Papio, suggesting that the trabeculae
vary in a predictable way, but do not reliably discriminate between locomotor
groups (Fajardo and M¨uller, 2001). Similarly, the femoral neck of A. fusciceps
(a.k.a. A. geoffroyi fusciceps) and A. paniscus has a more even distribution of
bone with a thicker superior cortex relative to inferior cortex as compared with
the rest of a primate-wide sample of 21 species due to the less stereotypical and
more generalized loading orientation of quadromanus climbing, another major
component of their locomotor repertoire (Rafferty, 1998).
The trunk and spine
The spine of Ateles has several unique adaptations to suspensory locomotion, the
most interesting of which enables the tail to twist, bend, and curl up on itself,
to be used in precision gripping and powerful clasping, and to support and
probably propel the full weight of the body during some phases of brachiation.
The tail is distinguished from the tails of other atelines in having more advanced
features associated with prehensility and acrobatic locomotion. Nevertheless,
it is clearly built on an ateline base, which differs from the morphology of the
semiprehensile tailed Cebus, for example. There are several reasons for thinking
that the unique ateline tails evolved prehensile adaptations independently of the
semiprehensile tails of Cebus (Rosenberger, 1983). For example, ateline tails
are relatively longer than expected relative to body weight (Figure 2.8), and the
sensorimotor regions of the brain dealing with tail function are morphologically
conspicuous.
The trunk, like the trunks of atelines generally, is rather short and stout
when compared with the trunks of the other platyrrhine primates. The shorten-
ing occurs in the lumbar region, which is reduced to four vertebrae. Alouatta
has five lumbar vertebrae and other platyrrhines have six to seven vertebrae
on average (Schultz, 1961; Erikson, 1963). Shortening and stiffening of the
lower back is also effected as the lumbar vertebral bodies are shorter antero-
posteriorly and deeper ventrodorsally than in other platyrrhines (Erikson, 1963;
Johnson and Shapiro, 1998). Metrically, this pattern is reflected by the ratio of
lumbar:thoracic length, with Ateles presenting a value of 43%, well outside the
range of other platyrrhine primates, at 91–110% (Erikson, 1963).
The functional significance of a shortened lumbar region is a matter of debate.
Rose (1975) holds that it is associated with erect postures and compressive
forces on the spine. While the atelines do exhibit orthograde postures, these
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36 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
Figure 2.8 Scaling relationships of platyrrhine tails relative to body length. (From
Rosenberger, 1983, by permission of the author.)
postures generally occur during suspensory behavior and would not result in
high levels of compressive stress on the spine (Johnson and Shapiro, 1998).
Johnson and Shapiro (1998) counter that the shortened lumbar region may be
an adaptation for reducing bending stress on the lower portion of the spine,
which would be pronounced if the animal were supporting most or all of its
body weight by the prehensile tail.
Ankel (1972) described a variety of specializations of the sacrum in Ateles
and other atelines. The sacroiliac joint is larger than in nonprehensile-tailed
monkeys, which most likely provides more extensive support during suspensory
activity. The sacral canal is of special interest. In primates that lack external tails,
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Morphology and evolution 37
the canal ends within the sacrum itself, while in forms with long nonprehensile
tails it narrows caudally. In contrast, Ateles has a unique canal that widens
caudally to allow a relatively large bundle of nerves to pass though. They
provide innervation to the sensitive tail tip. In addition to increased innervation
in this area, Ateles also has an enhanced caudal blood supply. It has two systems
of arteries, which are lacking on the nonprehensile-tailed forms. A correlate of
this vasculature arrangement is the high neural arches of the caudal vertebrae.
The morphology of the sacrocaudal joint of Ateles allows for an unusual
capacity to “hyperextend” the tail. It is directed distodorsally rather than dis-
tally as in most nonprehensile-tailed primates (Turnquist et al., 1999). Enhanced
extension allows Ateles to grasp branches directly above while hanging verti-
cally (Turnquist et al., 1999) and is particularly suited to tail hanging while
the torso is held relatively upright to form a sharp angle with the tail axis. The
proximal part of the tail is also very flexible and heavily muscled. This may be a
result of an unusual shortening of the proximal vertebrae relative to the patterns
found in other primates (Ankel, 1972; Turnquist et al., 1999). However, this
interpretation has been contested by German (1982), who shows no statisti-
cal differences between the sizes of the proximal vertebrae of nonprehensile-
and prehensile-tailed primates. The musculature of the proximal region is also
derived in Ateles. While most primate species have equally sized dorsal and
ventral bundles of muscles, Ateles has a much greater number of muscle fibers
in the dorsal muscle group than ventral muscle group (Ankel, 1972; German,
1982; Lemelin, 1995).
The proximal portion of the tail ends with a transitional vertebra, which
is followed by a longer string of distal tail vertebrae. On average, Ateles has
20–27 distal caudal vertebrae, thus bringing the total number to approximately
28–35 (Schultz, 1961). This is a higher count than both Alouatta (25–28 total
vertebrae) and Lagothrix (24–29 total vertebrae) (Schultz, 1961). Distally, the
spider monkey tail vertebrae taper by decreasing in both length and width. Also,
the most distal vertebrae are relatively flattened dorsoventrally in comparison
with those of nonprehensile-tailed monkeys, providing greater areas for muscle
attachment and producing a thicker tail overall (Ankel, 1972; Lemelin, 1995).
To enhance distal tail flexion, Ateles has a greater number of muscle fibers
positioned ventrally in the distal portion of the tail, which contrasts with the
thicker dorsal bundles in the more proximal portion. The tail tip is also very
sensitive. It is primarily used for grasping branches during suspensory postures
and locomotion where hand grasps and tail grasps alternate (Turnquist et al.,
1999). A naked patch of friction skin on the distal ventral surface assures the
grip. It is present in all of the atelines, but not in the semiprehensile tail of
Cebus, which is fully clothed in fur.
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38 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
Figure 2.9 The skull and mandible of Caipora bambuiorum.
Evolution and phylogeny: the lessons of Ateles
Little is known about the morphological evolution of genus Ateles specifically.
However, background studies, synthesizing some of evidence for ateline evolu-
tion, are provided by Rosenberger and Strier (1989) and Hartwig (2005). There
is no fossil record immediately relevant to the spider monkeys as there is for
some other modern platyrrhines, which may have evolved as long-lived genera
or tribes (e.g. Alouatta,Saimiri,Aotus,Callimico; Delson and Rosenberger,
1984; Setoguchi and Rosenberger, 1987; Rosenberger et al., 1990). There are
a few extinct forms to provide contextual perspective. For example, a single
lower molar tooth representing Solimoea acrensis is known from the ∼8 mil-
lion year old (Ma) Acre Formation of western Brazil (Kay and Cozzuol, 2006).
It resembles Ateles in some ways but is generally more primitive. Kay and
Cozzuol place the species as a stem atelin, inferring that it was 5–6 kg in
weight and interpreting its diet as Ateles-like based on comparable develop-
ment of molar shearing crests. This is somewhat surprising since the Ateles diet
is an evolutionary extreme, and other models (Rosenberger and Strier, 1989)
infer that a more Lagothrix-like molar morphology, suited for a more eclectic
frugivorous/folivorous diet, would be basal in atelins. The phylogenetics of this
taxon merits further study as more evidence becomes available.
A second fossil form appears to be more closely related to Ateles,Caipora
bambuiorum from the Pleistocene/Recent of central Brazil (Cartelle and
Hartwig, 1996; Figure 2.9). Ateles and Caipora present numerous shared
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Morphology and evolution 39
Table 2.2 Body weights of extinct and
extant atelines
Species Weight (kg)
Alouatta fusca 4.4a
Alouatta caraya 5.2a
Alouatta belzebul 5.6a
Alouatta palliata 6.0a
Alouatta seniculus 6.2a
Lagothrix lagothricha 6.9a
Ateles belzebuth 8.1a
Ateles geoffroyi 8.2a
Paralouatta varonai 9.6–10.2b
Brachyteles arachnoides 13.5a
Caipora bambuiorum 20.5c
Protopithecus brasiliensis 24.9d
Sources:aRosenberger (1992), bMacPhee and
Meldrum (2006), cCartelle and Hartwig (1996),
dHartwig and Cartelle (1996).
derived craniodental similarities but the latter is much larger in body size and
may be different in several aspects of the postcranial skeleton, all of which may
indicate different microhabitat preferences, and an alternative positional and
locomotor profile. Further work is required, but if Caipora, at a body weight of
20 kg, is as closely related to Ateles as we suspect, it raises interesting possibil-
ities concerning the foraging advantages to spider monkeys of being relatively
small in size for an atelin (Table 2.2), a perspective that was lacking in the
past (e.g. Rosenberger and Strier, 1989). Caipora and its equally large alouattin
counterpart from the same fauna, Protopithecus brasiliensis,may be autapomor-
phic giants at 20–25 kg, but there is also the possibility that Ateles has become
reduced in body size from a larger bodied ancestor as the brachiation complex
evolved. Another datum that is pertinent to long-term evolutionary history of
Ateles is the presence at La Venta, Colombia, at 12–14 Ma, of two Stirtonia
species, very closely related to Alouatta, if not representing the same genus.
This small body of paleontological evidence suggests that the alouattin and
atelin clades were probably established in South America by the late Middle
Miocene, and that there was dental morphology (e.g. Solimoea) of relevance to
the evolution of Ateles at that time. With the existence of Caipora, it is also more
evident that evolution produced a “clade of spider monkeys,” not simply the
one genus that is now split into several species, and that we should not expect
all of these close relatives to be adaptively constrained to resemble the modern
Ateles lifestyle in all its dimensions. Moreover, these extinct spider monkey
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40 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
relatives will offer important clues for piecing together a more detailed picture
of Ateles evolution, integrating their lessons with the information derived from
the living taxa.
Another morphological perspective was presented by Rosenberger and Strier
(1989). In the absence of fossils, other than one coming from the alouattin sister
taxon of atelines, Stirtonia, they took a different approach in employing an adap-
tational character analysis and cladistic study of the modern genera, combining
morphology, ecology and behavior. The branching pattern they endorsed (see
Figure 2.10) held that Ateles and Brachyteles are sister taxa that together link up
with Lagothrix, with the latter representing the stem atelin lineage. Their con-
clusions emphasized the soft fruit feeding and hyperactive locomotion of Ateles
as unique adaptations among the atelins, involving a pattern set that is more
derived than the more generalized frugivory/folivory and suspensory locomotor
style of the last common ancestor (LCA) shared by Ateles and Brachyteles.
Molecular evidence is consistent with this very general picture, as Hartwig
discussed at length in his re-examination of ateline interrelationships (Hartwig,
2005). There is only one point of discord between the ecomorphological
(Rosenberger and Strier, 1989; Rosenberger, 1992; Strier, 1992) and the molec-
ular studies, which is whether Ateles is more closely related to Lagothrix or
to Brachyteles. Several laboratories have investigated the interrelationships of
platyrrhines using a variety of nuclear and mitochondrial genes. They have
come to consistently demonstrate a monophyletic Atelini and a sister-taxon
relationship of Lagothrix and Brachyteles (e.g. Schneider et al., 1993; Harada
et al., 1995; Schneider et al., 1996; Horovitz et al., 1998; von Dornum and
Ruvolo, 1999; Meireles et al., 1999; Canavez et al., 1999). Collins (2004), on
the other hand, who also employed molecular data, suggested that this link is
not exceptionally robust since its return via parsimony algorithms is influenced
by taxonomic sampling. When different species of Ateles were included in
his analyses, the relationship among Ateles,Brachyteles, and Lagothrix were
shown to be unstable. The same phenomenon has been shown using cranial
morphology (L. Matthews and A. Rosenberger, unpublished data).
No matter how the relationships of this triad turn out in the long run, the
important point about what we have learned regarding Ateles phylogenetics
is that the genus is part of a small monophyletic group of modern atelins that
joins with Alouatta to comprise a coherent ecophylogenetic radiation. Prior to
the 1980s, it was widely assumed that howlers had little to do with atelins (e.g.
Hershkovitz, 1977), and that muriquis were the howler’s closest living relatives
(Zingeser, 1973). This latter view was promoted for a while even into the 1990s
(Kay, 1990; but see Anthony and Kay, 1993). Establishing, with a high degree
of confidence, that Ateles,Brachyteles and Lagothrix form a cladistic trio is
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Figure 2.10 Annotated cladograms illustrating possible interrelationships of the
ateline primates, with alternative positions of Brachyteles shown to reflect the
predominant views indicated by molecular (top) and morphological (bottom) studies.
1. Evidence for their generic separation of Alouatta and Stirtonia is meager; Stirtonia
is only known from dental remains. 2. While we hold that Protoalouatta and
Paralouatta are alouattins, with Paralouatta most likely being more closely related to
Stirtonia–Alouatta clade, their detailed interrelationships are currently under study. 3.
The position of Solimoea follows Kay and Cozzuol, 2006. Since it is based on a single
molar tooth that has an Ateles-like reduction in its shearing crests, which is not
consistent with our interpretation of the atelin morphotype, we caution that additional
information may easily alter this position. 4. The morphological and molecular
interpretations regarding the cladistic position of Brachyteles differ: morphology
supports a sister-group relationship with Ateles; molecules support the link to
Lagothrix. 5. See Cartelle and Hartwig (1996).
41
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42 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
a major step forward. It is the Big Idea behind all manner of evolutionary
hypotheses about the natural history of Ateles and the atelins.
Cladistics, however, is only a piece of the puzzle. A broader, more penetrat-
ing question asks: How, ecologically, did Ateles evolve? The Rosenberger and
Strier (1989) scenario, as mentioned, attempted to get at some of the answers
by examining how and why anatomical and behavioral features evolved trans-
formationally among atelines. Rosenberger et al. (in press) explore a different
aspect of the problem by raising questions about community evolution and the
biogeographic history of platyrrhines in the New World. Monkeys have been
scattered about South America in varying degrees of geographic isolation, occu-
pying habitats of varying quality, even as grasslands, now covering 60% of the
landscape, have been the predominant terrestrial biome on the continent for
almost 30 million years. Rosenberger et al. (in press) point out that over the
past 26 million years (at least), platyrrhine evolution has taken place in four
distinct provinces in South America: Amazonia, the Atlantic Coastal forest,
Patagonia, and the Caribbean, in addition to Central America. They propose
that several of the 14 living platyrrhine genera now inhabiting Amazonia may
actually have arisen elsewhere. Ateles is not one of these, nor is Lagothrix.
But like the eastern Brazilian endemic Brachyteles, which likely evolved in and
along with the Atlantic Coastal forest, there is a chance that the pan-Neotropical
Alouatta also emerged originally outside of Amazonia. Among nonatelines,
Cebus,Callicebus, and Aotus are other candidates for extra-Amazonian ori-
gins. While Ateles is ensconced in continental South and Middle America (and
has also been recorded as a prehistoric relic in Cuba, though possibly as an
import), its crossing of the Panamanian land bridge is a recent phenomenon,
related to uplift of the isthmus about 3 million years ago. Thus, effectively,
Ateles, a devotee of high, mature, wet, large-treed habitat – and decidedly not
an ecological marginalist – is an Amazonian endemic. It may have arisen in
that biogeographic province as the lowland region evolved its distinctive mod-
ern properties during the last 15 million years, according to one hypothesis of
Amazonia’s evolution (Campbell et al., 2006).
If Ateles is a creation of the lowland rain forest, its long Amazonian fixation
may be a vivid clue to its history by hinting at a community rationale for the spi-
der monkey’s adaptive differentiation. The Amazonian province, by comparison
with the Atlantic province and also Middle America, supports the highest degree
of primate endemism on the continent, the richest assemblages of sympatric pri-
mate diversity, and the most varied cornucopia of pertinent foodstuffs. Ateles
has succeeded by evolving a unique niche among Amazonia’s large biomass of
platyrrhine frugivores. This niche revolves around eating an array of ripe soft
fruit that perhaps only Ateles can afford, given the expensive time and energy
budget involved in being so choosy when targeted foods are widely dispersed in
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Morphology and evolution 43
space and also attractive to others. The capacity of spider monkeys to extract an
inordinate amount of its protein needs from fruit sources, apparently, is also a
matter of interest and may be part of its sympatric niche-differentiating strategy.
But the connection between this sugary fruit diet and an acrobatic locomotor
style is not clear. Easy rapid travel through the complex substrate web of the
treetops may provide a distinct advantage if the cost of racing to patchily dis-
tributed foods is balanced by the anatomical autapomorphies enabling Ateles to
do so in an energetically efficient manner. On the other hand, perhaps the acro-
batics are basic to mating as well as other social behaviors. Rapid brachiation
may be important in managing long-distance intertroop dispersal, maintaining
group spatial cohesion as a counterbalance to having widely dispersed, small
fission–fusion parties, or enabling exuberant, noisy agonistic displays as an
affectation related to mate attraction, or to dissuade food competitors. A ratio-
nale for the Ateles postcranial skeleton that ignores these “nonmorphological”
domains of behavior can only be incomplete, at best. If mating strategies and
sociality were not having a profound effect on the evolution of the Ateles body,
the genus would not be prone to sexual monomorphism.
One might also ask: Why quadrumanous, tail-mediated brachiation in the first
place? That is, why center the locomotor pattern on hanging? Another form of
quadrupedalism would seem to do just as well, as any arboreal cercopithecoid
would testify. The explanation for this must go to the very foundations of ate-
lines. Pedal hanging may have been a basal adaptation in atelids (Meldrum,
1993), inherited and abetted by tail-assisted hanging in atelines as body size
increased in their LCA (see Rosenberger and Strier, 1989). Originally, this is
likely to have been more important as a postural adaptation rather than man-
ifestly and narrowly locomotive. Principally, foot and tail hanging provide a
longer reach than simple forelimb extension, and in trees, a longer stable reach.
Forelimb elongation may have originally been part of this syndrome, useful for
climbing, for reaching foods and grabbing branches sturdy enough to support a
relatively heavy primate. Writ on a much smaller size scale, the unusually long-
forearmed Leontopithecus accomplishes similar objectives: clinging to vertical
supports of large diameter and probing huge arboreal bromeliads where prey
is cached. Where, precisely, in the canopy environment these biological roles
became prominent and of high selective value for Ateles is difficult to say. Most
likely it was universally important, in the terminal branch milieu as well on
larger boughs and branches. The value of tail hanging to augment reaching
below the canopy also should not be underestimated. There is a whole range
of fruit-bearing angiosperms whose niche is that of a small below-canopy tree,
perhaps small enough so that a tail-hanging ateline might prefer to forage them
from above, by suspension, rather than climb into them. With many simultane-
ous selective benefits accrued through semistatic hanging from limbs and tail,
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44 A. L. Rosenberger, L. Halenar, S. B. Cooke et al.
the final step in the spider monkey direction, taken partly by Brachyteles and
fully fledged by Ateles, was the addition of the brachiation dynamic as a new
locomotor pattern with multiple biological roles.
The varied hallmarks of spider monkeys and gibbons – acrobatic suspen-
sory positional behaviors, rapid long distance travel, preference for ripe pulpy
fruit, perhaps a somewhat small body size within their respective clades, size
monomorphism and a small foraging-group propensity – whether enforced by
a monogamous mating system or facilitated by a fission–fusion social system,
appear to be syndromes involving many parallelisms. The complete elegance of
this evolutionary package is far from what Geoffroy Saint-Hilaire had in mind
when he dubbed spider monkeys genus Ateles.
Acknowledgements
We thank the Tow Travel Fellowship of Brooklyn College and the Professional
Staff Congress of the City University of New York for providing funding that
made this research possible.
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