Chapter 2
Fossil Alouattines and the Origins of Alouatta:
Craniodental Diversity and Interrelationships
Alfred L. Rosenberger, Siobhán B. Cooke, Lauren B. Halenar,
Marcelo F. Tejedor, Walter C. Hartwig, Nelson M. Novo,
and Yaneth Muñoz-Saba
Abstract The howler monkey clade includes species of Alouatta and four extinct
genera, Stirtonia, Paralouatta, Protopithecus, and probably Solimoea as well.
Contrary to expectations, this radiation may have originated as a largely frugivorous
group; advanced, Alouatta-like leaf-eating is a novelty well-developed in the
Alouatta-Stirtonia sublineage only. Revised body mass estimates place Stirtonia
and Paralouatta within the size range exhibited by the living forms and confirm the
A.L. Rosenberger
Department of Anthropology and Archaeology, Brooklyn College, The City University
of New York, 2900 Bedford Avenue, Brooklyn, NY 11210, USA
The Graduate Center, The City University of New York, 365 Fifth Avenue, New York,
NY 10016, USA
New York Consortium in Evolutionary Primatology (NYCEP), The City University
of New York, New York, NY, USA
Department of Mammalogy, The American Museum of Natural History, Central Park
West at 79th St., New York, NY 10024, USA
S.B. Cooke
Department of Anthropology, Northeastern Illinois University,
5500 N. St. Louis Avenue, Chicago, IL 60625, USA
L.B. Halenar
Department of Biological Sciences, Bronx Community College, The City University
of New York, 2155 University Avenue, Bronx, NY 10453, USA
New York Consortium in Evolutionary Primatology (NYCEP), The City University
of New York, New York, NY, USA
M.F. Tejedor (*) • N.M. Novo
Centro Nacional Patagónico-CONICET,
Boulevard Brown 2915, (9120), Puerto Madryn, Provincia de Chubut, Argentina
e-mail: tejedor@cenpat.edu.ar
W.C. Hartwig
Department of Basic Sciences, Touro University College of Osteopathic Medicine,
Mare Island, Vallejo, CA 94592, USA
Y. Muñoz-Saba
Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá, DC, Colombia
© Springer Science+Business Media New York 2015
M.M. Kowalewski et al. (eds.), Howler Monkeys, Developments in Primatology:
Progress and Prospects, DOI 10.1007/978-1-4939-1957-4_2
21
22
A.L. Rosenberger et al.
place of Protopithecus in a larger, baboon-like size range. While their dentitions are
more primitive than the Alouatta-Stirtonia pattern, the cranial anatomy of
Protopithecus and Paralouatta is distinctly similar to living howler monkeys in
highly derived features relating to enlargement of the subbasal space in the neck and
in head carriage, suggesting that ancestral alouattines may have had an enlarged
hyolaryngeal apparatus. All alouattines also have relatively small brains, including
Protopithecus, a genus that was probably quite frugivorous. The successful origins
of the alouattine clade may owe more to key adaptations involving communication
and energetics than dental or locomotor breakthroughs. While the fossil record confirms aspects of previous character-analysis reconstructions based on the living
forms, alouattines experienced a complexity of adaptive shifts whose history cannot
be recoverable without a more complete fossil record.*
Resumen El clado de los monos aulladores incluye las especies de Alouatta y
cuatro géneros extintos, Stirtonia, Paralouatta, Protopithecus y probablemente
Solimoea. Contrario a las expectativas, esta radiación pudo haberse originado a partir de hábitos frugívoros. La avanzada folivoría de Alouatta es una novedad desarrollada solamente en el sublinaje de Alouatta-Stirtonia. Las estimaciones de masa
corporal ubican a Stirtonia y Paralouatta dentro del rango que exhiben las formas
vivientes y confirman la posición de Protopithecus en un rango de tamaño mayor,
similar al de los babuinos africanos. Considerando que la dentición es más primitiva
que el patrón observado en Alouatta-Stirtonia, la anatomía craneana de Protopithecus
y Paralouatta es similar a la de los aulladores vivientes debido a los rasgos altamente especializados relacionados al agrandamiento del espacio sub-basal en el
cuello, así como en la posición de la cabeza, sugiriendo que los alouatinos ancestrales pudieron haber tenido un gran aparato hiolaríngeo. Todos los alouatinos también presentan un cerebro pequeño, incluyendo Protopithecus, género que
probablemente haya sido frugívoro. El origen exitoso del clado de los alouatinos
pudo deberse más a adaptaciones de comunicación y energéticas que a cambios
dentarios o locomotores. Mientras que el registro fósil confirma ciertos aspectos de
análisis de caracteres previos basados en formas vivientes, los alouatinos experimentaron una complejidad de adaptaciones cuya historia no podría reconstruirse sin
el registro fósil.*
Keywords Fossil primates • Howler monkeys • Craniodental morphology •
Adaptation • Phylogeny
* Since this chapter was written, additional study by Halenar and Rosenberger (2013) of the material discussed here as Protopithecus led to the conclusion that the two samples actually represent
two different genera. The essentially complete Bahian skeleton, which forms the basis of the present discussion, is being assigned to a new genus and species, Cartelles coimbrafilhoi, within subfamily Alouattinae. The original Lund material from Minas Gerais bears the original name
Protopithecus, but its affinities are more likely to be found among atelines than alouattines.
2
Evolution of Alouattines
23
Abbreviations
%
CT
e.g.
Fig.
Figs.
i.e.
kg
m1
m3
M1
MA
mm
NWM
P3
p4
P4
2.1
Percent
Computed Tomography
For example
Figure
Figures
In other words
Kilograms
First lower molar
Third lower molar
First upper molar
Millions of years
Millimeters
New World monkeys
Third upper premolar
Fourth lower premolar
Fourth upper premolar
Introduction
Fossils discovered in recent years have added important information to our knowledge of the diversity and evolution of platyrrhines closely related to one of the most
anatomically divergent members of the radiation, the living howler monkeys,
Alouatta. While the record is still scant, these additions mean the alouattine-plusateline clade, i.e., the fully prehensile-tailed New World monkeys (NWMs), is
becoming one of the better-known lineages among the platyrrhines. Only pitheciines are better represented taxonomically among Tertiary and Quaternary remains
(Rosenberger 2002).
The first historical narratives of the evolution of howler monkeys are of recent
vintage, and they relied extensively on character analysis of the morphology and
behavioral ecology of living atelids rather than paleontology (e.g., Rosenberger and
Strier 1989; Strier 1992). Out of necessity, these studies focused on the contrasts
between the living members of the two sister clades, alouattines (Alouatta) and
atelines (Lagothrix, Ateles, Brachyteles). Few relevant, informative fossils were
known prior to the 1980s. The one exception was Stirtonia tatacoensis from the
middle Miocene La Venta beds of Colombia, 13.5–11.8 MA (Flynn et al. 1997). It
was first found as dental remains in the late 1940s (Stirton 1951) and the species has
been widely recognized as being both similar and related closely to Alouatta (e.g.,
Szalay and Delson 1979; Setoguchi et al. 1981; Delson and Rosenberger 1984;
Rosenberger 1992; Hartwig and Meldrum 2002; but see Hershkovitz 1970). In the
late 1980s, a second species, S. victoriae, was discovered at La Venta (Kay et al.
1987), and an isolated Stirtonia molar from the younger, late middle Miocene
24
A.L. Rosenberger et al.
Solimões Formation in western Brazil, about 8 MA, also came to light recently
(Kay and Frailey 1993). Stirtonia reinforced the notion that leaf-eating was an
enduring and essential aspect of the howler monkey’s ecophylogenetic biology. The
type specimen of another species related to Alouatta, Protopithecus brasiliensis
from the Quaternary of Brazil, had been known since 1838 (Lund 1838), but the
fossil was based on a partial humerus and femur and could not be properly interpreted for another 150 years (Hartwig and Cartelle 1996; see footnote above).
Finds in Brazil and Cuba add another dimension of complexity to the StirtoniaAlouatta story, introducing an unexpected anatomical diversity. This panorama of
diversity highlights the unusual nature of living Alouatta as a genus and suggests a
need to reevaluate the Rosenberger and Strier (1989)/Strier (1992) model of alouattine evolution. Besides Protopithecus brasiliensis, the Alouatta clade also includes
Paralouatta varonai from the Quaternary of Cuba (Rivero and Arredondo 1991)
and perhaps Paralouatta marianae from the Miocene of Cuba (see MacPhee et al.
2003). If the latter species, known only from a single astragalus, is indeed an alouattine, these congeners represent a lengthy span of geological time. More problematic
is Solimoea acrensis, described from a small set of isolated dental elements, two
specimens including three teeth, discovered in Brazil’s Solimões Formation (Kay
and Cozzuol 2006). The best evidence of its affinities consists of a single lower
molar, which has distinctive crown morphology. The species was originally interpreted as a stem ateline, but we present reasons why it is probably an alouattine.
Finally, also from a late Pleistocene cave of Bahia, Brazil, is a little known extinct
species of howler monkey, Alouatta mauroi (Tejedor et al. 2008), which we mention
only for the sake of completeness.
Our purpose here is to establish the taxonomic composition and interrelationships of living and extinct alouattines, present new information pertaining to their
craniodental diversity, and explore several aspects of alouattine evolutionary history
as an adaptive array. The phylogenetics and differentiation of this group has not
been discussed previously. Part of the reason for this is that the composition of the
subfamily Alouattinae is a matter of debate. In addition to the question of Solimoea,
raised here for the first time, there are different views about the affinities of
Paralouatta (e.g., Rivero and Arredondo 1991; MacPhee and Horovitz 2002;
Rosenberger 2002), which MacPhee and colleagues (MacPhee et al. 1995; Horovitz
and MacPhee 1999) maintain is monophyletically related to the other extinct
Caribbean primates and, among the extant forms, to mainland Callicebus, a pitheciid. The present study emphasizes why, from a functional-morphological perspective, an affinity with alouattines is the more parsimonious hypothesis, as Rivero and
Arredondo (1991) originally proposed.
2.2
Methods
Craniodental measurements of the modern samples used in this study are largely
from collections in the American Museum of Natural History, the United States
National Museum, the Field Museum of Natural History, the Natural History
2
Evolution of Alouattines
25
Museum (London), the Museu Nacional de Rio de Janeiro, and the Zoologisk
Museum, Statens Naturhistoriske Museum (Copenhagen). Species identifications
and sample sizes are given where appropriate. Standard linear craniodental measurements were taken to the 0.10 mm with digital calipers. Some teeth were measured using high-resolution laser scans of epoxy casts, using Landmark Editor
(Wiley et al. 2005). Endocranial volumes were taken by pouring small plastic beads
or other filler into the cavity then transferring the mass to a graduated glass beaker,
except in the case of Paralouatta varonai. It was CT scanned in Havana, Cuba,
using a medical scanner and a slice thickness of 0.8 mm. Using ImageJ (http://rsb.
info.nih.gov/ij/), the endocranial cavity was then outlined as individual slices, composited, and measured. Some measurement error was unavoidable due to difficulty
in separating bone from the matrix-filled cavity, but our figures here are consistent
with other measurements used in the context of our assessment of relative brain size
(see below).
Genealogical interrelationships were inferred using conventional, nonalgorithmic procedures of character analysis and cladistic reconstruction. Our methodology is based on the functional-adaptational approach (see Szalay and Bock
1991). Reviews of the methodology as applied to atelids can be found in Rosenberger
and Strier (1989), Rosenberger et al. (1990), and Rosenberger (1992), where additional references to the literature on cladistic phylogeny reconstruction can be
found. Our intent has been to produce a character analysis that elucidates the
homologies and polarities of functionally relevant anatomical features. We thus use
functional-adaptive inference as well as taxonomic distributional information. The
latter relies on commonality and out-group comparisons in order to develop hypotheses about the directionality of change in traits, but functional-adaptive information
is necessary to hypothesize why such changes may have taken place. Although we
do not specifically present distributional information on non-atelids, we draw on the
morphology of the other platyrrhines, living and extinct, as a collective out-group in
working out polarities.
We focus on large-scale morphological features that are demonstrably important
in distinguishing Alouatta from other atelids at the genus level and are also relevant
functionally to the evolution of howler monkey craniodental adaptations, since we
are interested in establishing how unit characters evolved within functional complexes as a part of the phylogenetic history of alouattines. Our rationale presumes
that the Alouatta cranium and dentition, which is radically different from most primates in many ways, is composed of an assortment of features that are derived relative to other atelids and platyrrhines. We hypothesize that the evolution of many
craniodental features has been driven specifically by a novel adaptive complex relating to howling and folivory.
Solimoea, which we limit to a single molar tooth as discussed below, is referenced only sparingly in the character analysis, which emphasizes cranial anatomy.
The basis for our interpretation of the fossil’s affinities is presented in the body of the
text following the same functional-adaptive lines employed to assess the cranium.
One feature we address but do not examine through a structured character analysis is body mass. While it has always been evident that body size would figure
26
A.L. Rosenberger et al.
prominently in narrative explanations of platyrrhine evolution (see Hershkovitz
1972; Rosenberger 1980), its importance for atelids has become stunningly reaffirmed by discovering the large subfossils Protopithecus and Caipora. The initial
body weight estimates for these genera (Cartelle and Hartwig 1996; Hartwig and
Cartelle 1996) placed both well outside the range of modern forms. However, they
were made using regression equations based on a catarrhine reference sample, a
phylogenetically less desirable methodology (Hartwig 1995). Statistically robust
equations based on platyrrhine postcranial elements which have been shown to be
closely linked with body size (e.g., Ruff 2003) have recently been published and
confirm the original estimates (Halenar 2011a, b). They have also been used to confirm an estimate of approximately 7–9.5 kg for Paralouatta (Cooke and Halenar
2012). We have taken a less formalistic approach in order to factor in this new information on size and integrate it with the broader analysis. The taxonomic terminology we use divides the monophyletic family Atelidae into alouattines (subfamily
Alouattinae: extant Alouatta; extinct Stirtonia, Paralouatta, Protopithecus, and
Solimoea) and atelines (subfamily Atelinae: extant Ateles, Brachyteles, and
Lagothrix; extinct Caipora).
2.3
2.3.1
Results
Craniodental Morphology and Paleontological Synopsis
Two of the three fossil alouattine genera are represented by very good crania
(Table 2.1). The third, Stirtonia, is known by excellent dental remains (e.g.,
Hershkovitz 1970; Szalay and Delson 1979; Setoguchi et al. 1981; Kay et al. 1987;
Fleagle et al. 1997; Fleagle 1999; Hartwig and Meldrum 2002). The latter preserves
both upper and lower cheek teeth that are unmistakably similar to Alouatta (see
Figs. 2.1 and 2.2), so much so that Delson and Rosenberger (1984) suggested that
generic separation obscures the possibility that Stirtonia and Alouatta may share an
ancestor–descendant relationship and that classifying them as congeners ought to be
considered. However, more work needs to be done to more accurately determine the
relationships between Stirtonia and Alouatta.
Like Alouatta, the upper molars of Stirtonia (Fig. 2.1) are relatively square, with
an elevated, lobe-like hypocone; high-relief buccal cusps carrying a long ectoloph;
deeply notched centrocrista; and a well-developed stylar shelf area. Lower molars
have a small, elevated trigonid with protoconid and metaconid set at an oblique
angle and a long talonid with a sharply angled, elongate cristid obliqua. This pattern
of features, including elements that have been assessed quantitatively in Alouatta
(e.g., Kay 1975; Rosenberger and Kinzey 1976; Kay and Hylander 1978; Kay et al.
1987), is universally interpreted as shearing, leaf-eating characteristics. The upper
and lower premolars of Stirtonia are also consistent with an Alouatta-like morphology, as are the tooth proportions. Incisors are not known for Stirtonia, but the intercanine span in the type mandible appears to be relatively narrow; Alouatta incisors
2
Genus and species
Stirtonia tatacoensis
Locality
La Venta,
Colombia
Age
Middle
Miocene
Attributed material
Mandible, isolated teeth
Body size (kg)
6
Stirtonia victoriae
La Venta,
Colombia
Rio Acre, Brazil
Cueva de Mono
Fosil, Cuba
Middle
Miocene
Late Miocene
Pleistocene
Gnathic-dental (including
deciduous teeth)
Isolated lower molar
Craniodental and
postcranial
10
Domo de Zaza,
Cuba
Lagoa Santa,
Brazil; Toca da
Boa Vista, Brazil
Rio Acre, Brazil
Early Miocene
Astragalus
Late
Pleistocene
Late Miocene
Gruta dos
Brejoes, Brazil
Late
Pleistocene
Proximal femur, distal
humerus; nearly complete
skeleton
Isolated lower molar
(provisionally m1)
Craniodental
Stirtonia sp.
Paralouatta varonai
Paralouatta marianae
Protopithecus brasiliensis
Solimoea acrensis
Alouatta mauroi
Major references
Stirton (1951), Hershkovitz (1970),
Setoguchi (1980), Setoguchi et al. (1981),
Setoguchi and Rosenberger (1985)
Kay et al. (1987)
5.4–6
Kay and Frailey (1993)
Rivero and Arredondo (1991), Horovitz
and MacPhee (1999), MacPhee and
Meldrum (2006)
MacPhee and Iturralde-Vinent (1995),
MacPhee et al. (2003)
Lund (1838), Hartwig (1995), Hartwig
and Cartelle (1996), Hartwig (2005),
(see footnote above)
Kay and Cozzuol (2006)
NA
Tejedor et al. (2008)
9.5
25
Evolution of Alouattines
Table 2.1 Summary of known fossil alouattines
27
28
A.L. Rosenberger et al.
Fig. 2.1 Laser scan
generated occlusal views of
atelid left maxillary molars
[digitized at 25 μm point
intervals (here and below)
from epoxy casts]. Teeth at
left are first molars, in most
cases brought to about the
same mesiodistal lengths. (1)
Ateles geoffroyi, (2) Caipora
bambuiorum, (3) Lagothrix
lagotricha, (4) Brachyteles
arachnoides, (5) Alouatta
seniculus, (6) Stirtonia
tatacoensis, (7) Paralouatta
varonai, (8) Protopithecus
brasiliensis
are relatively small (see below). There is no information on the posterior part of the
mandible of Stirtonia, the extreme expansion of which is diagnostic of Alouatta.
Protopithecus brasiliensis is now known from a nearly complete skeleton with a
very well-preserved skull (Figs. 2.3, 2.4, and 2.5) that includes the anterior teeth,
premolars, and a partial upper molar, as well as a mandible with anterior teeth and
premolars. It presents an interesting mosaic of craniodental and postcranial traits
not found in any other NWM (Hartwig and Cartelle 1996). It shares several cranial
features exhibited only in Alouatta among the living platyrrhines, including a
relatively extended basicranium and a compound temporo-nuchal crest, which led
Hartwig and Cartelle to recognize its alouattine affinities. The teeth of Protopithecus
are still incompletely analyzed. They are nonetheless highly informative for the
present purpose (see below).
2
Evolution of Alouattines
29
Fig. 2.2 Laser scan generated occlusal views of atelid left mandibular molars (protocols as above).
(1) Ateles geoffroyi, (2) Caipora bambuiorum, (3) Lagothrix lagotricha, (4) Brachyteles arachnoides, (5) Alouatta seniculus, (6) Stirtonia tatacoensis, (7) Paralouatta varonai (m1, m3)
Fig. 2.3 Crania of extant and extinct members of the alouattine and ateline radiations (lateral
view). Left to right, top row: Brachyteles, Lagothrix, Alouatta. Bottom row: Caipora, Protopithecus,
Paralouatta. Scale bars represent 1 cm. Note the similarities linking Alouatta, Protopithecus, and
Paralouatta to the exclusion of the other three genera, especially size and shape of the neurocranium and the airorynchous facial skeleton. The latter trait is indicated by the more acute angle
superimposed upon those three skulls between the nasal bridge and the tip of the incisors
Paralouatta has been classified as two species, P. varonai and P. marianae
(Rivero and Arredondo 1991; MacPhee et al. 2003). The latter is known only by an
astragalus. The former is represented by a fairly well-preserved but broken skull
with worn teeth, a mandible, various isolated teeth (Figs. 2.1, 2.2, 2.3, 2.4, and 2.5),
and postcranial material (Rivero and Arredondo 1991; Horovitz and MacPhee 1999;
MacPhee and Meldrum 2006). The phylogenetic connection to Alouatta that we
30
A.L. Rosenberger et al.
Fig. 2.4 Basal view of (left to right) Lagothrix, Alouatta, Protopithecus, and Paralouatta. Scale
bars represent 1 cm. Note the anterior-posterior elongation of the alouattine cranial base, as well as
the more marked postorbital constriction. The orientation of the foramen magnum and nuchal
region of the fossils is intermediate between the ateline condition of Lagothrix and the alouattine
condition of extant howler monkeys
Fig. 2.5 Posterior view of (left to right) Caipora, Protopithecus, and Paralouatta, brought approximately to same cranial width. Contrast the relatively small, low braincase; cylindrical brain shape;
and prominence of both the temporal (red arrow) and nuchal (blue arrow) crests of Protopithecus
and Paralouatta with the rounded, globular braincase; lack of marked temporal lines; and a much
less rugose nuchal plane of Caipora
advocate is a matter of controversy. The first specimen, the skull, was found prior to
the recovery of the new Brazilian Protopithecus material which, as we explain
below, supports the case for the alouattine affinities of Paralouatta. When initially
described, its overall morphology convinced Rivero and Arredondo (1991) that
Paralouatta is closely related to its namesake Alouatta. However, MacPhee and colleagues argued that Paralouatta belongs to a newly recognized clade of Greater
Antillean primates (MacPhee et al. 1995; Horovitz and MacPhee 1999; MacPhee
and Horovitz 2004) most closely related as a group to Callicebus. This was based
on the finding by Horovitz and MacPhee (1999) of three alleged unambiguous,
observable craniodental characters that support the clade including Antillothrix bernensis, Xenothrix mcgregori, and Paralouatta varonai: nasal fossa wider than palate
2
Evolution of Alouattines
31
at level of M1, lower canine alveolus buccolingually smaller than p4, and m1
protoconid with bulging buccal surface. While this is an intriguing result given the
isolation of these taxa from the mainland, it is far from definitive. Thus, Rosenberger
(2002) held that Rivero and Arredondo (1991) were correct, as we further elaborate
below. An added dimension to the paleobiology of Paralouatta was recently introduced by study of the postcranium. It led MacPhee and Meldrum (2006) to suggest
Paralouatta may have been semiterrestrial.
The fourth fossil species we present as alouattine is Solimoea acrensis (Kay and
Cozzuol 2006). The type specimen is an isolated lower molar with good crown
morphology, identified as an m1. The general description given above for Alouatta
and Stirtonia lower molars, which as we stated appears to be universally regarded as
howler monkey-like and largely unique to NWMs, compares favorably with the pattern of Solimoea. All are relatively long teeth, with a compact, small elevated trigonid, obliquely oriented trigonid wall (postvallid), elongate talonid, and a long and
deeply inflected cristid obliqua.
Caipora bambuiorum, from the same cavern that produced Protopithecus
(Cartelle and Hartwig 1996), is in our view the only known extinct ateline (but see
footnote above). It is included here for its comparative value in assessing the morphocline polarity of traits among the atelids.
2.3.2
Body Size
Body size deserves special mention here and we consider it separately from the rest
of the character analysis for reasons given above. We provide a series of alternative
weight estimates for the fossils based on regressions using different taxonomic samples of anthropoids and different independent variables, both dental and cranial
(Conroy 1987; Kay et al. 1998; Sears et al. 2008) (Fig. 2.6). We caution, however,
that difficulties remain and, as indicated above, the postcranial skeleton may be
more suitable for estimating body size in Protopithecus and Caipora (Halenar
2011a, b). Some equations using skulls have relatively low R2 values so they cannot
be considered highly reliable for projections. While the equations for molars have
R2 values of 0.9 or greater, lower molars are missing from Protopithecus. Caipora,
which is probably a frugivore, may also have relatively small teeth, which may bias
a molar-based weight estimation. Nevertheless, in our analysis Stirtonia and
Paralouatta fall within the range of modern howler monkeys in body mass, as does
Solimoea. As noted, new body mass estimates for Protopithecus and Caipora were
deemed necessary as the original estimates were calculated from regression equations based on a catarrhine reference sample (Hartwig 1995; Cartelle and Hartwig
1996; Hartwig and Cartelle 1996). Alternative regression equations to estimate size
were calculated using a sample of primates encompassing a wide range of body
sizes and locomotor patterns (for sample composition see Halenar 2011a, b). For
this exercise, the centroid sizes of the epiphyses of various long bones were
employed as the skeletal estimator and equations were generated based on the entire
32
A.L. Rosenberger et al.
Fig. 2.6 Male and female body weights as reported in the literature for the living atelids (DiFiore
and Campbell 2007) and their fossil relatives, the latter based on tooth and/or skull measurements.
Weights for Stirtonia and Paralouatta are from Fleagle (1999) and MacPhee and Meldrum (2006),
respectively. For other fossil species, including Paralouatta for which additional estimates are
included, weights were calculated using the monkey, anthropoid, all primate, and female anthropoid regression equations of Conroy (1987) and the female platyrrhine equation of Kay et al.
(1998). Body size estimates based on skull length and bizygomatic width were derived from Sears
et al. (2008) equations. The highs and lows are shown instead of averages to demonstrate the wide
and overlapping range of body sizes seen in the living atelids, making body mass a difficult character to code and interpret via character analysis. Estimates based on cranial measures are deemed
less reliable because of low coefficients of determination (R2) in the original regressions. Body
mass estimates for Protopithecus and Caipora using craniodental measures are substantially below
previous reports, but the original estimates of 20–25 kg are confirmed based on postcranial regression equations (Halenar 2011a)
sample, the platyrrhines only, and the atelids only. Three aspects of “body size”
were predicted for the fossil: body weight (kg), total length (TOTL; mm) which
includes the length of the tail (TAILL), and trunk length, head, and body (TrL; mm)
which includes the length of the skull and trunk (TOTL = TAILL + TrL; Ford and
Corruccini 1985). A relatively wide range of body size estimates was thus recovered
for Protopithecus: 12–35 kg, 1,479–1,887 mm TOTL, and 613–831 mm TrL. This
range reflects the use of different skeletal elements, reference samples, and regression models. The equation with the combined highest R2 (=0.98), lowest %SEE
(=11.0), MPE (=14.7), and QMLE (=1.005) is that which uses the distal humerus
with a platyrrhine-only reference sample; this gives an estimate of 28 kg for the
more recently discovered specimen from Toca da Boa Vista and 24 kg for the original specimen discovered by Lund in Lagoa Santa. Condensing all of the estimates
into an average, disregarding the obvious extreme outliers in estimate and confidence statistics, gives a body weight of approximately 23 kg, 1,675 mm TOTL, and
710 mm TrL. As an alternative to compiling an average value, a histogram of all
2
Evolution of Alouattines
33
body weight predictions shows 19, 21, and 25 kg as the most frequent estimates
with a reasonable range from 17 to 29 kg. This puts Protopithecus in the size range
of a large male baboon or proboscis monkey and confirms its place in a large-bodied
category that no longer exists among extant platyrrhines.
For simplicity, and taking into account the considerations discussed above, within
atelids we code the range of character states (Table 2.2) describing body mass at the
generic level as medium and large, choosing these terms in part as a semantic device
to distinguish them from other platyrrhines often regarded as being middling in size
for the radiation, e.g., pitheciids and Cebus (e.g., Hershkovitz 1977). We recognize
this grossly underrepresents intrageneric diversity (and likely selection for body
mass at the species level) and especially the nature and complex distribution of
sexual dimorphism among atelids. But it is a useful, operational approximation considering the foci of this study, fossils and genus-level systematics.
2.3.3
Character Analysis
Table 2.2 also summarizes the taxonomic distribution of the ten features we assess
in detail. As mentioned, the major reasons for selecting these are that they tend to
diagnose Alouatta as a genus, defining it morphologically, phylogenetically, and
adaptively relative to other living NWM, and they are well represented in the cranial
remains of three fossil genera. The fourth, Solimoea, is obviously an exception.
2.3.3.1
Facial Proportions
Rosenberger (1992) and Rosenberger and Strier (1989) suggested that the Lagothrixlike condition of the facial skeleton, here termed “moderately large”, is ancestral
overall for atelids (Figs. 2.3 and 2.4). This was based, in part, on the interpretation
that there are two other extremes in the atelid morphocline, exemplified by the
Ateles and the Alouatta poles, each one highly likely to be derived since they are
associated functionally with novel adaptations. In Ateles, ripe fruit frugivory is
linked with reduction of the cheek teeth, well-developed anterior teeth (e.g.,
Rosenberger 1992; Anthony and Kay 1993), and a small face. This pattern occurs in
Caipora as well. In Alouatta, massive changes in the placement and orientation of
the large facial skeleton are associated with specializations of the cranial base
related to extreme enlargement of the hyoid and the production of stentorian vocalizations (see Biegert 1963). Cheek teeth are also relatively large and anterior teeth
are proportionately small (e.g., Rosenberger 1992; Anthony and Kay 1993).
Regarding the fossils, we interpret the face of Protopithecus as moderately large,
hence similar to the condition seen in Lagothrix, although more work needs to be
done on the allometry of this region in the large-bodied fossil. Paralouatta, however, clearly does have a relatively large, long face resembling Alouatta in its proportions. Of the fossils under consideration, it is most comparable to Alouatta with
a markedly prognathic snout, but similar prognathism is also evident in Protopithecus.
Table 2.2 Character-analysis distributions
Body size
1. Facial
proportions
2. Craniofacial
haft
3. Postorbital
constriction
4. Cranial
crests
5. Nuchal
plane
6. Foramen
magnum
7. Brain size
and shape
8. Basicranial
shape
9. Incisor
proportions
10. Molar relief
and crown
shape
Atelid
morphotype
Medium
Moderately
large
Nonairorhynchous
Moderate
Ateline
morphotype
Medium
Moderately
large
Nonairorhynchous
Moderate
Moderate lines
Caipora
Large
Small
Alouattine
morphotype
Medium
Large
Nonairorhynchous
Moderate
Airorhynchous
Protopithecus
Large
Moderately
large
Airorhynchous
Paralouatta
Medium
Large
Solimoea
Medium
NA
Stirtonia
Medium
NA
Alouatta
Medium
Large
Airorhynchous
NA
NA
Airorhynchous
Marked
Marked
Marked
NA
NA
Marked
Moderate lines
Reduced lines
Marked lines
NA
Flat,
unreduced,
subvertical
Unreduced,
posterior
Unreduced,
non-cylindrical
Not elongate
Rounded,
unreduced
NA
NA
Marked lines,
compound
crests
Flat, reduced,
vertical
Unreduced,
posterior
? Enlarged,
globular
Short
Flat,
unreduced,
subvertical
Reduced, far
posterior
Reduced,
non-cylindrical
Elongate
Marked lines,
compound
crests
Flat, reduced,
subvertical
NA
Flat,
unreduced,
subvertical
Unreduced,
posterior
Unreduced,
non-cylindrical
Not elongate
Marked lines,
compound
crests
Flat, enlarged,
subvertical
Reduced, far
posterior
Reduced,
cylindrical
Elongate
Reduced, far
posterior
Reduced,
cylindrical
Elongate
NA
NA
NA
NA
NA
NA
Reduced, far
posterior
Reduced,
cylindrical
Elongate
Intermediate
? Intermediate
Enlarged
Intermediate
Enlarged
? Intermediate
NA
? Reduced
Reduced
Intermediate
Intermediate
Reduced
relief, short
Cristodont,
elongate
Cristodont
Moderately
cristodont,
elongate
? Cristodont,
elongate
Cristodont, Cristodont,
elongate
elongate
The atelid morphotype conditions generally reflect the states evident in non-atelid platyrrhines, which we consulted as a collective out-group. No transformations are inferred
for the ateline morphotype. See text for explanations regarding the questionable character states for incisor proportions and molar relief in the fossil taxa
2
Evolution of Alouattines
2.3.3.2
35
Craniofacial Haft
A feature correlated with facial size and prognathism is the orientation of the face
relative to the braincase. Alouatta, is unusual and highly derived among platyrrhines
in having an uptilted rostrum, a condition known as airorhynchy (Figs. 2.3 and 2.4).
This design contributes to the expansion of space in the neck for the permanently
inflated air sacs inside the hollowed-out hyoid bone and its associated cartilages.
Airorhynchy is also linked functionally with elongation of the cranial base (see
below). Paralouatta closely resembles Alouatta in this respect, although the dorsal
tilt of the face seems to be less exaggerated. Even though the tip of the fossil’s snout
is broken near the level of the canines, it is evident that the toothrow is nearly as
arched in lateral view, forming an exaggerated curve of Spee. Protopithecus has a
modestly uptilted face as well. The rostra of other platyrrhines are constructed differently and are generally non-airorhynchous, as in Caipora. The lateral profile of
the Brachyteles dental arcade, with large postcanine teeth and a moderately deep but
non-prognathic face, is slightly curved upward anteriorly.
2.3.3.3
Postorbital Constriction
The degree of postorbital constriction is influenced by braincase size and shape,
craniofacial proportions, and the anteroposterior alignment of the face at the craniofacial junction (Fig. 2.3). The modern alouattines and atelines present contrasting
character states. The constriction is moderate in atelines, including Caipora, but it
is marked (i.e., narrow or waisted) in Alouatta. In atelines such as Ateles and
Brachyteles, with retracted, subcerebral (below the horizontal axis of the brain)
faces and large, relatively globular braincases, width at the craniofacial junction is
not constricted. But even in Lagothrix, where the braincase is not globular, the constriction is unimpressive, as it tends to be in other platyrrhines, suggesting that this
state is ancestral in atelids. In Alouatta, in contrast, the combination of a precerebral, uptilted face, massive width of the posterior face, and narrow braincase produces the markedly constricted effect. In ventral view (Fig. 2.4), Paralouatta
resembles howler monkeys in these factors. The same is evident in Protopithecus,
but it manifests differently because the braincase is quite wide posteriorly, owing
largely to well-developed exocranial superstructures.
2.3.3.4
Cranial Crests
The development of exocranial temporal lines and nuchal crests may be strongly
influenced by size, age, gender, and sexual dimorphism, indicating caution in making comparisons without population samples of fossil atelids (Figs. 2.3 and 2.5).
Of the fossil specimens considered here, Caipora is a young adult; Protopithecus is
an adult but with relatively unworn teeth; Paralouatta is an adult with advanced
postcanine tooth wear. Judging by canine prominence, anterior premolar size,
and the known level of sexual dimorphism in the living species, Caipora and
A.L. Rosenberger et al.
36
Protopithecus appear to be males. The canine crowns of Paralouatta are broken
away, but the expression of cranial crests suggests the skull may also be male.
Among modern atelids, moderate to prominent temporal lines, evenly developed
anteriorly and posteriorly, are present in Lagothrix, Brachyteles, and Alouatta.
Strong nuchal lines or crests tend to occur in the robust Alouatta males and are quite
common interspecifically. Neither temporal lines nor nuchal crests are welldeveloped in Ateles, or in Caipora, which corresponds with their reduced cheek
teeth and rounded, large braincases, among other factors. We surmise this is a correlate of the soft/ripe-frugivory feeding complex seen in Ateles. It is also related to
what may be termed a semi-orthograde head carriage, i.e., the head is not strongly
cantilevered off the vertebral column but tends to rest atop the cervical vertebrae in
compliance with tail-assisted climbing and other semi-orthograde positional
behaviors.
With a small braincase and large temporal and nuchal muscles, a compound
temporo-nuchal crest is well-developed in Alouatta, although its distribution among
the modern species has not been mapped out. Nevertheless, in the larger and more
robust males, laterally away from the midline, the temporal enthuses fuse with the
nuchal line to form a raised lateral margin of the nuchal region. By comparison with
other atelids, these features are extremely well-developed in Protopithecus, probably as an elaboration of an Alouatta-like pattern exaggerated by the allometrics of a
very large body size. The compound temporo-nuchal crest is present also in
Paralouatta but exhibited less dramatically, comparing more favorably with the
variations seen in Alouatta.
2.3.3.5
Nuchal Plane
Alouatta is unusual among platyrrhines in having a nuchal plane that is flat, often
rugose in texture, reduced in size, vertically oriented (Fig. 2.5), and exhibiting a
semicircular dorsal perimeter when viewed from behind—all features corresponding with the cylindrical shape of the braincase and pronounced set of muscle attachments on the occiput. Sex differences exist, but this overall gestalt is fixed in howler
monkeys. It relates to head carriage and craniofacial mass. The foramen magnum
and occipital condyles are directed posteriorly rather than ventrally as in other
NWM, meaning that the large, heavy head of Alouatta, which is eccentrically loaded
up front due to its snouty prognathic design, tends to be extended dog- or lemur-like
out from the shoulders and neck, in typical pronograde fashion. The flat, vertical
nuchal plane presumably gives the trapezius and other neck muscles apt mechanical
advantage in supporting the horizontally disposed skull. Following previous arguments, we regard the Lagothrix-like condition, a relatively flat, subvertical, and
unreduced nuchal plane as ancestral in atelids. The contrasting rounded and unreduced morphology of Ateles and Caipora is considered derived for atelines.
Paralouatta resembles Alouatta generally, but the plane of the nuchal region appears
to be more primitive, slanted in a manner that compares with Lagothrix. Similarly,
Protopithecus retains an inclined nuchal plane but it is also greatly expanded laterally, owing to the hypertrophic compound temporo-nuchal crests. We hypothesize that
2
Evolution of Alouattines
37
this is at least partly an allometric contingency but it may also reflect differences in
the proportions of the jaw adductor muscles. The apparent lack of gonial expansion
in comparison to Alouatta suggests that Protopithecus had a less elaborate masseter
complex, while the enlarged temporo-nuchal crests suggest the posterior part of the
temporalis muscle was exaggerated instead.
2.3.3.6
Foramen Magnum
Both the position (see Schultz 1955) and relative size of the foramen magnum
differs among atelids. These features are related to head posture and endocranial
volume. As indicated, it is extremely posteriorly positioned in Alouatta, Paralouatta,
and Protopithecus, especially so in howler monkeys (Fig. 2.4), and the particulars
conform to the degree of nuchal plane modifications in these genera. Alouatta
exhibits the most derived pattern. The more anterior location of the foramen magnum in atelines is consistent with the more common location documented by
Schultz, which is ancestral for NWMs and atelines. For convenience we code it as
posterior, offsetting it from the condition in Saimiri and Cebus. They have foramina
magna that are distinctly more “centrally” located within the long axis of the skull.
The foramen magnum also varies in proportions, with atelines and alouattines
clearly having different scaling patterns (Fig. 2.7a). Relative to basicranial length,
foramen magnum area (length × breadth) is small in Alouatta, Paralouatta, and
Protopithecus, falling well below the scatter of points and the regression line representing modern atelines and Caipora. The size of the foramen is also closely correlated with endocranial volume across primates (e.g., Jerison 1973; Martin 1990).
Brain size is relatively larger in atelines than alouattines (Fig. 2.7b), which helps
explain why the foramen magnum is proportionately smaller in the latter. Again, the
alouattine condition is very likely the derived pattern among atelids, given the rarity
of de-encephalization, which is often associated in mammals with herbivory or folivory (see section below for an expanded explanation). But it is also possible that to
some degree, relatively small brain size in this group reflects primitive platyrrhine
proportions. The status of atelines also requires further examination. While Ateles
and Brachyteles have been singled out as having derived, elevated relative brain
sizes (Cole 1995, in Hartwig 2005), it appears from this assessment that all the
atelines, including Lagothrix and Caipora, jointly share this pattern. Even
Brachyteles, a genus that might be expected to have experienced selection for a
reduced relative brain size as a correlate to its more leafy diet, follows the ateline
pattern and is relatively larger-brained than any alouattine (Rosenberger et al. 2011).
2.3.3.7
Brain Size and Shape
As indicated, among modern platyrrhines, it is well established that howler monkeys
have an unusually small brain size relative to body mass (e.g., Stephan and Andy 1964;
Hershkovitz 1970; Stephan 1972; Clutton-Brock and Harvey 1980; Eisenberg 1981;
Martin 1984, 1990; Hartwig 1996), and this likely represents, at least in part, an
38
A.L. Rosenberger et al.
Fig. 2.7 Bivariate plots of (a) foramen magnum area and (b) endocranial volume relative to
nasion-basion length in atelids. Note the separate distributions of the atelines, including Caipora,
toward the top of the graph and the alouattines, including Protopithecus and Paralouatta, toward
the bottom. Data points for the living genera are sex-pooled means from the following samples:
Brachyteles arachnoides, 3; Ateles belzebuth, 16; Lagothrix lagotricha, 15; Alouatta belzebuth, 16.
Alouattines have relatively smaller brains, even the frugivorous Protopithecus, while the leaf-eating ateline Brachyteles does not have a reduced brain size
2
Evolution of Alouattines
39
adaptation to folivory (e.g., Clutton-Brock and Harvey 1980; Eisenberg 1981; Martin
1984, 1990; Harvey and Clutton-Brock 1985; Rosenberger et al. 2011). Since folivory
is clearly a derived habit among NWM, the correlative, relatively small Alouatta brain
may have evolved via de-encephalization. This does not, however, mean there is no
component of primitiveness in this character state, for early platyrrhines probably had
smaller brain sizes than modern members (see Tejedor et al. 2006; Sears et al. 2008),
parallel increases in relative brain size occurred, and basal lineages of the major clades
may logically be expected to retain the primitive platyrrhine condition (see Hartwig
et al. 2011).
The conjunction of a relatively small brain in howler monkeys with a posteriorly
positioned foramen magnum, small nuchal plane, extended basicranial platform, and
precerebral, airorhynchous face makes it likely that the cylindrical shape of the
Alouatta braincase is a derived by-product of a spatial packaging phenomenon (i.e.,
Biegert 1963; Gould 1977; Ross and Ravosa 1993). The Protopithecus skull closely
resembles Alouatta in this respect although its braincase differs in shape for it is
wider posteriorly than anteriorly, a pattern not seen elsewhere among platyrrhines.
However, some of this is an exocranial effect of the very wide nuchal plane, with
well-developed lateral nuchal crests and a massive set of temporal roots supporting
the zygomatic arches. The finding of Krupp et al. (2012) that the Protopithecus brain
resembles Alouatta in overall shape helps explain why Protopithecus cannot share
the globular braincase shape of Ateles, Brachyteles, and Caipora, all at the opposite
end of the spectrum. Roughly speaking, the Protopithecus braincase may more
closely resemble Lagothrix, whose morphology may be described as non-cylindrical
for convenience. This would suggest it shares the ancestral condition for atelids.
2.3.3.8
Basicranial Shape
Alouatta is unusual among platyrrhines and other primates in having an elongate
basicranium (Fig. 2.4), presumably as another derived correlate of subbasal spatial
packaging, i.e., making room for the enlarged hyoid complex (Biegert 1963).
However, it should be noted that within Alouatta, there is considerable interspecific
variation in cranial base shape, with A. palliata showing a shorter, more rounded
condition (Halenar 2008). A. seniculus males appear to be the most exaggerated,
perhaps because the foramen magnum is shifted posteriorly to such an extreme
degree. We designate the contrasting character states of Ateles and Caipora as short,
but their modified, encephalized skulls suggest this may not be the ancestral atelid
or ateline condition. We hypothesize that the deeper morphotype condition is more
moderate and designate the primitive condition as “not elongate.” Hartwig and
Cartelle (1996) pointed out that the Alouatta-like elongate pattern is evident in
Protopithecus, and it is exhibited in Paralouatta as well (Rivero and Arredondo
1991; Halenar 2012). We consider the Protopithecus morphology less derived than
in Alouatta and Paralouatta, largely because the nuchal plane continues to extend
behind it. In agreement with many of the qualitative statements made above regarding facial proportions and airorynchy, 3D geometric morphometric analysis of the
A.L. Rosenberger et al.
40
Fig. 2.8 The index of lower incisor size was calculated by dividing the incisal crown crosssectional area (length × breadth of i1) by first molar area (length × breadth). This exercise was
repeated for maxillary and mandibular first molars so as to be able to include both Paralouatta and
Protopithecus. Lower values, which indicate relatively small incisors, correspond with a more
folivorous diet, as in Alouatta. The position of Protopithecus toward the higher end of the
scale, with an index proportionately twice the size of Alouatta, suggests it was considerably
frugivorous
Protopithecus cranial base suggests that it exhibits an intermediate morphology
between the extremely derived Alouatta and Ateles conditions; principal components analysis aligns the fossil with extant Lagothrix in terms of its degree of basicranial elongation and flexion (Halenar 2012).
2.3.3.9
Incisor Proportions
Morphologically, the incisors of atelids appear to show an acute sensitivity to
selection reflecting critical dietary preferences (Fig. 2.8). Thus, Alouatta and Brachyteles, the most folivorous platyrrhines, have evolved relatively small-crowned incisors, probably independently (Eaglen 1984; Rosenberger 1992; Anthony and Kay
1993), whereas the other atelids have relatively larger incisors with the lower incisors being distinctly spatulate in shape. Reduced crowns like those of Alouatta and
Brachyteles are not prevalent among other platyrrhines, making it likely that the
unreduced condition is ancestral for atelids. The much enlarged incisors of Ateles
and Lagothrix may be another specialization related to intensive fruit harvesting
behaviors. This makes it difficult to specify the morphotype ateline condition.
By default, we regard it as being intermediate. Importantly, the proportions of
Paralouatta more closely resemble the condition seen in Alouatta and Brachyteles
2
Evolution of Alouattines
41
than Protopithecus or any modern atelines. Protopithecus incisors are quite large
proportionately, although not to the extent seen in Ateles and Lagothrix. Stirtonia
specimens lack incisors, but the well-preserved-type mandible of S. tatacoensis has
canines positioned relatively close together, suggesting these teeth were not especially enlarged.
2.3.3.10
Molar Relief and Crown Shape
Taking a very abstract approach in order to characterize the morphology of upper and
lower molars simultaneously, we define two crown patterns as character states: “low
relief”, with relatively low cusps and shallow, broad basins, and, “cristodont”, having
more relief and an emphasis on relatively elevated cusps and lengthy crests, which
thus restricts lower molar basins and lengthens the crown (Figs. 2.1 and 2.2). Alouatta
is the archetypical example of the cristodont pattern with upper molars also exhibiting a set of strongly developed buccal ectoloph crests (especially the centrocrista
between paracone and metacone) as well as a stylar region with a robust buccal
cingulum, which is associated with localized crest development. Brachyteles (see
Rosenberger 1992) shares several features of the cristodont pattern with Alouatta but
appears to have evolved aspects of it by a different, convergent pathway emphasizing
lingual, as opposed to buccal, shear. Hence, the massively developed metaconids and
entoconids seen in Brachyteles molars (Fig. 2.2).
Among platyrrhines, cristodont molars like those of Alouatta and Brachyteles
do not occur outside of the atelids, so it is reasonable to regard this state as derived
(in parallel). The low-relief pattern of Ateles and Lagothrix is also part of an unusual,
large-basin occlusal morphology among NWMs, functionally related to masticating
soft, ripe fruit (Kay 1975; Rosenberger 1992; Anthony and Kay 1993). Hence, we
interpret both patterns as derived from a still hypothetical architecture we term
“intermediate” for convenience. Among the fossils, Paralouatta upper molars
(Fig. 2.1) clearly share with Alouatta well-developed buccal and stylar cristodont
features, but the crown is more primitive lingually, retaining the well-differentiated
hypocone, for example, that is broadly similar to many living NWM and middle
Miocene fossils. The Paralouatta cusps and crests also tend to be more blunted than
sharp. The morphology of Protopithecus is poorly known since the specimen lacks
lower molars and the single M1 is broken; however, it evidently does not display the
cristodont pattern. The occlusal surface of the upper molar appears to be relatively
flat and the premolar cusps are bulbous. Both species of Stirtonia have very Alouattalike, cristodont upper molars. Caipora exhibits an ateline-like, low-relief pattern.
The cross-sectional crown shape of lower molars also tends to distinguish most
atelines from alouattines (Fig. 2.9). All alouattines have relatively long first lower
molars. Length exceeds breadth by approximately 25 % or more. Here, again,
Brachyteles converges on Alouatta, Stirtonia, Paralouatta, and Solimoea, while Caipora
is an outlier among atelines. Other modern NWMs tend to have proportions similar to
living atelines. First molars of species of Aotus, Callicebus, Pithecia, and Cebus, for
example, have length/breadth ratios of 1.0–1.1 (Fig. 2.9). The overall functional
42
A.L. Rosenberger et al.
continuity of this aspect with others that are part of the cristodont molar pattern
indicates that elongation is a homologously derived element of crown design in alouattines, probably related to maximizing the linear length of shearing blades.
2.4
2.4.1
Discussion
Implications: Taxonomic Composition of the Fossil
Alouattines and the Problem of Solimoea
The status of two of the three fossils at the focus of our character analysis has not been
challenged. Stirtonia and Protopithecus present a robust, persuasive series of craniodental features tying them to Alouatta. There are also several postcranial features of
the hip and thigh that may link Protopithecus and Alouatta (Halenar 2012). The affinities of Paralouatta have been debated (Rivero and Arredondo 1991; Horovitz and
MacPhee 1999; Rosenberger 2002). As evident above, we have proceeded with the
working hypothesis that the Cuban genus is an alouattine and refer readers elsewhere
(Rosenberger 2002; Rosenberger et al. 2008) for arguments countering the notion that
Paralouatta is a member of a monophyletic Caribbean group most closely affiliated
with Callicebus. In nine of ten cranial features assessed here, Paralouatta shares
the same derived state with Alouatta (Table 2.2). In two characters Paralouatta is “one
step” less derived. In no cases are there any phenetic discrepancies to challenge the
notion that these individual, intercorrelated elements are not homologous or functionally contrastive. We thus conclude that Paralouatta is a well-established alouattine.
The other species requiring attention is Solimoea acrensis. Kay and Cozzuol (2006)
maintain that Solimoea acrensis is a stem ateline. The claim is based on a cladistic
analysis using PAUP (Swofford 2002) of the two specimens they allocate to the taxon,
an isolated lower molar inferred to be m1, the type specimen, and a referred maxillary
fragment with P3–4, which is in poor condition. It is important to note that the Kay and
Cozzuol (2006) analysis is not an independent assessment of morphological evolution
among atelids because it is based on the “molecular scaffold” approach. In other
words, the results of a molecular study were first used to arrange the topology of the
tree. Then PAUP mapped characters onto the tree to produce the most economical
distribution of states among the taxa.
We do not find the arguments compelling and suggest, alternatively, that Solimoea
is an alouattine. There are major concerns that raise questions and warrant discussion:
(1) the existence of distinctive phenetic similarities as well as a unique constellation
of derived features shared by the type of Solimoea and alouattines, exclusively, and
(2) Kay and Cozzuol’s reliance on characters from the maxillary specimen which
may, in fact, not belong to the same taxon as the type.
The small-basin crown morphology of the type lower molar is far more similar
to an alouattine than any of the wide-basined, extant atelines (Fig. 2.2). While
Solimoea exhibits a crown pattern that appears to be less modified than the highly
2
Evolution of Alouattines
43
Fig. 2.9 Length breadth ratio (length/breadth) of m1 in selected platyrrhine species. Higher values
indicate relatively longer and narrower teeth, a correlate of lengthened shearing blades, and are a
derived feature associated with the alouattine clade and, independently, the semi-folivorous
species Brachyteles. The crown morphology and length: breadth ratio of Solimoea aligns it with
alouattines
distinctive Stirtonia and Alouatta, it conforms to expectations of the alouattine
morphotype. This configuration appears to be derived for atelids, based on character
analysis and, especially, the expanded sense of alouattine diversity that is informed
by taking Paralouatta into account. Solimoea shares with Alouatta and Stirtonia a
morphological combination not seen elsewhere among NWM: (a) abbreviated,
mesially narrowing, elevated trigonid and low, elongate, basined talonid; (b)
obliquely oriented postvallid; (c) sharply angled cristid obliqua, forming a prominent ectoflexid; and (d) relatively long and narrow crown shape (Fig. 2.9). Buccally,
the Solimoea lower molar also exhibits a resemblance to Paralouatta, whose
maxillary molars demonstrate a primitive version of Alouatta-like ectoloph features
as noted above. This is consistent with the Solimoea lower molar simply being more
primitive, i.e., less of a “shearing folivore,” than the highly committed leaf-eaters
Alouatta and Stirtonia. This functional and dietary inference is a conclusion also
reached by Kay and Cozzuol (2006) based on quantification of shearing potential.
Concerning resemblances between Solimoea and the ateline Brachyteles, some are
evident in the angularity of the buccal aspect of the crown. However, this is probably partly due to primitiveness as well as a joint emphasis on shearing features.
The allocation of the maxillary specimen to the taxon is not convincing, for it is
by no means evident that it is associated with the type lower molar. While there is a
general conformity in the sizes of the lower molar and the upper premolars and they
were recovered from the same locality, it would not be unusual for there to be several sympatric primate species and genera of similar size at an Amazonian locale (in
this regard we note with interest that the gigantic Protopithecus and Caipora were
44
A.L. Rosenberger et al.
found almost side by side in a cave, but their taphonomic histories remain a mystery).
Kay and Cozzuol (2006) justify this allocation quantitatively, referencing the proportions of the crown areas (length × breadth) of the two specimens. They present a
bivariate plot of m1 area vs. P4 area (Fig. 5, p. 677) based on a series of 13 Lagothrix
lagotricha specimens and note that the plot point for the paired set of Acre fossils
falls within the minimum convex polygon that bounds the distribution. We replicated and extended this exercise (Fig. 2.10) but arrive at a different conclusion.
In our larger sample population of L. lagotricha, when jointly plotted the Acre
specimens (termed Solimoea acrensis in the figure) do not lie within the polygon.
It is also evident there is considerable overlap in the size relationships of m1 and P4
among species and genera of platyrrhines across a broad spectrum of body sizes at
the 95 % confidence limits of populations, which undermines the taxonomic usefulness of this criterion (Fig. 2.10). The ellipses show that if the corresponding upper
and lower teeth of most Brachyteles and Alouatta, or of most Ateles, Lagothrix, and
Cebus, for example, were potted interchangeably by permutation, there would be no
way of distinguishing or sorting confidently any individual tooth or tooth set to a
species. Furthermore, our sample of howler monkeys uses A. seniculus only. If a
smaller species was included in this case study, incidental sampling bias may even
confound the metric associations of as many as six genera, Alouatta, Brachyteles,
Ateles, Lagothrix, Cebus, and Solimoea.
In essence, the preserved morphology of the upper premolars is insufficient to properly test for an occlusal match with the lower molar, and compatibility in size is of little
consequence. The premolars appear to be bunodont, rectangular, and of low relief,
with large lingual occlusal surfaces, which is inconsistent with the non-bunodont,
moderately high-relief morphology of the lower molar or with the latter’s abbreviated,
oblique trigonid. It appears to us that these teeth may be mismatched taxonomically
and, if so, this negates their utility in the generic diagnosis and cladistic analysis.
2.4.2
Interrelationships, Craniodental Morphology,
and Adaptations of Fossil Alouattines
The cladistic interrelationships derived from our character analysis are summarized
in Fig. 2.11. Our overall results continue to support prior arguments that Stirtonia is
the fossil most closely related to Alouatta. For example, the upper molar morphology
of Paralouatta tends to reinforce the Alouatta-Stirtonia linkage by default because
the Cuban form’s crowns are blunter, but its upper molars present a W-shaped ectoloph and moderately well-developed stylar elements, structural features that eventually became trenchant shearing surfaces in Alouatta and Stirtonia. The lingual aspect
of Paralouatta upper molars also had not yet developed the sharp, lobe-like hypocone, which is prominent in Alouatta and Stirtonia.
With a cylindrical braincase and constricted nuchal region, synapomorphies
shared with Alouatta but combinatorially absent in Protopithecus, Paralouatta is
not only more derived than Protopithecus in the direction of Alouatta. It also bears
2
Evolution of Alouattines
45
Fig. 2.10 Bivariate plot of m1 area (length × breadth) vs. P4 area (length × breadth) in selected
platyrrhine species. A mixed species sample was used for Aotus, Cacajoa, and Chiropotes, including: A. vociferans, A. lemurinus, A. infulatus, A. nigriceps, A. trivirgatus, and A. brumbacki;
Chiropotes albinasus and C. satans; and Cacajao calvus and C. melanocephalus. Mixed species
samples were included to increase sample size and were only marginally more variable than
single-species samples for this measure. Minimal convex polygons are shown in the main body of
the figure and the inset shows 95 % confidence intervals. Solimoea is identified by an enlarged
black dot in the inset. The multiple taxonomically overlapping proportions of these teeth across the
range of sizes exhibited by platyrrhine species and genera, some of which can occur sympatrically,
means that such size associations are not reliable as taxonomic identifiers in fossil assemblages
like the Rio Acre sample involving Solimoea
a distinctly closer phenetic resemblance to howler monkeys. This offsets
Protopithecus as a basal member of the alouattine clade given what we know currently of their diversity. In the basicranium as well, Protopithecus appears to exhibit
the ancestral end of the alouattine morphocline while Alouatta and Paralouatta
occupy the opposite pole. Equally important, Protopithecus has a very different
dental gestalt, lacking both the reduced incisors of Alouatta and Paralouatta and a
cristodont molar pattern as seen in Alouatta. Among all the fossils, Protopithecus
retains the largest combination of dental and cranial features consistent with the
alouattine morphotype. In a general way, the morphological pattern is concordant
with Rosenberger and Strier’s (1989) proposal of a Lagothrix-like craniodental
morphology being ancestral for alouattines and atelines.
46
A.L. Rosenberger et al.
Fig. 2.11 Cladogram showing the proposed interrelationships of alouattine platyrrhines. Dotted
lines indicate all possible positions for Solimoea. Images are for illustrative purposes and are not
shown to scale
Based on one lower molar, the position of Solimoea is still difficult to fix.
The shape of this tooth does not conform to the apparently open-basin crown morphology of the damaged Protopithecus upper molar (or with the bunodont pattern of
existing lower premolars). Its small-basin design is not consistent with the advanced
atelines, Lagothrix and Ateles. Resemblances to Brachyteles are confined to the
more primitive buccal aspect of the crowns, and this generalized angularity of shape
is also shared with alouattines. Solimoea most closely resembles Alouatta and
Stirtonia overall. The buccally flaring, elevated protoconid; strongly angled preand post-hypoconid cristae; and strong trigonid-talonid height differential appear to
be a derived combination that would facilitate folivory through selection for additional or more efficient shearing.
Cranially, both Protopithecus and Paralouatta present a mixture of features
resembling the unique patterns exhibited by Alouatta in areas of the basicranium and
nuchal region, overall braincase shape, and facial structure. The more detailed
resemblances shared by Paralouatta and Alouatta imply an important functional
overlap that appears to be related to a novel organization of the skull. These probably
relate to fixation of an enlarged hyolaryngeal mechanism in the neck between the
rami of the mandible and to a large, cantilevered head. The general organization of
Protopithecus clearly indicates a shift from a more general, Lagothrix-like pattern in
the Paralouatta-Alouatta direction.
An unexpected outcome of this study involves two related indicators of relative
brain size, endocranial volume and foramen magnum area. The same reduced
2
Evolution of Alouattines
47
scaling conditions were observed among all alouattines known from cranial material
but not in any of the atelines, not even the one genus with a pervasive tendency to
eat leaves, Brachyteles. As noted previously, the relatively small brain size in
Alouatta has been regarded as part of its folivorous feeding adaptation, so its occurrence in Protopithecus, with a decidedly frugivorous dentition, is thus counterintuitive. Noteworthy is a recent study (Krupp et al. 2012) that independently confirms
the relatively small size of the Protopithecus brain and demonstrates, via an endocranial cast, its Alouatta-like shape and surface morphology. Given that the
Protopithecus dentition is not howler monkey-like, these findings are consistent
with the hypothesis that the shift toward folivory in Alouatta may have been predicated on an earlier reliance on seeds (Rosenberger et al. 2011). This initial dependence on seeds could have benefitted from similar energy-saving features like small
brains (Rosenberger et al. 2011), if selection for large brains (possibly driven by
features such as functional association with a large, complex social organization)
was absent. If correct, the comparable small brains of Protopithecus, Paralouatta,
and Alouatta more likely reflect a derived de-encephalization than a primitively
atelid small-brain pattern, though parceling out these historical factors remains a
difficult proposition as we noted above.
Of the three fossil genera, only Stirtonia, the howler monkey’s closest relative
known thus far, can be considered a comparably committed leaf-eater by the detailed
functional similarities shared with Alouatta in molar morphology and by its inferred
body mass. The cheek teeth of Paralouatta are more bunodont and given to wearing
more flatly, contrasting with Alouatta, which exposes lines of dentine along the
crown perimeter and stems from a thin-enamel occlusal design that emphasizes and
maintains shearing. Thus is it likely that Paralouatta molars are not designed optimally for shredding leaves.
Upper molars of Protopithecus lack crested shearing perimeter lines, and the
large-basined crowns do not seem to resemble either the Alouatta-Stirtonia pattern
or the morphology of Paralouatta. The lower premolars are also notably bunodont.
Its incisor teeth are wide, spatulate, and relatively large in cross section, which is
consistent with a generalized frugivory as opposed to pitheciine-like, sclerocarpic
harvesting (Kinzey 1992; Rosenberger 1992). The summed cross-sectional area of
Protopithecus incisors is 82 % of the area of the upper molar. Comparable ratios
for leaf-eating folivores are 41 % in Alouatta seniculus and 46 % for Brachyteles
arachnoides. Thus, one of the three alouattine fossils shows consistently strong
indications of a non-leafy diet in aspects involving both anterior and posterior teeth.
Paralouatta is also suggestive of the same.
2.5
Conclusion
With the addition of fossils, the subfamily Alouattinae now consists of four extinct
genera in addition to Alouatta: Stirtonia, Paralouatta, Protopithecus, and Solimoea.
It understates the case to say that the only extant alouattine is a platyrrhine outlier in
48
A.L. Rosenberger et al.
its morphology, trophic adaptations, and clamorous mode of communicating. But as
the diversity of this group is filled in by the discovery of related fossils, it becomes
apparent that living howler monkeys are also something of an outlier among alouattines as well, for there is more than one “kind” of alouattine. Stirtonia is currently
the howler monkey’s closest relative and its teeth are barely distinguishable from
Alouatta, which suggests a fundamentally similar diet. The other fossils help strip
back the feeding specializations of the Alouatta-Stirtonia group to disclose more
primitive anatomies and different dietary adaptations and thus help close the trophic
gap between alouattines and atelines. The other crucial aspect regarding evolutionary history revealed by the fossils comes from the cranium, which helps trace
another signature adaptation of Alouatta, howling. We arrive at these conclusions
regarding phylogeny, diversity, divergence, and evolutionary adaptation as outcomes reflecting the particular approach used in our analysis.
Confidence that Solimoea is an alouattine is elevated by the observation that its
morphology falls within or along a morphocline that circumscribes the anatomical
patterns of genera whose monophyletic affinities with Alouatta are corroborated
independently by cranial morphology. It is also affirmed by the observation that
what limited functional morphology can be drawn from the Solimoea tooth, i.e., its
inferred mechanical shearing potential, is consistent with the notion that alouattines,
living and extinct, exhibit a range of dental features relating to frugivory-folivory
but that neither of the two most basal genera are projected to be as highly committed
to folivory as are Alouatta and Stirtonia. In other words, the functional morphology
of Solimoea is consistent with models of alouattine evolution, which predict what is
self-evident in the broader context of NWM evolution—alouattines more primitive
than Alouatta would have existed, and they would have exhibited a lesser emphasis
on shearing features. On the other hand, there is nothing in any of the models that
would predict primitive atelines would also resemble alouattines, only that they are
not likely to be comparable to either Ateles or Brachyteles dietarily and morphologically. A Lagothrix-like dentition may still serve adequately as the default model of
a morphotypic ateline dentition (Rosenberger and Strier 1989).
Of the two extinct genera known by cranial remains, the alouattine affinities of
the Brazilian Protopithecus seems well established although there has been debate
about the Cuban Paralouatta (e.g., MacPhee and Horovitz 2002; Rosenberger 2002).
Here, too, functional morphology and a morphoclinal perspective weigh heavily
in favor of Paralouatta being related cladistically to howler monkeys. With
Protopithecus and Alouatta representing the range of alouattine extremes in terms
of cranial character states and patterns, Paralouatta seems comfortably nested near
the middle anatomically but decidedly closer to Alouatta at the more derived end of
the spectrum. The functional explanation we propose as the underlying engine
behind this transformation series relates more to howling adaptations than to mastication and diet. Protopithecus, with its relatively extended basicranium and uptilted
face, exhibits the beginnings of a trend toward a greatly enlarged subbasal space,
and this may represent a primitive version of the architecture supporting an enlarged
hyolaryngeal apparatus. Paralouatta is clearly even more Alouatta-like in this
regard (see also Halenar 2012).
2
Evolution of Alouattines
49
The literature’s essentially unanimous endorsement of the hypothesis that
Stirtonia is an alouattine quite closely related to modern howler monkeys is reinforced by finding that comparable aspects of the molars of Paralouatta (and Solimoea)
are apparently more primitive, while the lesser known dentition of Protopithecus
presents a different anatomical pattern, perhaps closer to atelines and thus possibly
morphotype-like for alouattines. The evidence points strongly to the assessment that
this most basal genus of the clade was decidedly frugivorous.
It is difficult to say how long the alouattine clade has been evolving. Recent
molecular studies vary in their estimates. For example, Opazo et al. (2006) posit the
origins of the clade at 16.75 million years. Schrago (2007) estimates a mean divergence date for Alouatta at 12.4 MA but this involves a broad range of ages, 9.1–18.6
MA. In a narrower study, Hodgson et al. (2009) estimate the divergence of Ateles
relative to non-atelid platyrrhines, thus Alouatta by implication, at 18.0 MA, with a
range of 15.7–21.6 MA. The fossil record offers an indication of a Miocene differentiation as well. There is one report (Tejedor 2002) of possible alouattines existing
in Patagonia in the late-early Miocene, but it is based on meager evidence, isolated
canine teeth showing certain resemblances to Alouatta. This would be a pre-La
Venta occurrence, about four million years prior to Stirtonia victoriae and the
younger S. tatacoensis. The isolated astragalus from Cuba allocated to Paralouatta
marianae is dated stratigraphically to ~17 MA (MacPhee et al. 2003), also antedating La Venta, but the affinities of this bone must be considered tenuous.
What can be said with some confidence is that by La Venta times, ~11–13 MA, and
at the younger Acre site, ~ 8 MA, the modernized members of the Alouatta branch of
the radiation existed, probably as committed howler monkey-like leaf-eaters living in
the formative Amazon basin as this ecological community was being assembled
(Rosenberger et al. 2009). The fossils outside this zone, Paralouatta varonai in Cuba
and Protopithecus brasiliensis in eastern Brazil, shed light in a different direction,
toward the remote origins of Alouatta. Despite the recent geological ages of these two
species, they retain a variety of primitive morphologies and occupy positions on the
alouattine cladogram basal to the differentiation of the Stirtonia-Alouatta lineage.
This means that alouattines branching off before the La Venta horizon and outside of
Amazonia may have been less committed adaptively to masticating leaves, and may
thus come closer to approximating the original adaptive gestalt of the group.
Dentally, the fossils, all relatively large-bodied platyrrhines and all expected to
have used, as atelids, fully prehensile tails, comprise an adaptive radiation of mixed
feeders within the frugivore-folivore spectrum. At least two “stages” in the morphological evolution of the skull that relates to howling can be discerned. Paralouatta
is sufficiently similar to living howler monkeys in the cranial base and occipital
region to suggest the same set of novel specializations were present in terms of the
biological roles of the hyoid complex and occipital region as they relate to vocalization and head carriage. Protopithecus is less advanced in that direction. But it signifies that at the basal branch of the radiation, the alouattine clade had already shifted
toward some semblance of the loud-calling lifestyle of Alouatta before the clade
produced the specialized capacity to harvest and masticate leaves. Long call adaptations
also seem to have preceded the evolution of the howler monkey’s postcranial skeletal
50
A.L. Rosenberger et al.
adaptations (see Hartwig and Cartelle 1996; Jones 2008; Halenar 2011a, b), also
emerging in an alouattine that was more frugivorous, as exemplified by Protopithecus.
As morphologists, we emphasize here that a shift in social behavior, possibly
imprinted on the ancestral cranial morphology of the lineage, may have been instrumental in the successful differentiation of alouattines prior to the evolution of the
modified dental and locomotor adaptations that one might have expected as essential niche characteristics of this radiation.
We have elsewhere suggested (Rosenberger et al. 2009) that the natural history
and biogeography of living Alouatta species, potential pioneers due to their dietary
flexibility, suggests the possibility that the genus arose not in the greater Amazon
basin but elsewhere on the continent in less lush habitats. This idea appears to be
consistent with the interpretations we present here, since two genera more basal to
the Alouatta-Stirtonia clade occur outside Amazonia.
Another important insight is that relatively small brain sizes evolved among
alouattines before their intense dental commitment to leaf-eating. Protopithecus
appears to be a rare example of a small-brained, frugivorous anthropoid. This raises
several interesting questions. Is there an evolutionary link between ostentatious howling, which may well have been part of the Protopithecus repertoire, and relatively
modest brains, perhaps as a morphological constraint on cranial design? Have we
overemphasized the physiological and adaptive connections between small brains
and leaf-eating? Can facultative leaf-eating in a mixed feeder, perhaps enabled by
large body size and concomitantly large guts—Protopithecus may be such an example—form a trophic substrate that would motivate selection for de-encephalization?
Is relative brain size more sensitive to selection supporting folivorous or semi-folivorous diets (Rosenberger et al. 2011), or facultative leaf-eating, than dentition? Could
de-encephalization have evolved as a seed-eating adaptation in the absence of selection for brain size increase? We can only speculate that howling, small brains, and
leaf-eating are interconnected as low-energy balancing factors of potential adaptive
value: long-distance advertisement that requires little movement or exposure, a brain
that can be metabolically maintained relatively cheaply, and a food source that
requires little exercise to acquire and produces energy slowly and at low dosages.
These characteristics aptly describe facets central to the howler monkey lifestyle, but
they offer little in the way of explaining how and why Alouatta came to be. The first
batch of diverse alouattine fossils suggests some answers lay buried.
Acknowledgements We owe much to many: to the editors of this volume for inviting us to
contribute; to the museums mentioned above that make our research possible, especially our home
institution, the American Museum of Natural History; to Leandro Salles and Castor Cartelle and
their museums, MNRJ and PUC MINAS, for making this project possible; to Marilyn Norconk for
sharing her insights on platyrrhines; to Andi Jones and Mike Rose for discussions on the Brazilian
fossils and use of their photographs; to the agencies at Brooklyn College (Tow) and the City
University of New York (PSC CUNY) for financial assistance to ALR; to the Wenner-Gren
Foundation and CUNY NYCEP for a postdoctoral fellowship awarded to MFT which helped
support our collaboration; and to NSF DDIG awards to LBH (0925704) and SBC (0726134) and
an Alumnae Association of Barnard College Graduate Fellowship to help support SBC in her
research on Caribbean primates. We thank the reviewers and editors for many helpful suggestions.
The software package PAST was employed for several computations and charts (http://folk.uio.no/
ohammer/past/).
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51
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