Dionisios Youlatos

Sébastien Couette
email: sebastien.couette@u-bourgogne.fr

Lauren B Halenar
email: lauren.halenar@gmail.com

Morphology of howler monkeys: a review and quantitative analyses

Keywords: Alouatta, Cranium, Hyoid, Morphometrics, Postcranium, Teeth Palabras clave Alouatta, Cráneo, Hueso hioides, Morfometría, Postcráneo, Dientes

the forelimb bears a mixture of features that favor quadrupedalism with restricted abduction and overhead extension, providing stable contact and support along branches. In contrast, the hind limb appears to allow for a wider range of movement in all joints, with an emphasis on thigh extension and abduction, leg rotation, and powerful grasping with a habitually inverted foot. Interspecifi c variation reveals traits that can be ultimately related to subtle differences in the frequency of use of different positional modes, associated with variable eco-social factors. These results, deriving from different anatomical regions, provide evidence for understanding morphological variation across howler species in terms of morphofunctional adaptations, environmental pressure, and niche partitioning.

Resumen Reconocer la particular estrategia eco-comportamental del género Alouatta ha sido crucial para estudiar y entender su morfología craneal y post-craneal. La arquitectura única de su cráneo y mandíbula indican que muy probablemente evolucionaron en relación con su aparato masticatorio particular que se encuentra asociado a un incremento de una dieta folívora, así como con su comunicación vocal asociada a su comportamiento social y de estrategia de minimización energética. Comparaciones de la morfología craneal utilizando geometría morfométrica tridimensional resaltan diferencias signifi cativas inter-específi cas en la forma del cráneo. Alouatta seniculus es la especie más divergente en cuanto a la morfología del cráneo y del hueso hioides, exhibiendo los niveles más pronunciados de dimorfi smo sexual en esas áreas. La variabilidad craneal es expresada en el prognatismo facial y airorrinchia, fl exión basocraneal y altura zigomática. Diferencias inter-e intra-específi cas basadas en estos ejes de variación están muy posiblemente vinculadas a variaciones interespecífi cas en dieta, comportamiento e historias de vida. Por otra parte, evidencia adicional de la anatomía dental de este género indica adaptaciones de cambio a una dieta más folívora. Además, estudios recientes proporcionan evidencia adicional de variación inter-e intraespecífi ca signifi cativas en la forma y el tamaño del hueso hioides. Alouatta seniculus posee la bula más larga e infl ada del hueso hioides y las especies que ocupan los extremos de distribución del género ( A. palliata , A. caraya ) se distinguen por diferencias acentuadas en la forma del hueso hioides. Estos datos indican una compleja interrelación entre morfología y comportamiento, con posibles implicaciones biogeográfi cas. En términos de la morfología craneal, los miembros anteriores muestran una combinación de atributos que favorecen el cuadrupedalismo con abducción restringida y extensión amplia que proporciona contacto estable y soporte en las ramas. En contraste, los miembros posteriores parecieran permitir un mayor rango de movimiento de todas las articulaciones, con énfasis en la extensión y abducción del muslo, rotación de la pierna y una mayor capacidad de asir con una inversión común del pie. Variación interespecífi ca revela rasgos que ultimadamente podrían estar vinculadas con diferencias sutiles en la frecuencia de uso de diferentes posturas, asociadas con factores eco-sociales. Estos resultados, que derivan de diferentes regiones anatómicas, proporcionan evidencia para entender la variación morfológica a través de las especies de monos aulladores en términos de adaptaciones morfo-funcionales, presiones ambientales y partición de nichos.

Introduction

The monophyly of atelines as a group is unquestioned, but the interrelationships of the genera within the group remain unclear. The phylogenetic signals from molecular and morphological data disagree on the relationships among Lagothrix , Brachyteles , and Ateles , but all phylogenetic hypotheses distinguish Alouatta from the rest: howlers apparently diverged fi rst from the group around 15 MA and evolved unique morphobehavioral adaptations related to increased folivory, energyminimizing ecological strategies, cautious above-branch quadrupedal positional behavior, and enhanced sound production [START_REF] Rosenberger | Adaptive radiation of the ateline primates[END_REF][START_REF] Hartwig | Implications of molecular and morphological data for understanding ateline phylogeny[END_REF] for a review). The distinctiveness of Alouatta was pointed out very early by [START_REF] Lacépède | Mémoire sur une nouvelle table méthodique des animaux à mamelles[END_REF] and was later highlighted by several authors (e.g., [START_REF] Lönnberg | Notes on members of the genera Alouatta and Aotus[END_REF][START_REF] Hershkovitz | Mammals of Northern Colombia. Preliminary report n° 4: monkeys (Primates), with taxonomic revisions of some forms[END_REF][START_REF] Hill | Primates: comparative anatomy and taxonomy V Cebidae Part B[END_REF]. In this chapter, we attempt to point out the unique morphology of the genus Alouatta focusing on cranial, dental, hyoid, and postcranial traits. For these purposes, two approaches were adopted: review of the literature on cranial, dental, hyoid, and postcranial characters as well as quantitative multivariate analyses of new data on cranial and hyoid morphology. Reviews will help the reader to appreciate the derived morphology of Alouatta , while the analyses of original data will further highlight their remarkably different anatomy from that of other atelines and other platyrrhines and will address issues of intra-and interspecifi c morphological variations within a functional, phylogenetic, and, where available, biogeographic framework.

Cranium

The Uniqueness of Alouatta Cranial Morphology

Among atelines and other platyrrhines, Alouatta can be differentiated by the peculiar form of its skull [START_REF] Hill | Primates: comparative anatomy and taxonomy V Cebidae Part B[END_REF] ): the pyramidal shape of the relatively small brain case, the posteriorly directed nuchal plane, the prognathic face anterior to the braincase, and the extended and unfl exed basicranial axis. This morphological organization of the skull has been described as airorhynchy and corresponds to the upward rotation of the functional axis of the splanchnocranium on the neurocranium (see Tattersall 1972 ;[START_REF] Bruner | A geometric morphometric approach to airorhynchy and functional cranial morphology in Alouatta (Atelidae, Primates)[END_REF] ). The braincase, in comparison to the face, is small [START_REF] Schultz | The relative size of the cranial capacity in primates[END_REF], a relationship probably related to the early cessation of cranial growth and the obliteration of the cranial sutures [START_REF] Höfer | Die craniocerebrale topographie bei affen und ihre bedeutung fur die menschliche schadelform[END_REF][START_REF] Höfer | On the evolution of the craniocerebral topography in primates[END_REF]. Additionally, the foramen magnum and the occipital condyles face posteriorly, an orientation displaying individual variation, but also undergoing changes during ontogeny [START_REF] Bolk | Ueber lagerung, versehiebung und neigung des foramen magnum am schädel der Primaten[END_REF][START_REF] Senyurek | Cranial equilibrium index[END_REF][START_REF] Schultz | The position of the occipital condyles and of the face relative to the skull base in primates[END_REF].

The development and form of the face, mandible, and braincase have been interpreted as primitive traits [START_REF] Anthony | La surface de la voûte palatine rapportée à la capacité crânienne chez les Singes Platyrhiniens[END_REF] ). However, a long narrow cranial base with an airorynchous face, a fl at, posteriorly facing nuchal plane, and expanded gonial angles of the mandible are most often argued to be associated with opening the subbasal space for an enlarged hyoid [START_REF] Rusconi | Sobre morfogenesis basicraneana de algunos primates actuales y fosiles[END_REF][START_REF] Biegert | The evaluation of characteristics of the skull, hands, and feet for primate taxonomy[END_REF][START_REF] Miller | Facial fl exion and craniometric variation in the genus Alouatta[END_REF]. This functional interpretation is partly supported by the shared airorynchous face and well-developed anatomical structures for sound production in Alouatta and Pongo [START_REF] Biegert | The evaluation of characteristics of the skull, hands, and feet for primate taxonomy[END_REF][START_REF] Shea | On aspects of skull form in African apes and orangutans, with implications for hominoid evolution[END_REF][START_REF] Bruner | A geometric morphometric approach to airorhynchy and functional cranial morphology in Alouatta (Atelidae, Primates)[END_REF] ). Alternatively, this reorganization has been also functionally linked to folivory. For example, in the mandible, the wide bigonial breadth of Alouatta appears to both favor folivory and to accommodate the enlarged hyoid bone. The development and posterolateral displacement of the gonial angles is intrinsically related to the enlarged hyoid in males [START_REF] Watanabe | Mandible/basihyal relationships in red howler monkeys ( Alouatta seniculus ): a craniometrical approach[END_REF], but their fl aring allows the mandible to pass lateral to the enlarged hyoid bone during maximum gape, and their expansion also provides a larger area of attachment for the masseter muscles used during chewing [START_REF] Herring | Adaptations for gape in the hippopotamus and its relatives[END_REF][START_REF] Bruner | A geometric morphometric approach to airorhynchy and functional cranial morphology in Alouatta (Atelidae, Primates)[END_REF] ). An airorynchous face and a vertical nuchal plane change the orientation of the head on the neck, which has been suggested to make it easier to crop leaves (Tattersall 1972 ); this functional link has also been used in interpreting the cranial morphology of the large subfossil lemur Megaladapis , other folivorous subfossil lemurs [START_REF] Godfrey | Quaternary fossil lemurs[END_REF], and the folivorous koala Phascolarctos .

This reorganization is accompanied by analogous modifi cations to the arrangement of various cranial muscles. Thus, Alouatta is characterized by the pronounced size of the masticatory muscles, which are linked both to the expansion of the hyolaryngeal organs and the mandible. Furthermore, howlers possess a modifi ed insertion of m. digastricus on the mandible that does not extend posteriorly, as in other platyrrhines [START_REF] Leche | Über Beziehungen zwischen Gehirn und Schadel bei den Affen[END_REF]. The arrangement of facial muscles is comparable to that of the other atelines, but Alouatta displays overdeveloped mm. platysma colli and faciei , which reach the orbitozygomatic plate and are probably linked to the growth of the mandible. The mm. stylopharyngeus and the muscles of the pharynx have undergone a large increase in size, especially the pharyngeal middle constrictor and the membranous parts of the pharynx which are implicated in the emptying of the air sacs, as well as the pharyngeal inferior constrictor that is involved in the control of the vocal cords [START_REF] Schön | The muscular system of the red howling monkey[END_REF] ). M. pterygoideus medialis attaches to the enlarged gonial angle and helps elevate and protract the mandible during howling [START_REF] Schön | The muscular system of the red howling monkey[END_REF] ). Finally, mm. stylohyoideus , genioglossus , hyoglossus , styloglossus , sternohyoideus , and thyrohyoideus , which operate on the hyoid, are all well developed.

These morphological modifi cations differentiate Alouatta from the other atelines. However, their functional link to folivory and sound production, which both vary across howler species and sexes [START_REF] Fiore | The atelines: Variation in ecology, behavior, and social organization[END_REF], would imply some degree of intra-and interspecifi c differences. With this in mind, quantitative analytical approaches were used in this study to examine potential morphological variations.

Cranial Material and Analyses

For the current study, we collected data from the skulls of 14 Lagothrix (three species), 48 Ateles (seven species), 78 Alouatta (seven species) adult males and females, and one male Brachyteles . For our analysis at the genus level, we did not consider sex or species. In contrast, we considered both variables in our analysis of Alouatta cranial diversity at the species level. The Alouatta sample was composed of 15 A. paliatta (10M, 5F), 4 A. pigra (3M, 1F), 9 A. guariba (5M, 4F), 14 A. belzebul (7M, 7F), 10 A. caraya (6M, 4F), 15 A. seniculus (8M, 7F), and 11 A. nigerrima (6M, 5F). All specimens were wild-shot individuals housed in the Laboratoire des Mammifères et Oiseaux, Muséum national d'Histoire naturelle (Paris, France), Museu Paraense Emílio Goeldi (Bélem, Pará, Brasil), and the American Museum of Natural History (New York, USA). A set of 55 landmarks were used (Fig. 6.1 , Table 6.1 ), identical to those from previous studies and shown to successfully differentiate small shape variations [START_REF] Couette | Quantitative characterisation of the cranial development of Cebus apella and Alouatta seniculus (Primates, Platyrrhines). Interest of geometrical morphometric methods[END_REF][START_REF] Couette | Différenciation morphologique et génétique des populations de douroucoulis ( Aotus infulatus , Primates, Platyrhiniens, Cebidae) provenant des rives droite et gauche du rio Tocantins (Brésil)[END_REF]. The landmarks were digitized using a MicroScribe G2X (Immersion Corporation, San José, California). Bilateral landmarks have been digitized on the left side only, and mirroring was performed using the R software ( 2008 ). Each specimen was digitized twice in order to estimate measurement error, which varied between 1.9 and 2.3 %. 6.1 for landmark defi nitions). Dashed lines illustrate wireframes used for shape variation visualizations For our analysis, we used landmark-based 3DGM methods, such as generalized Procrustes analysis (GPA; [START_REF] Rohlf | Extensions of the Procrustes method for the optimal superimposition of landmarks[END_REF], which can involve a great number of variables for the quantifi cation of variation. A good solution to deal with such numerous variables is the use of multivariate statistics such as principal components analysis (PCA). Common parts of variation described by the variables are summarized and expressed by a new series of orthogonal (independent) axes that constitute new morphological variables. Each PC axis describes only a part of the total varia- tion within the sample, and the contribution of the initial variables on each axis constitutes a key for the understanding of morphological differences between specimens. However, with Procrustes techniques, a great number of variables and the nature of the variables themselves ( X , Y , and Z coordinates) usually complicate the polarization of morphological variations described by the PC axes. Therefore, wireframe diagrams and geometric reconstruction of cranial shape are frequently used to visualize PCA results. The GPAs and PCAs were performed using morphologika 2 v. 2.5 (O 'Higgins and Jones 2006 ), which also calculated centroid sizes, PC scores, wireframe diagrams, and the geometric reconstruction of cranial shape. The PAST 1.89 software package [START_REF] Hammer | PAST: Paleontological Statistics software package for education and data analysis[END_REF] ) was used to perform and output graphical representation of the PCAs. Finally, we used Statistica 7 (Statsoft Inc., USA) for other statistical analyses such as linear regressions to check for allometric effects on the pattern of variation described on each PC axis.

Cranial Variation

In the PCA at the generic level (Fig. 6.2a ), the fi rst two PCs accounted for 65.1 % of total variation (51.7 % for PC1 and 13.4 % for PC2). Multivariate regressions (reduced major axis) of the PC scores onto the logarithm of centroid size indicate a signifi cant linear correlation between PC1 scores and size ( a = -0.91; b = 5.15; R 2 = 0.32, p < 0.001). Size has a signifi cant infl uence on cranial morphology, and larger specimens lie on the negative side of PC1. Cranial distinction is mainly allometric, with Alouatta exhibiting the higher scores ( R 2 = 0.71; p < 0.001), compared to Ateles ( R 2 = 0.28, p = 0.02). Alouatta are clearly separated from the other atelines and occupy the negative side of the morphospace on PC1 but spread along PC2 with a plot centered at the origin of this axis. Ateles and Lagothrix overlap on the positive side of PC1 but are distinguishable on PC2. The latter are located on the negative side of the axis, while Ateles are mainly on the negative side, with signifi cant overlap in the center.

Regarding morphology, negative values on PC1 are associated with a relatively developed face and a high degree of prognathism, while positive values describe rounded skulls with a relatively small face compared to the neurocranium. On PC1, the main morphological variation is a downward and backward rotation and relative shortening of the face. This rotation implies verticalization of the snout and the orbital plane. The relative volume of the neurocranium increases, and the occipital undergoes a downward and forward rotation, a consequence of an increase in the fl exion of the basicranium associated with the facial rotation (Fig. 6.2b ). On PC2, the negative values describe skulls with a relatively fl attened neurocranium, while the positive values are associated with a high braincase. The main morphological variations are linked to the position of the bregma and the relative height of the braincase and the frontal part of the face (Fig. 6.2b ).

The main morphological differences between Alouatta and the other atelines are in the degree of prognathism, airorhynchy, the oblique position of the orbital plane, the relative reduction of the neurocranium (essentially in height), the posterior orientation of the occipital condyles and the foramen magnum, the unfl exed basicranium, and the robustness of the face and the zygomatic arches of howlers. As described above, functionally, these derived features have been associated with both diet and vocalizations. Although Alouatta and Brachyteles share dental adaptations to their semi-folivorous diet, the latter have skulls that are most similar to those of their ateline relatives, without an airorynchous face, posteriorly directed occipital, or a relatively small brain case [START_REF] Rosenberger | The making of platyrrhine semifolivores: models for the evolution of folivory in primates[END_REF]. Lack of nutrients in the mainly folivorous diet in Alouatta may account for a small brain, which may in turn be directly linked to an unfl exed cranial base, as the "spatial packing" hypothesis suggests [START_REF] Biegert | The evaluation of characteristics of the skull, hands, and feet for primate taxonomy[END_REF][START_REF] Gould | Ontogeny and phylogeny. Belknap, Cambridge Grand TI (1968a) Functional anatomy of the upper limb. In: Malinow MR (ed) Biology of the howler monkey ( Alouatta caraya ). Karger, Basel Grand TI (1968b) The functional anatomy of the lower limb of the howler monkey ( Alouatta caraya )[END_REF][START_REF] Ross | Basicranial fl exion, relative brain size, and facial kyphosis in nonhuman primates[END_REF][START_REF] Lieberman | Basicranial infl uence on overall cranial shape[END_REF]. Additionally, this morphology may be further associated with the necessity for opening of the subbasal space in order to accommodate the morphological modifi cations related to sound production. Therefore, it seems that the craniomandibular apomorphies of Alouatta are the result of complex adaptations to increased and frequent vocalization and also partly to folivory. However, this is variably expressed within the genus, and size seems to play a signifi cant role suggesting intra-(sexual) and interspecifi c (phylogeographic) variations.

In the analysis at the species level, the fi rst two PCs accounted for 61.1 % of total variation (37.4 % for PC1 and 23.7 % for PC2; Fig. 6.3a ). Morphological variations described by PC1 are very similar to the ones described by PC1 at genus level but with lower intensity. Negative values characterize skulls with a very prognathic face, while positive ones characterize skulls with a less well-developed face. This axis describes a reduction in the degree of prognathism accompanied by a verticalization of the nasal and frontal bones as well as the orbital plane. Variation along PC1 also includes a shortening of the palate, a relative increase of the size of the neurocranium, and a downward rotation of the occipital which leads to increased basicranial fl exion (Fig. 6.3b ). PC1 also separates males from females. In the morphospace, males occupy the negative side of the axis, while females are clustered in the positive side, with few overlapping. Gender differences and overall variation seem to be more pronounced in A. seniculus than for any other species, and are not in accord with body size dimorphism [START_REF] Ravosa | Craniodental allometry and heterochrony in two howler monkeys: Alouatta seniculus and A. palliata[END_REF] ). These differences in cranial morphological traits do, however, seem to agree with those from previous descriptions of cranial dimorphism [e.g., A. palliata (Blanco and Godfrey 2006 ), A. arctoidea [START_REF] Braza | El araguato rojo ( Alouatta seniculus )[END_REF]], although population level differences may be important [START_REF] Jones | Craniometric variation in a population of mantled howler monkeys ( Alouatta palliata ): evidence of size selection in females and growth in dentally mature males[END_REF]. The differences in cranial morphology between the sexes may be related to proximally hypermorphosis during male growth [START_REF] Ravosa | Craniodental allometry and heterochrony in two howler monkeys: Alouatta seniculus and A. palliata[END_REF][START_REF] Masterson | Degrees of sexual dimorphism in Cebus and other New World monkeys[END_REF][START_REF] Jones | Craniometric variation in a population of mantled howler monkeys ( Alouatta palliata ): evidence of size selection in females and growth in dentally mature males[END_REF][START_REF] Flores | Cranial ontogeny and sexual dimorphism in two New World monkeys: Alouatta caraya (Atelidae) and Cebus apella (Cebidae)[END_REF] but may also be linked evolutionarily to trophic and masticatory functions that are very important for male competition [START_REF] Flores | Cranial ontogeny and sexual dimorphism in two New World monkeys: Alouatta caraya (Atelidae) and Cebus apella (Cebidae)[END_REF].

Along PC2, the morphological variation represents a difference in the height of the cranial vault associated with a difference in the rotation of the occipital. Compared to the negative side of the axis, positive values are associated with a taller braincase, higher occipital condyles, thicker zygomatic arches, a downward directed muzzle, and a more vertical orientation of the orbital plane. PC2 partly distinguishes between certain species, and the positive side is occupied by the divergent Central American clade ( A. palliata , A. pigra ). The rest are rather mixed in the center ( A. belzebul , A. seniculus , A. nigerrima ), with the southernmost species, A. caraya and A. guariba , differing slightly. Alouatta belzebul , A. seniculus , and A. nigerrima are distributed widely across the morphospace, displaying higher intraspecifi c Fig. 6.3 ( a ) PCA results for the analysis of cranial variation at the species level. Morphological variations along PC1 describe differences explained by sexual dimorphism. Differences along PC2 describe geographical differences, distinguishing the Central American ( A. paliatta and A. pigra ) from the South American species. ( b ) Polarization of the morphologies described by the negative ( gray ) and positive ( black ) values of PC1 and PC2 for the analysis of cranial variation at the species level (on the left ). Superimposition of the extreme morphologies of each axis (on the right ) variation (on both PCs). This is noticeable for A. nigerrima , with specimens of both sexes positioned on both sides, implying two probable morphological groups for this species. The cranial particularities of the Central American species have been previously reported by [START_REF] Watanabe | Mandible/basihyal relationships in red howler monkeys ( Alouatta seniculus ): a craniometrical approach[END_REF], and their differentiation within the genus is also supported by molecular data (e.g., [START_REF] Cortés-Ortiz | Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta[END_REF]. [START_REF] Watanabe | Mandible/basihyal relationships in red howler monkeys ( Alouatta seniculus ): a craniometrical approach[END_REF] detected differences between A. palliata and A. seniculus in basicranium length, height of the nasal bones, bigonial breadth, and the development of the pterygoid wing, which is associated with m. pterygoideus medialis , an elevator and a protractor of the mandible [START_REF] Schön | The muscular system of the red howling monkey[END_REF] ).

Dental Morphology

In terms of overall proportions, the Alouatta dentition can be described as molar centric, where the incisors at the front of the jaw are much smaller than the molars and are often offset from the canines by a diastema (Fig. 6.4 ). This is the opposite condition seen in many frugivorous primates, including the atelines Ateles and Lagothrix , which tend to have larger, bladelike incisors for processing the large, potentially tough-skinned fruit into bite-sized pieces [START_REF] Hylander | Incisor size and diet in anthropoids with special reference to the Cercopithecidae[END_REF][START_REF] Kay | The dental structure of mammalian folivores with special reference to primates and phalangeroids (Marsupialia)[END_REF][START_REF] Eaglen | Incisor size and diet revisited: the view from a platyrrhine perspective[END_REF][START_REF] Anthony | Tooth form and diet in ateline and alouattine primates: refl ections on the comparative method[END_REF]. In contrast, the narrow width of the incisor row of Alouatta , as well as the mediolateral tapering of each incisor itself, refl ects the more concentrated force per tooth used to bite and pull leaves [START_REF] Ungar | Incisor microwear and feeding behavior in Alouatta seniculus and Cebus olivaceus[END_REF][START_REF] Anapol | Morphological adaptation to diet in platyrrhine primates[END_REF]. The upper incisors are also oriented at an angle due to the howler's airorynchous face and are therefore in an advantageous position for cropping leaves off tree branches (Tattersall 1972 ). Alouatta is highly sexually dimorphic in body size, hyoid size, and canine size so male canines are considerably more prominent than those of females of the same species [START_REF] Ford | Evolution of sexual dimorphism in body weight in platyrrhines[END_REF].

The molars are large and square with complex surfaces made up of long crests of thin enamel (Fig. 6.4 ); Alouatta has the largest postcanine tooth area of all the ateline primates [START_REF] Rosenberger | Adaptive radiation of the ateline primates[END_REF]. Their distinct morphology is marked by high crowns, deep basins, deep intercuspal notches on the buccal and lingual sides of the crown, and a long cristid obliquid (Fig. 6.4 ; Cooke 2011 ). This is particularly clear when comparing the "shearing quotient" of folivorous howler monkeys to frugivorous spider monkeys [START_REF] Kay | Molar structure and diet in extant Cercopithecidae[END_REF]1984 ;[START_REF] Anthony | Tooth form and diet in ateline and alouattine primates: refl ections on the comparative method[END_REF]. The high-crested molars of the howlers are adapted to slicing through the tough structural carbohydrates, like cellulose, that make up their leafy diet, while the lowrelief molars of the spider monkeys are better suited to mashing up softer fruit pulp [START_REF] Kay | The functional adaptation of primate molar teeth[END_REF][START_REF] Rosenberger | Functional patterns of molar occlusion in platyrrhine primates[END_REF][START_REF] Anthony | Tooth form and diet in ateline and alouattine primates: refl ections on the comparative method[END_REF][START_REF] Anapol | Morphological adaptation to diet in platyrrhine primates[END_REF]. More recent analyses of the overall surface relief and topography of the molars, not just shearing crest length, also illustrate this difference between howler monkeys and their more frugivorous relatives (i.e., [START_REF] Cooke | Paleodiet of extinct platyrrhines with emphasis on the Caribbean forms: threedimensional geometric morphometrics of mandibular second molars[END_REF].

The shearing capability of Alouatta molars has been shown to be convergent upon the superfi cially similar surface topography of the molars of another ateline, Brachyteles [START_REF] Rosenberger | Adaptive radiation of the ateline primates[END_REF][START_REF] Rosenberger | Evolution of feeding niches in New World monkeys[END_REF] ). The folivorous woolly spider monkeys also have relatively small incisors and large, high-relief molars that have a high shearing quotient, but the crests appear on a different aspect of the molar surface. Alouatta 's shearing crests are concentrated on the buccal side of the molars which exhibit a large paracone, metacone, and ectoloph in the upper tooth row and an elongate talonid and cristid obliquid in the lower (Fig. 6.4 ; [START_REF] Rosenberger | Adaptive radiation of the ateline primates[END_REF]. Brachyteles , on the other hand, shears on the lingual side of the molars with a large protocone and a tall metaconid, which occludes into the gap between the protocone and hypocone; they are also unique among atelines in possessing a strong lingual notch between the metaconid and entoconid [START_REF] Rosenberger | Adaptive radiation of the ateline primates[END_REF]. Genetic evidence points to a sister-taxon relationship between Brachyteles and Lagothrix , while skeletal morphology favors a Brachyteles -Ateles pair; no evidence for a close relationship between Alouatta and Brachyteles exists besides their shared dental morphology, which has convincingly been shown to be a convergent adaptation to their folivorous diet [START_REF] Anthony | Tooth form and diet in ateline and alouattine primates: refl ections on the comparative method[END_REF].

Some differences in relative incisor size have been described between various species of Alouatta (i.e., [START_REF] Anthony | Tooth form and diet in ateline and alouattine primates: refl ections on the comparative method[END_REF], which is to be expected based on their differing degrees of folivory [START_REF] Fiore | The atelines: Variation in ecology, behavior, and social organization[END_REF], but no systematic study of interspecifi c dental morphology exists to date [but see the dissertation work of [START_REF] Orlosky | Comparative dental morphology of extant and extinct Cebidae. Ph.D. dissertation, University Microfi lms, Ann Arbor Oxnard CE[END_REF]]. At least one species, Alouatta palliata , shows a characteristic species-wide wear sequence as their high-relief molars are fl attened over time with use, reducing the shearing crest length but preserving the "angularity," or jaggedness, of the surfaces necessary for processing leaves [START_REF] Dennis | Dental topography and molar wear in Alouatta palliata from Costa Rica[END_REF]. This is in agreement with [START_REF] Rosenberger | Functional patterns of molar occlusion in platyrrhine primates[END_REF] insights on the ontogenetic maintenance of molar shear in folivores such as Alouatta , as well as more insectivorous taxa, like Callithrix . The thin enamel and large molar surface area assure that the howler monkey teeth will retain their shearing functions while they wear down (see also [START_REF] Kay | On the use of anatomical features to infer foraging behavior in extinct primates[END_REF][START_REF] Anapol | Morphological adaptation to diet in platyrrhine primates[END_REF].

Hyoid

A Unique Hypertrophied Hyoid

Alouatta is said to make the loudest vocalizations of any terrestrial vertebrate and has the largest, most infl ated hyoid bone within the primate order. While the basic anatomy of the hyoid bone, thyroid and epiglottic cartilages, and air sacs of Alouatta have been described by many authors, inter-and intraspecifi c variations are not as well known, and there is debate about how their morphology relates to diet, vocalizations, body size, respiration, and the functional morphology of the skull. Unlike in humans, the hyoid bone of Alouatta is always attached to the cranial base through a chain of cartilaginous, or sometimes even ossifi ed, elements, i.e., the more common "integro-cornuate" condition [START_REF] Howes | On the mammalian hyoid, with especial reference to that of Lepus , Hyrax , and Choloepus[END_REF]. It also sits wedged between the gonial angles of the mandible. The hyoid serves as an attachment point for muscles and ligaments that also serve the mandible, tongue, laryngeal cartilages, pharynx, sternum, and cranial base, hence its proposed functions involving several systems including respiration, swallowing, and vocalizations. In most mammals, the hyoid apparatus lies at or above the entrance to the larynx and consists of two basic parts: inferiorly, the unpaired basihyal and paired thyrohyal "horns" which connect the basihyal to the thyroid cartilage and superiorly, the paired suspensory stylohyoid chains which are made up of four cartilaginous or ossifi ed links, the ceratohyal, epihyal, stylohyal, and tympanohyal, that connect the basihyal to the temporal bone (e.g., [START_REF] Howes | On the mammalian hyoid, with especial reference to that of Lepus , Hyrax , and Choloepus[END_REF][START_REF] Negus | The comparative anatomy and physiology of the larynx[END_REF].

It is the size and shape of the basihyal portion that vary across primate species. Some Old World monkeys have a caudally expanded basihyal that covers the top of the thyroid cartilage [START_REF] Negus | The comparative anatomy and physiology of the larynx[END_REF][START_REF] Hilloowala | Comparative anatomical study of the hyoid apparatus in selected primates[END_REF][START_REF] Nishimura | Comparative morphology of the hyo-laryngeal complex in anthropoids: two steps in the evolution of the descent of the larynx[END_REF], but none are as extremely modifi ed as that of Alouatta . Howler monkeys are the only living primates that have evolved a pneumatized hyoid bone with a large, hollow balloon-like basihyal, which is argued to serve, along with their air sacs, as a resonating chamber [START_REF] Chapman | My tropical air castle. D. Appleton, New York Chiarello A[END_REF][START_REF] Kelemen | The vocal organ of the howling monkey ( Alouatta palliata )[END_REF][START_REF] Schön | The anatomy of the resonating mechanism in howling monkeys[END_REF][START_REF] Hewitt | The functions of laryngeal air sacs in primates: a new hypothesis[END_REF]. As the larynx of howlers, and the other nonhuman primates, is positioned so high in the throat, the supralaryngeal dimensions of the pharynx are small, limiting the range of sounds that can be made [START_REF] Laitman | Evolution of the human larynx: nature's great experiment[END_REF]. The expanded hyoid bone and air sacs positioned above the larynx in Alouatta increase the volume of this space and, along with stretching out the neck and manipulations of the lips [START_REF] Schön | Loud calls of adult male red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Whitehead | Vox Alouattinae: a preliminary survey of the acoustic characteristics of longdistance calls of howling monkeys[END_REF], shape the sound and volume of their loud long calls.

The laryngeal cartilages are also enlarged in Alouatta , especially the thyroid, cuneiforms, and epiglottis, which are also sometimes ossifi ed [START_REF] Kelemen | The vocal organ of the howling monkey ( Alouatta palliata )[END_REF][START_REF] Hill | Primates: comparative anatomy and taxonomy V Cebidae Part B[END_REF] ). The basihyal is joined to the thyroid cartilage with a membranous attachment, and the two are freer to move more independently of one another in Alouatta than in other primates [START_REF] Ma | A comparative approach to the nonhuman primate vocal tract: implications for sound production[END_REF]. As mentioned above, the stylohyoid chain is of the common mammalian integro-cornuate type, connecting to the cranial base anterior to the stylomastoid foramen [START_REF] Howes | On the mammalian hyoid, with especial reference to that of Lepus , Hyrax , and Choloepus[END_REF][START_REF] Hilloowala | Comparative anatomical study of the hyoid apparatus in selected primates[END_REF]. Not enough is known about variation in the associated hyoid musculature, hence how the hyoid may move during howling in the different species, as only a few specimens of A. seniculus [START_REF] Hill | Primates: comparative anatomy and taxonomy V Cebidae Part B[END_REF][START_REF] Schön | The muscular system of the red howling monkey[END_REF][START_REF] Schön | The anatomy of the resonating mechanism in howling monkeys[END_REF], A. palliata [START_REF] Kelemen | The vocal organ of the howling monkey ( Alouatta palliata )[END_REF][START_REF] Hilloowala | Comparative anatomical study of the hyoid apparatus in selected primates[END_REF], and A. caraya [START_REF] Schön | The anatomy of the resonating mechanism in howling monkeys[END_REF] ) have been dissected. It is worth emphasizing that the size of the hyoid and the anatomical space it requires in the head are not trivial. For example, an average endocranial volume for a mixed sex sample of 16 A. belzebul individuals from the American Museum of Natural History was 55 ml, and the average hyoid volume for four males of that species was 57 mL; in two individuals, hyoid volume was approximately 140 % of their endocranial volume.

The impact of this anatomical specialization on the howler skull has yet to be adequately investigated and synthesized, but various unique aspects of cranial and mandibular morphology in Alouatta have been suggested to be related to the large size of these vocal tract structures (e.g., [START_REF] Biegert | The evaluation of characteristics of the skull, hands, and feet for primate taxonomy[END_REF][START_REF] Watanabe | Mandible/basihyal relationships in red howler monkeys ( Alouatta seniculus ): a craniometrical approach[END_REF]. While the unique morphology of the bone was mentioned by many early authors (e.g., Grew 1681 ), variation in hyoid size and shape among the species of Alouatta was fi rst systematically described by Hershkovitz in 1949 . The morphology of this region has been used as a diagnostic character for species recognition since then by [START_REF] Hill | Primates: comparative anatomy and taxonomy V Cebidae Part B[END_REF] and many others. This section will quantitatively explore hyoid size and shape within Alouatta in order to better understand interspecifi c differences that in the past have been used as a basis for taxonomic, phylogenetic, and functional interpretations about the genus.

Hyoid Material and Analyses

Over 100 undeformed Alouatta hyoids from collections at the American Museum of Natural History (New York, USA), the United States National Museum (Washington, DC, USA), and the Field Museum of Natural History (Chicago, IL, USA) were laser scanned using either a portable Minolta Vivid 910 laser surface scanner or a NextEngine desktop 3D scanner (Table 6.2 ). As the bony walls of many of the smaller hyoids were too thin to be "seen" properly by the lasers, the hyoid bullae were stuffed with paper towels to make the bone more opaque. The scans were edited using Geomagic Studio and ScanStudio HD v. 1.3.0, and a .ply fi le was created for each specimen [START_REF] Tallman | Analysis of selected hominoid joint surfaces using laser scanning and geometric morphometrics: a preliminary report[END_REF]. The Landmark Editor program (Wiley 2006 ) was then used to place homologous landmark points across the superior aspect of the tentorium as well as at the four corners of the posterior opening of the basihyal. These landmarks were used as anchors for drawing automated curves that generate semi-landmarks which quantify the bulbous aspect of the anterior portion of the bone [START_REF] Bookstein | Landmark methods for forms without landmarks: localizing group differences in outline shape[END_REF][START_REF] Rawlins | Semilandmarks in three dimensions[END_REF]Fig. 6.5 ). This procedure captured not only the size of the hyoid, which has been approximated in previous studies by measuring its length and/or width (see, for example, [START_REF] Watanabe | Mandible/basihyal relationships in red howler monkeys ( Alouatta seniculus ): a craniometrical approach[END_REF][START_REF] Halpern | The relationship between the hyoid and cranial and mandibular morphology in Alouatta : a factor analytic approach[END_REF] ), but also the bone's contours, which contribute to the unique shape of the hyoid in each species. Several Lagothrix hyoids, which are much smaller and less concave than those of Alouatta , were also scanned and landmarked, functioning as an "outgroup."

The data were subjected to a GPA [START_REF] Rohlf | Extensions of the Procrustes method for the optimal superimposition of landmarks[END_REF] to translate, rotate, and scale all specimens to unit centroid size using the morphologika 2 v2.5 software program (O 'Higgins and Jones 2006 ). The curves of semi-landmarks on the hyoids were also subjected to a "sliding" protocol using a program implemented in MATLAB in order to minimize Procrustes distance between the specimens and the calculated reference specimen [START_REF] Bookstein | Landmark methods for forms without landmarks: localizing group differences in outline shape[END_REF][START_REF] Rawlins | Semilandmarks in three dimensions[END_REF]. Sliding the semi-landmarks along the outline curves is an extension of the standard GPA superimposition procedure and is necessary to properly account for type III semilandmarks having fewer degrees of freedom than those of type I or type II [START_REF] Adams | Geometric morphometrics: ten years of progress following the "revolution[END_REF]. PCA was then used to visualize the morphological variation in the sample. The PAST 1.89 software package [START_REF] Hammer | PAST: Paleontological Statistics software package for education and data analysis[END_REF] ) was used to perform and output graphical representation of the PCAs.

Hyoid Variation

The development of the tentorium superiorly and the size and shape of the posterior opening of the basihyal are the most important variables for distinguishing the species from one another [START_REF] Hershkovitz | Mammals of Northern Colombia. Preliminary report n° 4: monkeys (Primates), with taxonomic revisions of some forms[END_REF][START_REF] Hill | Primates: comparative anatomy and taxonomy V Cebidae Part B[END_REF]Fig. 6.6a, b ). Male A. seniculus have the largest, most infl ated hyoid bullae with relatively small posterior openings and wide convex tentoria. A. guariba has a larger posterior opening with a less infl ated tentorium and no cornua. The hyoid of A. belzebul is also in a larger size class with the largest posterior opening and a slightly concave tentorium. Of the larger species, A. caraya has the smallest tentorium but a very large posterior opening and a uniquely shortened anteroposterior dimension that gives the bone a "snubnosed" appearance. The hyoid bullae of A. palliata are the smallest, with a fl ared opening, extremely reduced tentorium, and broad attachment sites for the thyrohyal proximally and the stylohyoid ligament distally. While A. pigra has been considered a subspecies of A. palliata and shares with it a Central American distribution, the female hyoid looks more similar to that of the South American species, while the bone in the male has a very unique, almost two-dimensional appearance.

These qualitative descriptions led [START_REF] Hershkovitz | Mammals of Northern Colombia. Preliminary report n° 4: monkeys (Primates), with taxonomic revisions of some forms[END_REF] to divide the genus into three groups: the seniculus group which includes A. seniculus , A. belzebul , and A. guariba ; the palliata group which includes A. palliata and A. pigra ; and the caraya group for the snub-nosed A. caraya . For Hershkovitz, these groups have evolutionary signifi cance, with A. palliata retaining the ancestral condition and A. seniculus , especially the males, exhibiting the most derived hyoid shape. Interestingly, while Alouatta males do have larger, more infl ated hyoid bullae than females of the same species, body size differences between the species do not seem to correspond to differences in hyoid size or the length of the supralaryngeal vocal tract [START_REF] Hilloowala | Comparative anatomical study of the hyoid apparatus in selected primates[END_REF][START_REF] Ma | A comparative approach to the nonhuman primate vocal tract: implications for sound production[END_REF]. In other words, the species with the largest average body size does not have the absolutely largest hyoid volume (Table 6.3 ). These differences in howler monkey hyoid size and shape do, however, seem to correlate with various acoustic features of their calls (Table 6.3 ): A. palliata has been shown to vocalize for shorter periods of time over a narrower bandwidth and higher frequency [START_REF] Sekulic | The signifi cance of call duration in howler monkeys[END_REF][START_REF] Whitehead | Vox Alouattinae: a preliminary survey of the acoustic characteristics of longdistance calls of howling monkeys[END_REF], they have the smallest hyoids, and they only have one type of air sac [START_REF] Ma | A comparative approach to the nonhuman primate vocal tract: implications for sound production[END_REF][START_REF] Hewitt | The functions of laryngeal air sacs in primates: a new hypothesis[END_REF]. From [START_REF] Whitehead | Vox Alouattinae: a preliminary survey of the acoustic characteristics of longdistance calls of howling monkeys[END_REF] e From [START_REF] Sekulic | The signifi cance of call duration in howler monkeys[END_REF] and [START_REF] Whitehead | Vox Alouattinae: a preliminary survey of the acoustic characteristics of longdistance calls of howling monkeys[END_REF] In the PCA results, the A. palliata and nonpalliata groups are not as distinct as one might expect based on the descriptions given above or quantitative studies of interspecifi c variation of the skull, but this could be due to the much smaller sample size of A. palliata compared to the other species (Figs. 6.7 and 6.8 ). These groupings do, however, generally agree with those described in previous studies of interspecifi c hyoid variation (i.e., [START_REF] Hershkovitz | Mammals of Northern Colombia. Preliminary report n° 4: monkeys (Primates), with taxonomic revisions of some forms[END_REF][START_REF] Halpern | The relationship between the hyoid and cranial and mandibular morphology in Alouatta : a factor analytic approach[END_REF][START_REF] Gregorin | Taxonomy and geographic variation of species of the genus Alouatta Lacépède (Primates, Atelidae) in Brazil[END_REF]. While having a slightly concave basihyal, the three Lagothrix hyoids are clearly separated from the Alouatta sample; Ateles hyoids look similar to those of Lagothrix , but unfortunately none could be laser scanned for this analysis. The anteriorposterior dimensions of the basihyal, along with the position of the four corners surrounding the posterior opening, are the main variables driving separation of the species clusters seen across PC1. The phenetic similarities in hyoid shape suggested by the overlap of the A. guariba and A. belzebul samples agree with their linkage in molecular phylogenetic studies of the genus (e.g., [START_REF] Cortés-Ortiz | Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta[END_REF]. The molecular evidence, however, also suggests a sister-taxon relationship between A. seniculus and A. caraya , two species that are shown here to be quite distinct in their hyoid morphology. Interestingly, there is some suggestion of geographic separation within the A. caraya and A. seniculus samples; Brazilian and Bolivian A. caraya form relatively distinct clusters as do Colombian and non-Colombian A. seniculus (Fig. 6.7 ). Perhaps hyoid size and shape are more infl uenced by socioecological factors related to long call behavior, like group size and habitat type (e.g., [START_REF] Sekulic | The signifi cance of call duration in howler monkeys[END_REF]Chiarello 1995 ), rather than phylogenetic relatedness.

PC2 separates Alouatta male hyoid shape from female hyoid shape within each species cluster reasonably well, and the dimorphism index calculated by dividing male hyoid centroid size by female hyoid centroid size confi rms a relatively high degree of sexual dimorphism in Alouatta hyoid size (Fig. 6.9 ; Table 6.3 ). The species with the largest hyoids as measured by centroid size, A. belzebul , A. seniculus , and A. guariba , are also the most dimorphic. But as noted above, these are not the species with the largest body sizes nor the highest body size dimorphism indices (Table 6.3 ). Male hyoid centroid sizes also vary more widely from species to species than those of females. An explanation for this, as well as why there are some males on the "female side" of the clusters in Fig. 6.7 , could be that non-dominant but fully adult males are vocalizing less than the dominant males and therefore have smaller musculature moving their smaller, more female-like hyoids.

A Derived Postcranium

This section reviews the current evidence on postcranial apomorphies and provides a functional interpretation of the Alouatta skeleton.

Forelimb

In Alouatta , the forelimb is relatively short compared to other atelines, representing only 91 % of the length of the vertebral column, whereas it is much longer in Lagothrix and Ateles (109 % and 150 % respectively, [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF] ). However, it is almost equal in length compared to the hind limb, as indicated by the intermembral index (IMI), which ranges between 97 and 99 [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). A similar condition is encountered in Lagothrix (IMI = 97.6), whereas Ateles is very different (IMI = 105; [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF].

The scapula is positioned relatively cranially compared to most other quadrupeds [START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. It is craniocaudally wide and reminiscent of climbing and suspensory mammals, compared to the more dorsoventrally elongated scapular shape of Fig. 6.9 Sexual dimorphism in the Alouatta hyoid. This shows the same distribution of specimens as in Fig. 6.6 , but with male individuals symbolized by open squares and females by closed squares . Graphically, the separation between males and females for most species looks distinct, but regressing in centroid size on PC1 scores gives R 2 values for PC1 and PC2 that are both relatively low at 0.4. This would indicate that hyoid shape differs more than hyoid size between the sexes in Alouatta both arboreal and terrestrial quadrupeds (Fig. 6.10 ; Roberts 1974 ). The scapular spine is only slightly oblique, compared to the more oblique position in Lagothrix and very oblique in Ateles , facilitating the rotatory action of the powerful m. trapezius during quadrupedal activities [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF][START_REF] Anapol | Fossil platyrrhine forelimb bones from the early Miocene of Argentina[END_REF].

The suprascapular fossa is particularly enlarged (Fig. 6.10 ), a condition also encountered in many climbing and suspensory mammals and associated with the substantial arm raising and abducting action of m. supraspinatus (Oxnard 1963 ;[START_REF] Schön | The muscular system of the red howling monkey[END_REF][START_REF] Larson | The use of supraspinatus in the quadrupedal locomotion of vervets ( Cercopithecus aethiops ): implications for interpretation of humeral morphology[END_REF][START_REF] Youlatos | Functional anatomy of forelimb muscles in Guianan atelines (Platyrrhini: Primates)[END_REF]. However, the greater relative surface area in Alouatta (33-42 % of total scapular surface area) compared to climbing primates (24-33 %, Youlatos 1994 ) may be related to a more cranial origin and the overdevelopment of m. atlantoscapularis posterior providing additional support for the neck [START_REF] Schön | The muscular system of the red howling monkey[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF] ).

The acromion is large and protuberant facing moderately dorsad (Fig. 6.10 ), whereas it is slightly less prominent and dorsally oriented in Ateles [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF] ). This provides a better leverage for m. deltoideus during powerful arm protraction and abduction. Medially, the coracoid process is moderately developed, protruding distally over the glenoid fossa in a way reminiscent of Lagothrix and arboreal quadrupeds. In contrast, Ateles possess an enlarged coracoid, oriented cranio-distally, contributing to a better leverage for mm. coracobrachialis and biceps brachii caput breve [START_REF] Schön | The muscular system of the red howling monkey[END_REF][START_REF] Anapol | Fossil platyrrhine forelimb bones from the early Miocene of Argentina[END_REF].

The glenoid fossa faces cranially, in contrast to the more lateral and completely lateral direction in Lagothrix and Ateles , respectively. This is related to the position of the scapula on the dorsoventrally elongated rib cage of Alouatta , compared to the more mediolaterally wide ribcage of Ateles [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF][START_REF] Rosenberger | Adaptive radiation of the ateline primates[END_REF] 1989 ; Youlatos 1994 ). Its shape is oblong in Alouatta (Fig. 6.10 ) with a relatively prominent cranial buttress with dense trabecular bone distribution, unlike the more spherical facet in Lagothrix and Ateles with a reduced buttress [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Anapol | Fossil platyrrhine forelimb bones from the early Miocene of Argentina[END_REF][START_REF] Fleagle | Locomotor behavior and skeletal morphology of two sympatric pithecine monkeys, Pithecia pithecia and Chiropotes satanas[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF][START_REF] Kagaya | Glenohumeral joint surface characters and its relation to forelimb suspensory behavior in three ateline primates, Ateles , Lagothrix , and Alouatta[END_REF].

The humeral head is ovoid in shape, relatively mediolaterally narrow and faces posteriorly (Fig. 6.11 ; [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF][START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Kagaya | Glenohumeral joint surface characters and its relation to forelimb suspensory behavior in three ateline primates, Ateles , Lagothrix , and Alouatta[END_REF]. Its mediolateral convexity is shorter and more pronounced than the anteroposterior one [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). The head is more circular and larger in Ateles , and its surface also expands and faces medially [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF][START_REF] Larson | Subscapularis function in gibbons and chimpanzees: implications for interpretation of humeral head torsion in hominoids[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). This has been metrically expressed by the intertuberosity angle, which is quite reduced in Alouatta (63.5°), compared to the intermediate position in Lagothrix (76.7°) and the very wide one in Ateles (111.2°; Jones 2004 ). The head projects proximad to the tuberosities (Fig. 6.11 ). The latter are rather well developed, compared to their reduced development in Lagothrix and Ateles [START_REF] Fleagle | The humerus of Aegyptopithecus zeuxis : a primitive anthropoid[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). The lesser tuberosity, the insertion point of m. subscapularis , is also well marked, whereas it is quite reduced in Ateles and Brachyteles and may be related to ample arm rotations [START_REF] Fleagle | The humerus of Aegyptopithecus zeuxis : a primitive anthropoid[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). This combination of humeral head features allows a greater degree of arm protraction and retraction, as well as increased stability during arm abduction necessary for arm raising movements during climbing and suspensory locomotion, as well as in foraging activities [START_REF] Fleagle | The humerus of Aegyptopithecus zeuxis : a primitive anthropoid[END_REF][START_REF] Harrison | New postcranial remains of Victoriapithecus from the Middle Miocene of Kenya[END_REF].

The bicipital groove is wide and shallow in Alouatta (Fig. 6.11 ), somewhat more defi ned in Lagothrix , and narrow and deep in Ateles ; this keeps the tendon of the biceps in place during arm movements [START_REF] Fleagle | The humerus of Aegyptopithecus zeuxis : a primitive anthropoid[END_REF][START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Harrison | New postcranial remains of Victoriapithecus from the Middle Miocene of Kenya[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). The deltopectoral crest on the humeral shaft is moderately developed and similar to climbing and suspensory forms, unlike the prominent and distally situated crest in more quadrupedal primates [START_REF] Fleagle | The humerus of Aegyptopithecus zeuxis : a primitive anthropoid[END_REF][START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF].

Alouatta , and to a lesser extent Lagothrix , possesses straight and quite robust humeri (robusticity index = 6.9) similar to most other quadrupedal platyrrhines able to withstand the frequent action of compressive forces [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). In contrast, Ateles and Brachyteles are characterized by equally straight but more slender shafts (5.2 and 5.0, respectively; Jones 2004 ).

The distolateral crest, where m. brachialis originates, is noticeable and seems to extend rather proximally on the lateral side of the humeral shaft as in other primates which habitually fl ex their elbow [START_REF] Conroy | Primate postcranial remains from the Oligocene of Egypt[END_REF][START_REF] Fleagle | The humerus of Aegyptopithecus zeuxis : a primitive anthropoid[END_REF]. The crest is less evident and more distally located in Ateles [START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF]. At its distal end, the lateral epicondyle is unreduced in Alouatta , but small in Ateles [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF][START_REF] Rosenberger | Adaptive radiation of the ateline primates[END_REF].

The humeral trochlea is shallow and spool-like, with a well-developed medial trochlear lip, and is relatively mediolaterally extended (Fig. 6.11 ), a morphology that facilitates arboreal quadrupedal movements by allowing a certain degree of mediolateral translation [START_REF] Jenkins | The functional anatomy and evolution of the mammalian humeroulnar articulation[END_REF][START_REF] Feldesman | Morphometric analysis of the distal humerus of some Cenozoic catarrhines: the late divergence hypothesis revisited[END_REF][START_REF] Fleagle | The humerus of Aegyptopithecus zeuxis : a primitive anthropoid[END_REF][START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF][START_REF] Rose | Another look at the anthropoid elbow[END_REF][START_REF] Harrison | New postcranial remains of Victoriapithecus from the Middle Miocene of Kenya[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). In contrast, Lagothrix and Ateles possess more cylindrical trochlea with relatively reduced medial lips, morphology associated with well-guided elbow fl exion and extension during suspensory activities [START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF].

Alouatta possesses a transversely ovoid and proximodistally high capitulum (Fig. 6.11 ), which seems to be functionally associated with habitual elbow fl exion and forearm pronation during arboreal quadrupedal movements [START_REF] Feldesman | Morphometric analysis of the distal humerus of some Cenozoic catarrhines: the late divergence hypothesis revisited[END_REF][START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Rose | Another look at the anthropoid elbow[END_REF][START_REF] Harrison | New postcranial remains of Victoriapithecus from the Middle Miocene of Kenya[END_REF][START_REF] Ma | Arboreal quadrupedism and forelimb articular anatomy of red howling monkeys[END_REF]. On the other hand, Lagothrix and Ateles possess a low, well-developed, and more spherical capitulum that provides ample pronosupinatory rotations during elbow excursions [START_REF] Rose | Another look at the anthropoid elbow[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF].

The medial epicondyle of Alouatta is well developed and faces slightly posteromedially but is prominent and medially oriented in Ateles (Fig. 6.11 ;[START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF][START_REF] Feldesman | Morphometric analysis of the distal humerus of some Cenozoic catarrhines: the late divergence hypothesis revisited[END_REF][START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Harrison | New postcranial remains of Victoriapithecus from the Middle Miocene of Kenya[END_REF] ). The overall projection of the condyle increases the leverage of the forearm fl exors and pronators that contribute to arboreal quadrupedal locomotion, and a more posterior direction further enhances the moment of the acting forces in quadrupedalism [START_REF] Jenkins | The functional anatomy and evolution of the mammalian humeroulnar articulation[END_REF][START_REF] Fleagle | The humerus of Aegyptopithecus zeuxis : a primitive anthropoid[END_REF][START_REF] Ma | Arboreal quadrupedism and forelimb articular anatomy of red howling monkeys[END_REF] ).

In the ulna, the olecranon is large and faces anteriorly (Fig. 6.12 ; [START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ) providing enhanced mechanical advantage to the action of mm. triceps during elbow extension and supporting the weight during habitual elbow fl exion [START_REF] Ybarra | Non-metric features in the ulna of Aegyptopithecus, Alouatta, Ateles , and Lagothrix[END_REF][START_REF] Rodman | Skeletal differentiation of Macaca fascicularis and Macaca nemestrina , in relation to arboreal and terrestrial quadrupedalism[END_REF][START_REF] Harrison | New postcranial remains of Victoriapithecus from the Middle Miocene of Kenya[END_REF][START_REF] Ma | Arboreal quadrupedism and forelimb articular anatomy of red howling monkeys[END_REF][START_REF] Rein | Skeletal correlates of quadrupedalism and climbing in the anthropoid forelimb: implications for inferring locomotion in Miocene catarrhines[END_REF][START_REF] Drapeau | Functional anatomy of the olecranon process in hominoids and Plio-Pleistocene hominins[END_REF]. In contrast, it is moderately developed in Lagothrix and relatively reduced in Ateles , as in most forelimb suspensory mammals [START_REF] Drapeau | Functional anatomy of the olecranon process in hominoids and Plio-Pleistocene hominins[END_REF].

The sigmoid notch is relatively wide, proximodistally concave and its axis angles medially and distally, with both proximal borders fl aring proximally [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF] ). These characters indicate the weight-bearing role of the ulna and elbow excursions that are mediolaterally stable with controlled deviation of the forearm for its placement on arboreal substrates [START_REF] Conroy | Primate postcranial remains from the Oligocene of Egypt[END_REF][START_REF] Ybarra | Non-metric features in the ulna of Aegyptopithecus, Alouatta, Ateles , and Lagothrix[END_REF][START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Fleagle | Locomotor behavior and skeletal morphology of two sympatric pithecine monkeys, Pithecia pithecia and Chiropotes satanas[END_REF][START_REF] Harrison | New postcranial remains of Victoriapithecus from the Middle Miocene of Kenya[END_REF][START_REF] Ma | Arboreal quadrupedism and forelimb articular anatomy of red howling monkeys[END_REF]. Additionally, over the coronoid, the surface is fl at and slopes distally; this is related to the habitually fl exed postures of the elbows (Fig. 6.12 ; [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Anapol | Fossil platyrrhine forelimb bones from the early Miocene of Argentina[END_REF]. The sigmoid of Ateles is slightly different, characterized by a weaker angle and being wide, deep, and semicircular with a reduced coronoid process facing anteriorly.

The radial notch is reduced, gently concave, and facing anterolaterally, a condition encountered in most arboreal quadrupedal primates (Fig. 6.12 ; Youlatos 1994 ; Halenar 2011 ). This morphology allows a certain degree of forearm rotation and provides increased stability during pronation [START_REF] Rose | Another look at the anthropoid elbow[END_REF]. In contrast, Ateles possess a large concave notch facing anterolaterally, as in other suspensory primates.

In Alouatta , and to a lesser extent Lagothrix , the ulnar shaft is straight, very robust, and gently concave anteriorly (Fig. 6.12 ). It is ovoid in section and similar to arboreal quadrupedal platyrrhines [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). This morphology withstands the action of high compressive forces, resists the action of the elbow fl exors, and provides space for radial rotations [START_REF] Conroy | Primate postcranial remains from the Oligocene of Egypt[END_REF][START_REF] Fleagle | Locomotor behavior and skeletal morphology of two sympatric pithecine monkeys, Pithecia pithecia and Chiropotes satanas[END_REF]. In contrast, Ateles and Brachyteles are characterized by quite slender shafts that are T-shaped in section [START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). Distally, the Alouatta ulna is characterized by a robust styloid process, which protrudes distally within the wrist joint. This morphology establishes an extended articulation between the ulna and the lateral part of the wrist, assuring wrist stability and resistance to compressive forces at ulnar deviation during quadrupedal activities [START_REF] Lewis | Functional morphology of the evolving hand and foot[END_REF].

Alouatta , and to a lesser extent Lagothrix , possess very robust radii similar to other quadrupedal platyrrhines, implying the action of frequent compressive forces [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Fleagle | Locomotor behavior and skeletal morphology of two sympatric pithecine monkeys, Pithecia pithecia and Chiropotes satanas[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). In contrast, Ateles and Brachyteles are characterized by quite slender shafts [START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF].

The head of the radius is slightly elliptical with a shallow articular facet that is laterally inclined as in most arboreal quadrupedal primates (Fig. 6.13 ; [START_REF] Conroy | Primate postcranial remains from the Oligocene of Egypt[END_REF][START_REF] Rose | Another look at the anthropoid elbow[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). A similar morphology indicates limits to the range of forearm rotation and extended radioulnar and radiohumeral contact during forearm pronation, establishing a locking mechanism for elbow stability [START_REF] Jenkins | The functional anatomy and evolution of the mammalian humeroulnar articulation[END_REF][START_REF] Conroy | Primate postcranial remains from the Oligocene of Egypt[END_REF][START_REF] Rose | Another look at the anthropoid elbow[END_REF][START_REF] Harrison | New postcranial remains of Victoriapithecus from the Middle Miocene of Kenya[END_REF][START_REF] Ma | Arboreal quadrupedism and forelimb articular anatomy of red howling monkeys[END_REF]. Lagothrix and Ateles possess horizontal, more cylindrical radial heads with deep facets that permit articular contact throughout a wide range of forearm rotations [START_REF] Jenkins | The functional anatomy and evolution of the mammalian humeroulnar articulation[END_REF][START_REF] Conroy | Primate postcranial remains from the Oligocene of Egypt[END_REF][START_REF] Rose | Another look at the anthropoid elbow[END_REF].

The bicipital tuberosity, that hosts the insertion of m. biceps brachii , is distally located as in most quadrupedal platyrrhines [START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF]. In contrast, it is rather proximally located in Lagothrix and even more so in Ateles , indicating a short lever arm, which favors rapid and wider forearm movements [START_REF] Harrison | New postcranial remains of Victoriapithecus from the Middle Miocene of Kenya[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ).

The distal radioulnar joint is a distally restricted and anteroposteriorly wide facet hosting a syndesmosis that allows a certain range of forearm rotations [START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF][START_REF] Lewis | Functional morphology of the evolving hand and foot[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. In Ateles , the facet is practically absent, refl ecting the wide range of pronosupination that occurs in the forearm of this suspensory platyrrhine. Distally, Alouatta and Lagothrix have relatively wide radiocarpal articular surfaces (Fig. 6.13 ) that provide wide contact for the carpus to withstand compressive forces. Nevertheless, this facet is still narrower than that of other platyrrhines. In contrast, Ateles possess very narrow distal articular surface, very likely associated with the reduced presence of compressive forces during their habitual suspensory locomotion [START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ).

Alouatta 's wrist is rather short and its relative proportions do not depict any functional specializations, other than generalized quadrupedal activities [START_REF] Godinot | Early euprimate hands in evolutionary perspective[END_REF]. The proximal carpal row, composed of the scaphoid, lunate, triquetrum, and pisiform, is mediolaterally extended and gently curved (Fig. 6.14 ). In Alouatta and Lagothrix , the proximal facets of the scaphoid and lunate are similar to most quadrupedal primates and assure an extended contact with the wide distal radial facet allowing fl exion and extension movements with limited abduction and adduction [START_REF] Jenkins Fa | Knuckle-walking and the functional anatomy of the wrists in living apes[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF][START_REF] Kivell | New primate carpal bones from Rudabanya (late Miocene, Hungary): taxonomic and functional implication[END_REF].

The proximal facets of the triquetrum and pisiform are concave and articulate with the corresponding well-developed distal facets of the styloid process of the ulna (Fig. 6.14 ; Youlatos 1994 ). This morphology, also encountered in Lagothrix and other quadrupedal primates, assures a stable joint during quadrupedal stances when the hand is ulnarly deviated (O 'Connor 1975 ;[START_REF] Beard | Carpal anatomy of Smilodectes gracilis (Adapiformes, Primates) and its signifi cance for lemuriform phylogeny[END_REF][START_REF] Lewis | Functional morphology of the evolving hand and foot[END_REF] ). This stability is further enhanced by the long and robust pisiform which is supported by two ligaments that connect with the palmar tubercle of the hamate and the styloid process of metacarpal V (Grand 1968a ;[START_REF] Ziemer | Functional morphology of the forelimb joints in the woolly monkey Lagothrix lagothricha[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF].

The distal carpal row is composed of the trapezium, trapezoid, capitate, and hamate, which articulate proximally with the distal facets of the proximal carpal row and distally with the metacarpals (Fig. 6.14 ). At the level of the midcarpal joint, the proximal facets of the capitate and hamate of Alouatta and Lagothrix are smoothly curved allowing a certain degree of midcarpal rotation [START_REF] Jenkins Fa | Knuckle-walking and the functional anatomy of the wrists in living apes[END_REF] ; Kivell and Begun 2009 ). Additionally, the capitate bears a dorsal expansion of the proximal facet for the os centrale, similar to that found in Lagothrix , Ateles , and some other suspensory primates, which seem to enhance midcarpal pronosupination [START_REF] Ziemer | Functional morphology of the forelimb joints in the woolly monkey Lagothrix lagothricha[END_REF]. Furthermore, the dorsal facet of the hamate bears a facet for the triquetrum, similar to that of other atelines. This facet allows for the radial rotation of the os centrale over the hamate and increases midcarpal supination [START_REF] Jenkins | Wrist rotation in primates: a critical adaptation for brachiators[END_REF][START_REF] Sarmiento | Anatomy of the hominoid wrist joint: Its evolutionary and functional implications[END_REF][START_REF] Kivell | New primate carpal bones from Rudabanya (late Miocene, Hungary): taxonomic and functional implication[END_REF]. However, a palmar process on the head of the capitate, non-existent in Lagothrix and Ateles , would eventually restrain the extended rotations permitted by the above morphology [START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF].

The ulnoradial direction and proximodistal elongation of the ulnar facet of the hamate, for the triquetrum, is similar to Lagothrix and other quadrupedal primates and is indicative of restricted mobility and enhanced stability for weight bearing [START_REF] Ziemer | Functional morphology of the forelimb joints in the woolly monkey Lagothrix lagothricha[END_REF][START_REF] Beard | Carpal anatomy of Smilodectes gracilis (Adapiformes, Primates) and its signifi cance for lemuriform phylogeny[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF] ). The corresponding facet on the distal surface of the triquetrum is ulnoradially elongated establishing an interlocking mechanism with the hamate in the ulnar side of the wrist [START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF].

Intrinsic hand proportions do not show any functional specializations and fall within the ranges of most arboreal quadrupedal primates (Fig. 6.14 ; [START_REF] Jouffroy | Biometrical characteristics of primate hands[END_REF][START_REF] Godinot | Early euprimate hands in evolutionary perspective[END_REF] ). Alouatta 's metacarpals and phalanges are comparably short and very gently curved, morphology associated with pronograde quadrupedal habits and contrasted with the particularly long and especially curved metacarpals of Ateles and other suspensory primates [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF][START_REF] Jouffroy | Biometrical characteristics of primate hands[END_REF][START_REF] Hamrick | Anthropoid phalanges from the Oligocene of Egypt[END_REF][START_REF] Stern | Quantifying phalangeal curvature: an empirical comparison of alternative methods[END_REF][START_REF] Rosenberger | The making of platyrrhine semifolivores: models for the evolution of folivory in primates[END_REF][START_REF] Rein | The correspondence between proximal phalanx morphology and locomotion: implications for inferring the locomotor behavior of fossil catarrhines[END_REF]. Alouatta also possess a paraxonal hand with digits III and IV having similar lengths, while the functional axis of the hand usually passes through digit III (Fig. 6.14 ;Grand 1968a ;[START_REF] Youlatos | The schizodactylous grasp of the howling monkey[END_REF]. The metacarpal I and trapezium facets are rather fl at, indicating limited excursions of the pollex [START_REF] Napier | Prehensility and opposability in the hands of primates[END_REF][START_REF] Rose | Kinematics of the trapezium-1st metacarpal joint in extant anthropoids and Miocene hominoids[END_REF] ). The pollex is capable of being positioned against the lateral digits mainly because of the arrangement of digits II-V, but advanced rotatory movements, similar to the ones observed in catarrhines are practically impossible [START_REF] Rose | Kinematics of the trapezium-1st metacarpal joint in extant anthropoids and Miocene hominoids[END_REF] ). However, strong manual prehension upon substrates is achieved by frequent use of a zygodactylous grasp (Fig. 6.14 ; Grand 1968a ). Morphologically, this is assured by the convex joint between the capitate and metacarpal II and between the proximal ends of the latter and metacarpal III, which provide enhanced mobility in both the dorsopalmar and radioulnar planes [START_REF] Youlatos | The schizodactylous grasp of the howling monkey[END_REF]. Furthermore, the functional separation of the tendons of m. fl exor digitorum profundus and m. extensor digitorum profundus towards the two pincer arms and the well-developed adductor of digit II probably assure a strong grasp (Youlatos 1999 ).

Hind Limb

In the pelvis, the iliosacral joint is located cranially in Alouatta and the other atelines [START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. The particularly cranial location of the joint increases the distance from the hip joint, providing better leverage for the transmission of the hind limb forces during quadrupedal progression [START_REF] Rodman | Skeletal differentiation of Macaca fascicularis and Macaca nemestrina , in relation to arboreal and terrestrial quadrupedalism[END_REF] ). More cranially, the surface of the insertion of mm. erector spinae is signifi cantly reduced in Alouatta , as in other atelines [START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. A reduced insertion area is functionally associated with the lesser development of these muscles in Alouatta and other climbing primates, as these muscles have been shown instead to contribute to pelvic movements during running [START_REF] Waterman | Studies on the evolution of the pelvis of man and other primates[END_REF][START_REF] Stern | Functional myology of the hip and thigh of Cebid monkeys and its implications for the evolution of erect posture[END_REF]Grand 1968b[START_REF] Grand | Body weight: its relation to tissue composition, segment distribution, and motor function. I. Interspecifi c comparisons[END_REF].

The gluteal surface of the iliac blade is long, wide, concave, and oriented dorsolaterally, presenting an intermediate morphology between the quadrupedal platyrrhines and the more suspensory atelines. The wider and more concave blades in the latter very likely host a well-developed m. gluteus medius , which also contributes to hind limb adduction during quadrupedal climbing and frequent suspensory postures [START_REF] Stern | Functional myology of the hip and thigh of Cebid monkeys and its implications for the evolution of erect posture[END_REF][START_REF] Zuckerman | Some locomotor features of the pelvic girdle in primates[END_REF].

The sciatic area, between the acetabulum and the iliosacral joint, is comparably elongated in Alouatta , as in other atelines, and the distribution of trabecular bone is not very dense, as in most quadrupedal primates [START_REF] Zuckerman | Some locomotor features of the pelvic girdle in primates[END_REF][START_REF] Leutenegger | Functional aspects of pelvic morphology in simian primates[END_REF]. This condition may be related to the action of tensile forces applied during tail and hind limb hanging postures (Grand 1968b ;[START_REF] Zuckerman | Some locomotor features of the pelvic girdle in primates[END_REF].

Alouatta possess a large and shallow acetabulum, similar to that found in other atelines and suspensory/climbing mammals, which allows for a wide range of femoral movements [START_REF] Schultz | Observation on the acetabulum of primates[END_REF][START_REF] Jenkins Fa | Hip structure and locomotion in ambulatory and cursorial carnivores[END_REF]. In addition, it is located rather dorsally and caudally and has equally developed dorsal and ventral buttresses [START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. This morphology very likely refl ects resistance to forces applied equally during pronograde quadrupedal actions and hind limb suspension [START_REF] Fleagle | Anatomy of the bony pelvis in parapithecid primates[END_REF].

The ischium of Alouatta is intermediate in length, between the short ischia of the other atelines and the longer ones of quadrupedal platyrrhines. As relatively long ischia provide a better leverage for rapid retraction of the thighs during quadrupedal activities [START_REF] Smith | Some locomotor adaptations in mammals[END_REF], the intermediate condition of Alouatta probably refl ects slower and more controlled retraction associated with a quadrupedal and climbing repertoire.

The femoral head is more proximally located than the greater trochanter (Fig. 6.15 ). This condition is encountered in most arboreal mammals and allows a greater range of femoral movements at the hip joint [START_REF] Dagosto | Postcranium of Adapis parisiensis and Leptadapis magnus (Adapiformes, Primates)[END_REF] ). However, this position is also related to the femoral neck angle which is a variable character among atelines [START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF]. In all cases, scansorial and climbing mammals tend to possess higher angles, thus placing the head over the trochanter than more quadrupedal forms [START_REF] Halaczek | Reconstructing the locomotor repertoire of Protopithecus brasiliensis . II. Forelimb morphology[END_REF][START_REF] Fleagle | Locomotor behavior and skeletal anatomy of sympatric Malaysian leaf monkeys ( Presbytis obscura and Presbytis melalophos )[END_REF][START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF]. The femoral head is semispherical and extends over the neck of the femur (Fig. 6.15 ). This posterior extension is reduced in Ateles and almost lacking in Lagothrix , and its expansion in Alouatta may be related to its climbing habits as it provides contact between the acetabulum and the head during increased abduction [START_REF] Jenkins Fa | Hip structure and locomotion in ambulatory and cursorial carnivores[END_REF][START_REF] Dagosto | Postcranium of Adapis parisiensis and Leptadapis magnus (Adapiformes, Primates)[END_REF]. The fovea capitis is large and deep and located either on or near the intersection of the meridian and equator (Fig. 6.15 ; [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. Its morphology and position favor abducted and laterally rotated postures of the hind limb used during climbing and hind limb suspension [START_REF] Jenkins Fa | Hip structure and locomotion in ambulatory and cursorial carnivores[END_REF][START_REF] Rose | The skeleton of early Eocene Cantius , oldest lemuriform primate[END_REF].

Alouatta is characterized by a large, deep, and medially oriented trochanteric fossa and a wide intertrochanteric line (Fig. 6.15 ). This arrangement deviates the tendons of mm. obturatores and gemelli to an acute angle that favors wide femoral excursions with rotations and abduction (Grand 1968b ;[START_REF] Jenkins Fa | Hip structure and locomotion in ambulatory and cursorial carnivores[END_REF][START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Bacon | Les os longs du membre pelvien chez les primates Miocènes et plio-pleistocènes: morphologie fonctionnelle, taxinomie, phylogénie[END_REF]. Additionally, the increased depth of the fossa enhances the power of the tendons by elongating their lever arm providing controlled and powerful hip rotations [START_REF] Bacon | Les os longs du membre pelvien chez les primates Miocènes et plio-pleistocènes: morphologie fonctionnelle, taxinomie, phylogénie[END_REF].

The lesser trochanter is large as in other atelines and is medio-posteriorly directed, as in Lagothrix (Fig. 6.15 ). In contrast, Ateles possess a more medially oriented trochanter. This morphology provides a better leverage for the fl exion and lateral rotation of the femur by the action of m. iliopsoas during climbing activities [START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF][START_REF] Ford | Locomotor adaptations of fossil platyrrhines[END_REF].

The femoral shaft is relatively robust, gently convex anteriorly, and anteroposteriorly compressed (Fig. 6.15 ; [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. This morphology, also shared by the other atelines, is functionally related to the action of forces in various planes, as during climbing and suspensory activities [START_REF] Halaczek | Reconstructing the locomotor repertoire of Protopithecus brasiliensis . II. Forelimb morphology[END_REF][START_REF] Godfrey | Adaptive diversifi cation of Malagasy strepsirrhines[END_REF][START_REF] Ruff | Hindlimb articular surface allometry in Hominoidea and Macaca , with comparisons to diaphyseal scaling[END_REF][START_REF] Ruff | Body mass, sexual dimorphism and femoral proportions of Proconsul from Rusinga and Mfangano Islands, Kenya[END_REF].

The distal femur of Alouatta and the other atelines is mediolaterally wide and oriented slightly laterally (Fig. 6.15 ;[START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. This morphology and deviation is indicative of ample movements in different planes and a more abducted position of the knee joint and is also shared with hominoids and lorisoids [START_REF] Halaczek | Reconstructing the locomotor repertoire of Protopithecus brasiliensis . II. Forelimb morphology[END_REF][START_REF] Ciochon | Morphometric analysis of platyrrhine femora with taxonomic implications and notes on two fossil forms[END_REF][START_REF] Dagosto | Postcranium of Adapis parisiensis and Leptadapis magnus (Adapiformes, Primates)[END_REF][START_REF] Tardieu | The functional signifi cance of airorhynchy in Megaladapis[END_REF]. The patellar groove of Alouatta , Ateles , and Lagothrix is relatively deep and wide, similar to that of climbing and suspensory mammals (Fig. 6.15 ; [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. This morphology allows mediolateral excursions at the knee joint, permitting analogous rotations of the tibia to place the hindfoot on the branches [START_REF] Rose | Miocene Hominoid postcranial morphology: monkey-like, ape-like, neither or both?[END_REF][START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF][START_REF] Bacon | Les os longs du membre pelvien chez les primates Miocènes et plio-pleistocènes: morphologie fonctionnelle, taxinomie, phylogénie[END_REF][START_REF] Madar | New Sivapithecus postcranial remains from the Siwaliks of Pakistan[END_REF].

Both femoral condyles are rather circular in profi le implying an extensive range of fl exion and extension in contact with the tibial plateau [START_REF] Rose | Miocene Hominoid postcranial morphology: monkey-like, ape-like, neither or both?[END_REF][START_REF] Tardieu | The functional signifi cance of airorhynchy in Megaladapis[END_REF]. However, the medial condyle is slightly longer anteroposteriorly, narrower, and angled medially and posteriorly (Fig. 6.15 ). This condition refl ects the action of stresses through the medial side of the joint and is indicative of mediolateral rotations and a more abducted knee posture [START_REF] Tardieu | The functional signifi cance of airorhynchy in Megaladapis[END_REF][START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF][START_REF] Bacon | Les os longs du membre pelvien chez les primates Miocènes et plio-pleistocènes: morphologie fonctionnelle, taxinomie, phylogénie[END_REF][START_REF] Rafferty | Articular structure and function in Hylobates , Colobus , and Papio[END_REF]. Finally, Alouatta possesses a very wide and deep intercondylar fossa, a character shared with other climbing primates and mammals. This morphology, in association with the very low intercondylar tibial tubercles, enables mediolateral rotations at the knee joint while keeping the knee fl exed [START_REF] Tardieu | The functional signifi cance of airorhynchy in Megaladapis[END_REF][START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF] ).

In the tibia, the shape of the plateau is rectangular, similar to arboreal quadrupedal primates and not mediolaterally elongated as in most climbing mammals (Fig. 6.16 ). The plateau strongly retrofl exes and overhangs the shaft posteriorly, a condition indicating habitual fl exion of the knee joint (Grand 1968b ;[START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. The tibial facets for the femoral condyles are gently concave with the lateral being longer and narrower than the medial (Fig. 6.16 ). These features refl ect the action of stresses through the medial side of the joint and would favor fl exion and medial rotations of the knee (Grand 1968b ;[START_REF] Tardieu | The functional signifi cance of airorhynchy in Megaladapis[END_REF][START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF].

Additionally, the anterior tibial tuberosity, insertion of the distal tendon of mm. vasti and rectus femoris , is relatively reduced and characterized by the presence of dissipated trabecular fi bers [START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF] ). This morphology is functionally asso- ciated with a controlled role of knee extensors with a reduced lever arm for the tendon's insertion, as well as the presence of multiplanar forces during fl exion and extension of the knee joint.

The tibial shaft is straight, relatively robust, and moderately mediolaterally compressed, as in the other atelines (Fig. 6.16 ). This morphology indicates that major compressive forces act through the medial side of the hind limb and that their action is multidirectional, as encountered during climbing activities [START_REF] Schön-Ybarra | Positional behavior and limb bone adaptations in red howling monkeys ( Alouatta seniculus )[END_REF][START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF]. The fi bula is slender and situated laterally and away from the tibial shaft. This condition is reminiscent of other climbing and hind limb suspensory mammals, providing a wide interosseous membrane for the origin of mm. fl exor digitorum tibialis and fl exor digitorum fi bularis that fl ex the pedal digits for powerful hindfoot grasping (Grand 1968b ;[START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF].

The distal tibiofi bular facet is low and anteroposteriorly wide as in most platyrrhines [START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF]. This condition hosts a synovial articulation that allows a degree of tibiofi bular movement that assures a relatively fl exible talocrural joint [START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF]. The medial malleolus is slightly reduced and fairly medially oriented, similar to the other atelines and most suspensory primates and other mammals (Fig. 6.16 ;[START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF][START_REF] Desilva | A hominoid distal tibia from the Miocene of Pakistan[END_REF]. Additionally, the anterior surface of the tibiotalar facet is wide and lacks a pronounced distal projection in the middle, as in other atelines (Fig. 6.16 ). The combination of these features contributes to ample talocrural movements along multiple planes, assuring wide contact with the talus during fl exion/extension and inversion/eversion [START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF][START_REF] Gebo | The functional morphology of caudal vertebrae in New World monkeys[END_REF][START_REF] Harrison | New postcranial remains of Victoriapithecus from the Middle Miocene of Kenya[END_REF][START_REF] Bacon | Les os longs du membre pelvien chez les primates Miocènes et plio-pleistocènes: morphologie fonctionnelle, taxinomie, phylogénie[END_REF][START_REF] Desilva | A hominoid distal tibia from the Miocene of Pakistan[END_REF].

Alouatta has a moderately high talus, higher than Ateles , indicating comparably less mobility associated with foot inversion and suspensory habits [START_REF] Gebo | Anthropoid origins-the foot evidence[END_REF][START_REF] Gebo | The functional morphology of caudal vertebrae in New World monkeys[END_REF][START_REF] Meldrum | New fossil platyrrhine tali from the early Miocene of Argentina[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). The talar trochlea is large, shallow, and proximodistally wedged as in other atelines. These features provide wide contact of the talus with the tibia throughout fl exion, extension, inversion, and eversion of the foot during climbing activities [START_REF] Dagosto | Postcranium of Adapis parisiensis and Leptadapis magnus (Adapiformes, Primates)[END_REF][START_REF] Langdon | Functional morphology of the Miocene hominoid foot[END_REF][START_REF] Gebo | The functional morphology of caudal vertebrae in New World monkeys[END_REF][START_REF] Lewis | Functional morphology of the evolving hand and foot[END_REF].

The talar neck and head deviate slightly medially, to enable a powerful foot-hold during climbing or pedal suspension against the action of medially directed forces during foot supination [START_REF] Langdon | Functional morphology of the Miocene hominoid foot[END_REF][START_REF] Gebo | The functional morphology of caudal vertebrae in New World monkeys[END_REF]. Furthermore, the talar head exhibits a moderate lateral inclination associated with ample midtarsal movements positioning the navicular and entocuneiform, and thus the hallux, more vertically and enhancing habitual foot supination for powerful foot grasping [START_REF] Conroy | Primate postcranial remains from the Oligocene of Egypt[END_REF] ). Powerful grasping is achieved by the leverage of the well-developed m. fl exor digitorum fi bularis [START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF], which is evident through the deep groove at the posterior side of the talus and at the plantar surface of the sustentaculum tali of the calcaneus. Additionally, midtarsal supination is further facilitated by the confl uent and convex distal talocalcaneal facets on the plantar surface of the head which articulate with the corresponding concave and extended common calcaneal facet on the dorsal surface of the sustentaculum [START_REF] Dagosto | Postcranium of Adapis parisiensis and Leptadapis magnus (Adapiformes, Primates)[END_REF][START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF][START_REF] Gebo | The functional morphology of caudal vertebrae in New World monkeys[END_REF] ). The proximal talocalcaneal facet is long, wide, and gently curved and associates with a long and equally curved proximal calcaneal facet. This morphology, also shared by the other atelines, facilitates extensive talocalcaneal movements and enhances ankle fl exibility during pedal grasping in foot hanging postures [START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF][START_REF] Gebo | The functional morphology of caudal vertebrae in New World monkeys[END_REF][START_REF] Lewis | Functional morphology of the evolving hand and foot[END_REF][START_REF] Meldrum | New fossil platyrrhine tali from the early Miocene of Argentina[END_REF].

The proximal part of the calcaneus is relatively short, as in most medium-sized arboreal primates, and refl ects the leverage for the action of the mm. triceps surae (Fig. 6.17 ; [START_REF] Strasser | Pedal evidence for the origin and diversifi cation of cercopithecid clades[END_REF] ). Their action is further improved by the elongated tuber calcanei, which further increases their insertion angle for increased power and controlled plantar fl exion. Furthermore, the well-developed calcaneal tubercle on the plantar side (Fig. 6.17 ), where m. fl exor digitorum brevis originates, refl ects its powerful action assisting in digital fl exion during foot hanging activities [START_REF] Sarmiento | The signifi cance of the heel process in anthropoids[END_REF].

On the medial surface of the calcaneal body, the sustentaculum tali is protruding and medially inclined. These features contribute to frequent subtalar inversion and midtarsal supination related to habitual climbing activities [START_REF] Gebo | The functional morphology of caudal vertebrae in New World monkeys[END_REF] ). On the lateral surface of the calcaneal body, the peroneal tubercle of Alouatta is large, compared to that of other atelines, refl ecting the important action of mm. peroneus longus and peroneus brevis , responsible for foot eversion during quadrupedal activities [START_REF] Langdon | Functional morphology of the Miocene hominoid foot[END_REF].

Distally, the calcaneocuboid facet is semicircular in shape and relatively shallow, with a well-developed lateral surface. It articulates with a mediolaterally wide calcaneocuboid facet with an equally developed lateral surface on the proximal surface of the cuboid. This morphology enables a certain degree of midtarsal excursions that facilitate mediolateral rotations contributing to foot inversion [START_REF] Langdon | Functional morphology of the Miocene hominoid foot[END_REF][START_REF] Ford | Postcranial adaptations of the earliest platyrrhine[END_REF][START_REF] Strasser | Pedal evidence for the origin and diversifi cation of cercopithecid clades[END_REF][START_REF] Gebo | The functional morphology of caudal vertebrae in New World monkeys[END_REF].

Alouatta and Ateles possess a proximodistally short cuboid, which suggests frequent hindfoot reversal associated with hind limb hanging activities [START_REF] Gebo | The functional morphology of caudal vertebrae in New World monkeys[END_REF][START_REF] Meldrum | New fossil platyrrhine tali from the early Miocene of Argentina[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). The proximodistally wide and robust navicular refl ects the action of compressive forces on the medial side of the foot during climbing and quadrupedal activities [START_REF] Langdon | Functional morphology of the Miocene hominoid foot[END_REF]. In Alouatta , and the other atelines, these two bones articulate via a proximodistally extended facet which enables a wide range of movements between them and contributes to overall midtarsal mobility of the foot [START_REF] Langdon | Functional morphology of the Miocene hominoid foot[END_REF] ). On the distal surface of the navicular, the facets reserved for the cuneiforms are transversely arranged, in a manner similar to most quadrupedal primates.

The facet between the medial cuneiform and metatarsal I is similar to most platyrrhines. The dorsomedial part is ovoid in shape refl ecting an alignment of the hallux in relation to the lateral digits. Additionally, the plantar part is reduced but retains a saddle-shaped facet that stabilizes the articulation during hallucal prehension (Fig. 6.17 ; [START_REF] Szalay | Evolution of hallucial grasping in the primates[END_REF]. This grasping performance is further assured by the relatively elongated and robust metatarsal I, which is achieved by well-developed hallucal musculature, of which the adductors and fl exors represent almost 70 % (Youlatos 1994 ).

Vertebral Column

The vertebral column of Alouatta is longer than that of the other atelines in both number of vertebrae in the thoracic and lumbar region, as well as in relative length, and seems similar in these metrics to quadrupedal Cebus (Fig. 6.18 ; [START_REF] Erikson | Brachiation in New World monkeys and in anthropoid apes[END_REF][START_REF] Johnson | Positional behavior and vertebral morphology in atelines and cebines[END_REF]. This morphology likely provides more fl exibility and lengthens the stride during quadrupedal walking but may also contribute to bridging and clambering maneuvers commonly used by both taxa [START_REF] Slijper | Comparative biologic-anatomical investigations on the vertebral column and spinal musculature of mammals[END_REF].

Alouatta possesses relatively long lumbar vertebral bodies for their size, contrasting with the rather craniocaudally short vertebrae of Ateles [START_REF] Johnson | Positional behavior and vertebral morphology in atelines and cebines[END_REF]. Furthermore, the transverse processes of these vertebrae are oriented approximately perpendicular to the sagittal plane, a character shared with other atelines [START_REF] Ankel | Vertebral morphology of fossil and extant primates[END_REF][START_REF] Johnson | Positional behavior and vertebral morphology in atelines and cebines[END_REF]. These features contribute to a relative fi rmness and resistance to fl exing moments and assure a lumbar region that helps support a hanging animal by the tail and hind limbs [START_REF] Johnson | Positional behavior and vertebral morphology in atelines and cebines[END_REF].

The sacral vertebrae of Alouatta are large with wide neural arches, whose proximal and distal openings are more or less the same height, in contrast to most nonprehensile-tailed primates. However, in Ateles and Lagothrix , the distal opening is even longer than the proximal one, a condition metrically expressed by the sacral index and scoring as high as 112-120 in the latter forms, compared to the 94.4 in Alouatta [START_REF] Ankel | Vertebral morphology of fossil and extant primates[END_REF]. This morphology may be associated with the bulkier nerves that provide a fi ne motor control in the Atelini , compared to that in Alouatta , which uses its tail comparatively less [START_REF] Ankel | Vertebral morphology of fossil and extant primates[END_REF].

More distally, at the caudal region, Alouatta and the other atelines possess several apomorphies that are functionally related to tail prehensility and its extensive use in hanging postures and locomotion. Alouatta possesses a very heavy tail, representing ~6 % of total body weight, where caudal vertebrae represent the major component [START_REF] Grand | Body weight: its relation to tissue composition, segment distribution, and motor function. I. Interspecifi c comparisons[END_REF]. Additionally, while atelines have a relatively long tail for their body size, it is least elongate in Alouatta [START_REF] Rosenberger | Tale of tails: parallelism and prehensility[END_REF]. In effect, howlers have tails that are the same length as their bodies (tail to head body ratio = 0.99 [START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF] ; see also [START_REF] Braza | El araguato rojo ( Alouatta seniculus )[END_REF], while there is a gradient to comparably longer tails from Lagothrix (1.25) towards Ateles (1.38; see also [START_REF] Rosenberger | Tale of tails: parallelism and prehensility[END_REF]. Interestingly, the relative extension of the naked tactile area shows some variation between atelines. Alouatta and Brachyteles possess the greatest relative naked areas (0.41 of total tail length) compared to the shorter areas of Lagothrix and Ateles (0.35 and 0.34, respectively).

In terms of caudal vertebral morphology, Alouatta possesses the least number of caudal vertebrae (~25-26) and total caudal vertebral length, compared to Ateles (~29-30 [START_REF] Ankel | Vertebral morphology of fossil and extant primates[END_REF]German 1982 ;[START_REF] Youlatos | Maîtrise de l'espace et accès aux ressources chez le singe hurleur roux ( Alouatta seniculus ) de la Guyane française: étude morpho-fonctionnelle. PhD Dissertation, Muséum national d'Histoire naturelle, Paris Youlatos D[END_REF][START_REF] Organ | Structure and function of platyrrhine caudal vertebrae[END_REF] )). The caudal region is divided into proximal and distal regions, delineated by the transitional vertebra [START_REF] Ankel | Vertebral morphology of fossil and extant primates[END_REF]. Despite the variability in caudal vertebrae number, all atelines possess a relatively long proximal region characterized by short and high vertebrae articulated by lumbar-like joints that facilitate intrinsic mobility and favor elevation and dorsal fl exion of the tail [START_REF] Ankel | Vertebral morphology of fossil and extant primates[END_REF]. Compared to nonprehensile- tailed primates, the transitional vertebra is located more or less in the same place along tail length in all atelines, indicating a constant relative position (German 1982 ;[START_REF] Organ | Structure and function of platyrrhine caudal vertebrae[END_REF]. Thus, the relatively long proximal caudal region would favor increased mobility and is associated with its frequent engagement in tail-assisted behaviors [START_REF] Ankel | Vertebral morphology of fossil and extant primates[END_REF].

Alouatta , like all atelines and Cebus , possess robust caudal vertebrae (German 1982 ;[START_REF] Lemelin | Comparative and functional myology of the prehensile tail in New World monkeys[END_REF][START_REF] Organ | Structure and function of platyrrhine caudal vertebrae[END_REF], a condition also shared by other prehensiletailed mammals [START_REF] Youlatos | Osteological correlates of tail prehensility in carnivorans[END_REF]. However, within atelines, Ateles has even shorter, more robust vertebrae; this difference is particularly evident in the distal region and more particularly towards the tip of the tail [START_REF] Ankel | Vertebral morphology of fossil and extant primates[END_REF]German 1982 ;[START_REF] Lemelin | Comparative and functional myology of the prehensile tail in New World monkeys[END_REF][START_REF] Organ | Structure and function of platyrrhine caudal vertebrae[END_REF]. These adaptations refl ect the action of frequent and high reaction stresses involving the substrate during extended tail contact and the forces exerted by the powerful m. fl exor caudae longus .

In effect, mm. fl exor and extensor caudae longii are powerful in prehensile-tailed atelines and span fewer caudal vertebrae (4-7 and 7-9, respectively) compared to nonprehensile-tailed primates. This condition assures greater precision in fl exion and extension and more controlled actions [START_REF] Lemelin | Comparative and functional myology of the prehensile tail in New World monkeys[END_REF]. Additionally, the mm. intertransversarii caudae , which are the primary lateral tail fl exors and rotators, are bulkier in mass and show higher physical cross section area (PCSA) in prehensiletailed primates, which refl ects greater force while maximizing tail contact with the substrate. In Alouatta , however, this muscle is not as developed as in other atelines [START_REF] Lemelin | Comparative and functional myology of the prehensile tail in New World monkeys[END_REF][START_REF] Organ | Functional correlates of fi ber architecture of the lateral caudal musculature in prehensile and nonprehensile tails of the platyrrhini (Primates) and Procyonidae (Carnivora)[END_REF].

This difference within atelines is skeletally evident in the transverse processes of the caudal vertebrae, whereupon insert mm. fl exor caudae longus and intertransversarii caudae . They are large in atelines compared to those of other platyrrhines, but within the group, Alouatta possess the narrowest processes [START_REF] Ankel | Vertebral morphology of fossil and extant primates[END_REF]German 1982 ;[START_REF] Lemelin | Comparative and functional myology of the prehensile tail in New World monkeys[END_REF][START_REF] Jones | The evolution of brachiation in atelines: a phylogenetic comparative study[END_REF] ). These muscles fl ex the tail and provide for an enhanced grasp between the distal part of the tail and the substrate while resisting the torsion exerted during tail-assisted locomotion [START_REF] Lemelin | Comparative and functional myology of the prehensile tail in New World monkeys[END_REF]. Their morphology in Alouatta may refl ect their comparably reduced role in such tail-assisted suspensory activities.

Alouatta Anatomy

The above review of the cranial, dental, hyoid, and postcranial anatomy of Alouatta highlights the distinctive morphology of the genus, compared to other atelines and the other platyrrhines as well. The skull of Alouatta is quite unique among platyrrhines and reveals strong adaptations to a combination of increased folivory and enhanced sound production. The former is strongly indicated by the arrangement and morphology of the teeth, while the latter is even more prominently evident in the highly modifi ed hyoid bone. Finally, the postcranial skeleton reveals a body plan adapted to above-branch quadrupedal movements with relative arm protraction, abducted forelimbs, and relative stability at the forearm and wrist joints to withstand compressive forces from the substrate. On the other hand, the hind limb refl ects adaptations to increased fl exion, extension, and abduction, with the capacity for knee rotation and strong fl exion and powerful foot grasping. These movements accommodate propulsion as well as a frequent use of suspensory postural behavior, aided by the modifi cations of the lumbar and caudal parts of the axial skeleton.

This suite of morphological modifi cations was further substantiated by quantitative analyses of the skull and hyoid bone, which represent the most noticeably derived areas of the skeleton. Alouatta is the only extant representative of a group of alouattines that has changed signifi cantly since their divergence from the basal ateline stock at least 15.5 MA, as indicated by molecular and paleontological data [START_REF] Rosenberger | Adaptive radiation of the ateline primates[END_REF][START_REF] Cortés-Ortiz | Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta[END_REF][START_REF] Hartwig | Implications of molecular and morphological data for understanding ateline phylogeny[END_REF][START_REF] Jones | The evolution of brachiation in ateline primates, ancestral character states and history[END_REF] ). This group followed a very distinct evolutionary path from the ancestral stock and the rest of the atelines, which resulted in a very different activity strategy and remarkable morphobehavioral adaptations that currently characterize the genus as a whole. These adaptations are functionally linked to four major behavioral axes: variable but generally increased rates of folivory, enhanced sound production, decreased daily ranges, and emphasis on an above-branch quadrupedal positional repertoire [START_REF] Rosenberger | Adaptive radiation of the ateline primates[END_REF][START_REF] Rosenberger | The making of platyrrhine semifolivores: models for the evolution of folivory in primates[END_REF][START_REF] Rosenberger | Fossil Alouattines and the origin of Alouatta: craniodental diversity and interrelationships[END_REF]. These axes are strongly interrelated and very likely evolved in parallel. The simultaneous shift of Alouatta 's diet to one focused on leaves, a nutrient-poor food source that imposes important developmental and ontogenetic constraints and also benefi ts from an energy-minimizing strategy with extended periods of resting for digestion and cautious locomotion, as well as avoidance of costly intergroup violence by the development of an impressive sound production mechanism, probably accounts for the particularly derived skeletal morphology of Alouatta . Given the more fl exible and ateline-like anatomy and behavior of the last common ancestor of Alouatta and the rest of the atelines [START_REF] Jones | The evolution of brachiation in ateline primates, ancestral character states and history[END_REF][START_REF] Halenar | Paleobiology of Protopithecus brasiliensis , a plus-size Pleistocene platyrrhine from Brazil[END_REF][START_REF] Rosenberger | Fossil Alouattines and the origin of Alouatta: craniodental diversity and interrelationships[END_REF] ), it appears that Alouatta evolved a mosaic of cranial and postcranial features that promoted this novel morphobehavioral strategy. Adaptations to these unusual patterns very likely evolved prior to the wide geographic dispersal of howlers in Central and South America and probably contributed to the successful invasion of divergent forested habitats from the northern Mesoamerican wet and dry forests to the seasonal forests of the northern parts of the southern cone [START_REF] Rosenberger | Platyrrhine ecophylogenetics in space and time[END_REF] ) .

Fig. 6 . 1

 61 Fig. 6.1 Set of the 55 landmarks defi ned on the skull. Bilateral landmarks were digitized on the left side only and mirrored (see Table6.1 for landmark defi nitions). Dashed lines illustrate wireframes used for shape variation visualizations

Fig. 6

 6 Fig. 6.2 ( a ) PCA results for the analysis of cranial variation at the genus level. Alouatta cranial morphology is clearly different from that of the other atelines; ( b ) polarization of the morphologies described by the negative ( gray ) and positive ( black ) values of PC1 and PC2 for the analysis of cranial variation at the genus level (on the left ). Superimposition of the extreme morphologies of each axis (on the right )

Fig. 6 . 4

 64 Fig. 6.4 Occlusal views of the upper dentition ( left ) and lower dentition ( right ) of male Alouatta (third upper molar length = 5.8 mm; third lower molar length = 7.5 mm)

Fig. 6 . 5

 65 Fig. 6.5 Landmarks recorded on the hyoid. Images are from Landmark Editor , showing points and curves on a typical male A. seniculus hyoid in (from left to right ) anterior, lateral, and posterior views

Fig. 6 . 6

 66 Fig. 6.6 Interspecifi c variation in hyoid shape across Alouatta , lateral ( a , top ) and posterior ( b , bottom ) views. Images are .ply fi les created from laser surface scans of individual specimens (see Materials and Methods-ragged edges around the posterior opening of the hyoid are an artifact of the scan editing process) chosen from the hyoid sample as typical representatives of each species and scaled to similar size to emphasize shape differences. Top row in each view are males, bottom row are females ( A. pigra female is mislabeled as a male)

Fig. 6

 6 Fig.6.7 PCA results for the hyoid. Sample includes males and females of all species of Alouatta and three Lagothrix individuals. PC1 (37 % total variance) separates A. seniculus from the other species as the most bulbous with the smallest posterior opening. PC2 (18 %) separates males, individuals towards the positive end of the axis, from females, individuals towards the negative end (also see Fig.6.8 ). PC2 is also somewhat related to geographic differences within the A. seniculus and A. caraya samples. The gray polygon bounds the subset of the A. seniculus sample not from Colombia. The A. caraya individuals bounded by the gray polygon are from Bolivia, while those bounded in black are from Brazil. Wireframes show the curves on the basihyal in lateral view with the anterior portion of the bone facing to the right to more easily visualize the shape change along PC1 and the difference between males and females of each species (see Fig.6.5 )

Fig. 6

 6 Fig. 6.8 PCA results for the hyoid using the Alouatta sample, PC1 vs. PC3. When the Lagothrix individuals are excluded from the sample, PC3 (9 % total variance) separates A. palliata from A. caraya . PC1 (39 %) is still driven by the contours of the inferior portion of the basihyal as well as the dimensions of the posterior opening and tentorium. Wireframes show the hyoid in posterior view, again to visualize the shape differences between the species

Fig. 6 .

 6 Fig. 6.10 Lateral view ( left ) and proximal view ( right ) of the scapula of A. seniculus (glenoidmidaxillary border length is 71.4 mm) showing the enlargement of the suprascapular fossa, the development of the acromion, the distal extension of the coracoid process joining the cranial end of the suprascapular fossa via a large ligament ( left ), and the oblong shape of the glenoid fossa ( right )

Fig. 6 .

 6 Fig. 6.11 Humeral features of Alouatta : narrow proximal humeral head ( top left ), wide bicipital groove and reduced humeral tuberosities ( top right ), protruding medial condyle and shallow olecranon fossa ( bottom left ), wedged trochlea, and ovoid capitulum ( bottom right ) (humeral head width = 16.4 mm; distal epiphysis width = 28.5 mm)

Fig. 6 .

 6 Fig. 6.12 Radial view of the ulna of Alouatta (ulna length = 176.3 mm) showing the gentle anterior curvature of the shaft, the robust straight olecranon proximally, and the prominent styloid distally ( left ); the distally inclined shallow sigmoid and the gently concave radial notch in closer views ( right )

Fig. 6 .

 6 Fig. 6.13 Ulnar view of the proximal part of the radius (radial length = 160.9 mm), showing the inclination of the head and the extended articular facet for the radial notch ( left ), proximal view of the ovoid and shallow radial head (radial head length = 12.8 mm) ( right top ), and distal view of the broad radiocarpal facet ( bottom right )

Fig. 6 .

 6 Fig. 6.14 Radiograph of the hand of Alouatta , showing the arrangement of the proximal and distal carpal rows, with the well-developed heads of the capitate and hamate, the well-developed pisiform ulno-proximally , and the extended contact between the distal capitate, and proximal ends of metacarpal II and metacarpal III that accommodate the zygodactylous grasp (metacarpal III length = 33.7 mm)

Fig. 6 .

 6 Fig. 6.15 Anterior view of the femur of Alouatta ( left ; femur length = 154.2 mm); posterior view of proximal femur showing the head and the greater and lesser trochanters ( top middle ); medial view of the femoral head showing the position of the fovea capitis ( top right ); proximal view of the head and trochanter showing their arrangement ( center middle ); distal view of the knee joint, showing its shape, the depth of the trochlea, and the relative extent and width of the condyles ( center right ); posterior view of the distal femur showing the condyles ( bottom middle ); anterior view of the trochlea showing its shape and its borders ( bottom right )

Fig. 6 .

 6 Fig. 6.16 Anterior view of the tibia and fi bula of Alouatta (left; tibia length = 139.3 mm), proximal view of the rectangular tibial plateau ( top right ), and distal view of the wide talocrural joint and the direction of the medial malleolus ( bottom right )

Fig. 6 .

 6 Fig. 6.17 Dorsal view of the foot of A. seniculus showing the divergent hallux ( bottom ; metatarsal III length = 35.4 mm) and the metatarsal I medial cuneiform joint ( top )

Fig. 6 .

 6 Fig. 6.18 Radiograph of the vertebral column of Alouatta showing the different vertebral regions (length of last sacral vertebra = 21.6 mm)

Table 6 .1

 6 List of the 55 landmarks used for the analyses of cranial variations (consult Fig.6.1 for visualizations)

Table 6 .2

 6 Extant sample for hyoid measurements

					Hyoid
	Genus	Species	Subspecies a	Country	M	F
	Alouatta	belzebul	belzebul	Brazil		7
				N		7
	Alouatta	caraya		Brazil		6
				Bolivia		6
				N		12
	Alouatta	guariba	guariba	Brazil (NE)		2
	Alouatta	guariba	clamitans	Brazil (SE)		4
				N		6
	Alouatta	palliata	palliata	El Salvador		1
	Alouatta	palliata	aequatorialis	Panama		-
				N		1
	Alouatta	pigra		Guatemala		1
				N		1
	Alouatta	seniculus		Bolivia		4
				Brazil		-
	Alouatta	seniculus	seniculus	Colombia		22
				Peru		2
	Alouatta	seniculus	straminea b	Guyana		2
				N		30
	Lagothrix	lagotricha	lagotricha	Colombia		-
	Lagothrix	lagotricha	lugens	Colombia		-
				N		0

a Taxonomic allocation and provenance taken from specimen boxes b Currently recognized as A. macconnelli

Acknowledgments All authors wish to thank the editors for inviting us to participate in this exciting volume, thus giving us the opportunity to contribute our knowledge on specifi c issues of the morphology of howler monkeys. This work would not have been possible without the funding provided by the Muséum national d'Histoire naturelle and the Centre National de la Recherche Scientifi que, France; the Aristotle University of Thessaloniki and the State Scholarship Foundation, Greece; and the National Science Foundation. Advice provided by Jeffrey Laitman, Alfred Rosenberger, and Eloïse Zoukouba is much appreciated by the authors.