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Morphology of Howler Monkeys: A Review and Quantitative Analyses

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Howler Monkeys

Part of the book series: Developments in Primatology: Progress and Prospects ((DIPR))

Abstract

Recognition of a particularly derived eco-behavioral strategy for the genus Alouatta has been crucial for studying and understanding its equally derived cranial and postcranial morphology. The unique architecture of the skull and mandible has very likely evolved in relation to both masticatory correlates associated with an increasingly folivorous diet as well as the use of vocal communication associated with social behavior and an energy-minimizing strategy. Comparisons of cranial morphology using three-dimensional geometric morphometrics have highlighted significant interspecific shape differences. Alouatta seniculus is the most divergent in both cranial and hyoid morphology and exhibits the most pronounced levels of sexual dimorphism in those areas. Cranial variability is expressed in facial prognathism and airorhynchy, basicranial flexure, and zygomatic height. Inter- and intraspecific differences based on these axes of variation are very likely linked to interspecific variations in diet, behavior, and life history. This is further evident in the dental anatomy of the genus, indicating adaptations to a shift to a more folivorous diet. In addition, recent studies provide further evidence for significant inter- and intraspecific variations in hyoid size and shape. Alouatta seniculus possesses the largest and most inflated hyoid bulla, and the species that occupy distributional extremes (A. palliata, A. caraya) are differentiated by highly distinct hyoid shapes. These data indicate a complex relationship between morphology and behavior, with possible biogeographic implications. In terms of postcranial morphology, 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. Interspecific 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 significativas inter-específicas 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 dimorfismo sexual en esas áreas. La variabilidad craneal es expresada en el prognatismo facial y airorrinchia, flexión basocraneal y altura zigomática. Diferencias inter- e intra-específicas basadas en estos ejes de variación están muy posiblemente vinculadas a variaciones interespecíficas 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 intraespecífica significativas en la forma y el tamaño del hueso hioides. Alouatta seniculus posee la bula más larga e inflada 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 biogeográficas. 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 interespecífica 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.

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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 specific 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 Scientifique, 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.

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Authors and Affiliations

  1. Department of Zoology, School of Biology, Aristotle University of Thessaloniki, Thessaloniki, Greece

    Dionisios Youlatos

  2. Ecole Pratique des Hautes Etudes, Laboratoire Paléobiodiversité et Evolution & UMR uB/CNRS 6282 “Biogéosciences”, Dijon, France

    Sébastien Couette

  3. Department of Biological Sciences, Bronx Community College, The City University of New York, 2155 University Avenue, Bronx, NY, 10453, USA

    Lauren B. Halenar

  4. New York Consortium in Evolutionary Primatology (NYCEP), The City University of New York, New York, NY, USA

    Lauren B. Halenar

Authors
  1. Dionisios Youlatos
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  2. Sébastien Couette
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  3. Lauren B. Halenar
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Correspondence to Dionisios Youlatos .

Editor information

Editors and Affiliations

  1. Estación Biológica Corrientes, Museo Argentino de Ciencias Naturales, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Martín M. Kowalewski

  2. Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA

    Paul A. Garber

  3. Museum of Zoology, Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA

    Liliana Cortés-Ortiz

  4. Centro de Antropología, Instituto Venezolano de Investigaciones Científicas, Caracas, Venezuela

    Bernardo Urbani

  5. Department of Zoology, Aristotle University of Thessalonik, Thessaloniki, Greece

    Dionisios Youlatos

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Youlatos, D., Couette, S., Halenar, L.B. (2015). Morphology of Howler Monkeys: A Review and Quantitative Analyses. In: Kowalewski, M., Garber, P., Cortés-Ortiz, L., Urbani, B., Youlatos, D. (eds) Howler Monkeys. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1957-4_6

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