Fossil Alouattines and the Origins of Alouatta: Craniodental Diversity and Interrelationships

  • Alfred L. Rosenberger
  • Siobhán B. Cooke
  • Lauren B. Halenar
  • Marcelo F. TejedorEmail author
  • Walter C. Hartwig
  • Nelson M. Novo
  • Yaneth Muñoz-Saba
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


The howler monkey clade includes species of Alouatta and four extinct genera, Stirtonia, Paralouatta, Protopithecus, and probably Solimoea as well. Contrary to expectations, this radiation may have originated as a largely frugivorous group; advanced, Alouatta-like leaf-eating is a novelty well-developed in the Alouatta-Stirtonia sublineage only. Revised body mass estimates place Stirtonia and Paralouatta within the size range exhibited by the living forms and confirm the place of Protopithecus in a larger, baboon-like size range. While their dentitions are more primitive than the Alouatta-Stirtonia pattern, the cranial anatomy of Protopithecus and Paralouatta is distinctly similar to living howler monkeys in highly derived features relating to enlargement of the subbasal space in the neck and in head carriage, suggesting that ancestral alouattines may have had an enlarged hyolaryngeal apparatus. All alouattines also have relatively small brains, including Protopithecus, a genus that was probably quite frugivorous. The successful origins of the alouattine clade may owe more to key adaptations involving communication and energetics than dental or locomotor breakthroughs. While the fossil record confirms aspects of previous character-analysis reconstructions based on the living forms, alouattines experienced a complexity of adaptive shifts whose history cannot be recoverable without a more complete fossil record.*


Fossil primates Howler monkeys Craniodental morphology Adaptation Phylogeny 





Computed Tomography


For example






In other words




First lower molar


Third lower molar


First upper molar


Millions of years




New World monkeys


Third upper premolar


Fourth lower premolar


Fourth upper premolar


El clado de los monos aulladores incluye las especies de Alouatta y cuatro géneros extintos, Stirtonia, Paralouatta, Protopithecus y probablemente Solimoea. Contrario a las expectativas, esta radiación pudo haberse originado a partir de hábitos frugívoros. La avanzada folivoría de Alouatta es una novedad desarrollada solamente en el sublinaje de Alouatta-Stirtonia. Las estimaciones de masa corporal ubican a Stirtonia y Paralouatta dentro del rango que exhiben las formas vivientes y confirman la posición de Protopithecus en un rango de tamaño mayor, similar al de los babuinos africanos. Considerando que la dentición es más primitiva que el patrón observado en Alouatta-Stirtonia, la anatomía craneana de Protopithecus y Paralouatta es similar a la de los aulladores vivientes debido a los rasgos altamente especializados relacionados al agrandamiento del espacio sub-basal en el cuello, así como en la posición de la cabeza, sugiriendo que los alouatinos ancestrales pudieron haber tenido un gran aparato hiolaríngeo. Todos los alouatinos también presentan un cerebro pequeño, incluyendo Protopithecus, género que probablemente haya sido frugívoro. El origen exitoso del clado de los alouatinos pudo deberse más a adaptaciones de comunicación y energéticas que a cambios dentarios o locomotores. Mientras que el registro fósil confirma ciertos aspectos de análisis de caracteres previos basados en formas vivientes, los alouatinos experimentaron una complejidad de adaptaciones cuya historia no podría reconstruirse sin el registro fósil.*

* Since this chapter was written, additional study by Halenar and Rosenberger (2013) of the material discussed here as Protopithecus led to the conclusion that the two samples actually represent two different genera. The essentially complete Bahian skeleton, which forms the basis of the present discussion, is being assigned to a new genus and species, Cartelles coimbrafilhoi, within subfamily Alouattinae. The original Lund material from Minas Gerais bears the original name Protopithecus, but its affinities are more likely to be found among atelines than alouattines.



We owe much to many: to the editors of this volume for inviting us to contribute; to the museums mentioned above that make our research possible, especially our home institution, the American Museum of Natural History; to Leandro Salles and Castor Cartelle and their museums, MNRJ and PUC MINAS, for making this project possible; to Marilyn Norconk for sharing her insights on platyrrhines; to Andi Jones and Mike Rose for discussions on the Brazilian fossils and use of their photographs; to the agencies at Brooklyn College (Tow) and the City University of New York (PSC CUNY) for financial assistance to ALR; to the Wenner-Gren Foundation and CUNY NYCEP for a postdoctoral fellowship awarded to MFT which helped support our collaboration; and to NSF DDIG awards to LBH (0925704) and SBC (0726134) and an Alumnae Association of Barnard College Graduate Fellowship to help support SBC in her research on Caribbean primates. We thank the reviewers and editors for many helpful suggestions. The software package PAST was employed for several computations and charts (


  1. Anthony MRL, Kay RF (1993) Tooth form and diet in ateline and alouattine primates: reflections on the comparative method. Am J Sci 293:356–382CrossRefGoogle Scholar
  2. Biegert J (1963) The evaluation of characteristics of the skull, hands and feet for primate taxonomy. In: Washburn SL (ed) Classification and human evolution. Aldine, ChicagoGoogle Scholar
  3. Cartelle C, Hartwig WC (1996) A new extinct primate among the Pleistocene megafauna of Bahia, Brazil. Proc Natl Acad Sci U S A 93:6405–6409PubMedCentralPubMedCrossRefGoogle Scholar
  4. Clutton-Brock TH, Harvey PH (1980) Primates, brains and ecology. J Zool 207:151–169Google Scholar
  5. Cole TM (1995) Comparative craniometry of the Atelinae (Platyrrhini, Primates): function, development, and evolution. PhD Dissertation. State University of New York at Stony Brook, New YorkGoogle Scholar
  6. Conroy GC (1987) Problems of body-weight estimation in fossil primates. Int J Primatol 8:115–137CrossRefGoogle Scholar
  7. Cooke SB, Halenar LB (2012) The evolution of body size in the Caribbean primates (Abstract). International Primatological Society meetings, 13 August 2012, CancunGoogle Scholar
  8. Delson E, Rosenberger AL (1984) Are there any anthropoid primate living fossils? In: Eldredge N, Stanley SM (eds) Living fossils. Springer, New YorkGoogle Scholar
  9. DiFiore A, Campbell C (2007) The Atelines: Variation in ecology, behavior, and social organization. In: Campbell C, Fuentes A, MacKinnon K, Panger M, Bearder S (eds) Primates in Perspective. New York, Oxford University PressGoogle Scholar
  10. Eaglen RH (1984) Incisor size and diet revisited: the view from a platyrrhine perspective. Am J Phys Anthropol 64:263–275PubMedCrossRefGoogle Scholar
  11. Eisenberg JF (1981) The mammalian radiations. University of Chicago, ChicagoGoogle Scholar
  12. Fleagle JG (1999) Primate adaptation and evolution. Academic, New YorkGoogle Scholar
  13. Fleagle JG, Kay RF, Anthony MRL (1997) Fossil New World monkeys. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ (eds) The history of a Neotropical Fauna: vertebrate paleobiology of the Miocene of tropical South America. Smithsonian Institution, Washington, DCGoogle Scholar
  14. Flynn JJ, Guerrero J, Swisher CC (1997) Geochronology of the Honda group, Columbia. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ (eds) The history of a Neotropical fauna: vertebrate paleobiology of the Miocene of tropical South America. Smithsonian Institution, Washington, DCGoogle Scholar
  15. Ford SM, Corruccini RS (1985) Intraspecific, interspecific, metabolic and phylogenetic scaling in platyrrhine primates. In: Jungers WL (ed) Size and scaling in primate biology. Plenum, New YorkGoogle Scholar
  16. Gould SJ (1977) Ontogeny and phylogeny. Harvard University, CambridgeGoogle Scholar
  17. Halenar LB (2008) Agreement between interspecific variation in vocalization patterns and cranial base morphology in Alouatta: preliminary results and future directions (Abstract). Am J Phys Anthropol (Suppl. 46):111Google Scholar
  18. Halenar LB (2011a) Reconstructing the locomotor repertoire of Protopithecus brasiliensis. I. Body size. Anat Rec 294:2024–2047CrossRefGoogle Scholar
  19. Halenar LB (2011b) Reconstructing the locomotor repertoire of Protopithecus brasiliensis. II. Forelimb morphology. Anat Rec 294:2048–2063CrossRefGoogle Scholar
  20. Halenar LB (2012) Paleobiology of Protopithecus brasiliensis, a plus-sized Pleistocene Platyrrhine from Brazil. PhD Dissertation, CUNY Graduate Center, New YorkGoogle Scholar
  21. Halenar, LB, Rosenberger, AL (2013) A closer look at the “Protopithecus” fossil assemblages: new genus and species from Bahia, Brazil. J Hum Evol 65:374–390Google Scholar
  22. Hartwig WC (1995) A giant New World monkey from the Pleistocene of Brazil. J Hum Evol 28:189–196CrossRefGoogle Scholar
  23. Hartwig WC (1996) Perinatal life history traits in New World monkeys. Am J Primatol 40:99–130CrossRefGoogle Scholar
  24. Hartwig WC (2005) Implications of molecular and morphological data for understanding atelid phylogeny. Int J Primatol 26:999–1015CrossRefGoogle Scholar
  25. Hartwig WC, Cartelle C (1996) A complete skeleton of the giant South American primate Protopithecus. Nature 381:307–311PubMedCrossRefGoogle Scholar
  26. Hartwig W, Meldrum DJ (2002) Miocene platyrrhines of the northern Neotropics. In: Hartwig WC (ed) The primate fossil record. Cambridge University, CambridgeGoogle Scholar
  27. Hartwig WG, Rosenberger AL, Norconk M, Young Owl M (2011) Relative brain size, gut size and evolution in New World monkeys. Anat Rec 294:2207–2221CrossRefGoogle Scholar
  28. Harvey PH, Clutton-Brock TH (1985) Life history variation in primates. Evolution 39:559–581CrossRefGoogle Scholar
  29. Hershkovitz P (1970) Notes on Tertiary platyrrhine monkeys and description of a new genus from the late Miocene of Colombia. Folia Primatol 12:1–37PubMedCrossRefGoogle Scholar
  30. Hershkovitz P (1972) The recent mammals of the Neotropical Region: a zoogeographic and ecological review. In: Keast A, Erk FC, Glass B (eds) Evolution, mammals, and southern continents. State University of New York, AlbanyGoogle Scholar
  31. Hershkovitz P (1977) Living New World monkeys (Platyrrhini), with an introduction to the primates, vol 1. University of Chicago, ChicagoGoogle Scholar
  32. Hodgson JA, Sterner KN, Matthews LJ, Burrell AS, Jania RA, Raaum RL, Stewart C-B, Disotell TR (2009) Successive radiations, not stasis, in the South American primate fauna. Proc Natl Acad Sci U S A 106:5534–5539PubMedCentralPubMedCrossRefGoogle Scholar
  33. Horovitz I, MacPhee RDE (1999) The quaternary Cuban platyrrhine Paralouatta varonai and the origin of the Antillean monkeys. J Hum Evol 36:33–68PubMedCrossRefGoogle Scholar
  34. Jerison HJ (1973) Evolution of the brain and intelligence. Academic, New YorkGoogle Scholar
  35. Jones AL (2008) The evolution of brachiation in ateline primates, ancestral character states and history. Am J Phys Anthropol 137:123–144PubMedCrossRefGoogle Scholar
  36. Kay RF (1975) The functional adaptations of primate molar teeth. Am J Phys Anthropol 43:195–216PubMedCrossRefGoogle Scholar
  37. Kay RF, Cozzuol MA (2006) New platyrrhine monkeys from the Solimoes Formation (late Miocene, Acre State, Brazil). J Hum Evol 50:673–686PubMedCrossRefGoogle Scholar
  38. Kay RF, Frailey CD (1993) Large fossil platyrrhines from the Rio Acre local fauna, late Miocene, western Amazonia. J Hum Evol 25:319–327CrossRefGoogle Scholar
  39. Kay RF, Hylander WI (1978) The dental structure of mammalian folivores with special reference to Primates and Phalangeroidea (Marsupialia). In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Institution, Washington, DCGoogle Scholar
  40. Kay RF, Madden R, Plavcan JM, Cifelli RL, Diaz JG (1987) Stirtonia victoriae, a new species of Miocene Colombian primate. J Hum Evol 16:173–196CrossRefGoogle Scholar
  41. Kay RF, Johnson D, Meldrum DJ (1998) A new pitheciin primate from the middle Miocene of Argentina. Am J Primatol 45:317–336PubMedCrossRefGoogle Scholar
  42. Kinzey WG (1992) Dietary adaptations in the Pitheciinae. Am J Phys Anthropol 88:499–514PubMedCrossRefGoogle Scholar
  43. Krupp A, Cartelle C, Fleagle JG (2012). Size and external morphology of the brains of the large fossil platyrrhines Protopithecus and Caipora. (Abstract) Am J Phys Anthropol (Suppl. 54):186Google Scholar
  44. Lund PW (1838) Blik paa Brasiliens dyreverden for sidste jordomvaeltning. Det Kongelige Danske Videnskabernes Selskabs Naturvidenskabelige og Mathematiske Afhandlinger 8:61–144Google Scholar
  45. MacPhee RDE, Horovitz I (2002) Extinct quaternary platyrrhines of the Greater Antilles and Brazil. In: Hartwig WC (ed) The primate fossil record. Cambridge University, CambridgeGoogle Scholar
  46. MacPhee RDE, Horovitz I (2004) New craniodental remains of the Quaternary Jamaican monkey Xenothrix mcgregori (Xenotrichini, Callicebinae, Pitheciidae), with a reconsideration of the Aotus hypothesis. Am Mus Novitates 3434:1–51CrossRefGoogle Scholar
  47. MacPhee RDE, Iturralde-Vinent MA (1995) Origin of the Greater Antillean land mammal fauna, 1: new Tertiary fossils from Cuba and Puerto Rico. Am Mus Novitates 3141:1–32Google Scholar
  48. MacPhee RDE, Meldrum J (2006) Postcranial remains of the extinct monkeys of the Greater Antilles (Platyrrhini, Callicebinae, Xenotrichini), with a consideration of semiterrestriality in Paralouatta. Am Mus Novitates 3516:1–65CrossRefGoogle Scholar
  49. MacPhee RDE, Horovitz I, Arredondo O, Vasquez OJ (1995) A new genus for the extinct Hispaniolan monkey Saimiri bernensis Rimoli, 1977, with notes on its systematic position. Am Mus Novitates 3134:1–21Google Scholar
  50. MacPhee RDE, Iturralde-Vinent M, Gaffney ES (2003) Domo de Zaza, an early Miocene vertebrate lin South-Central Cuba, with notes on the tectonic evolution of Puerto Rico and the Mona Passage. Am Mus Novitates 3394:1–42CrossRefGoogle Scholar
  51. Martin RD (1984) Body size, brain size and feeding strategies. In: Chivers D, Wood B, Bilsborough A (eds) Food acquisition and processing in primates. Plenum, New YorkGoogle Scholar
  52. Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Chapman and Hall, LondonGoogle Scholar
  53. Opazo JC, Wildman DE, Prychitko T, Johnson RM, Goodman M (2006) Phylogenetic relationships and divergence times among New World monkeys (Platyrrhini, Primates). Mol Phylo Evol 40:274–280CrossRefGoogle Scholar
  54. Rivero M, Arredondo O (1991) Paralouatta varonai, a new quaternary platyrrhine from Cuba. J Hum Evol 21:1–11CrossRefGoogle Scholar
  55. Rosenberger AL (1980) Gradistic views and adaptive radiation of platyrrhine primates. Z Morphol Anthropol 71:157–163PubMedGoogle Scholar
  56. Rosenberger AL (1992) Evolution of feeding niches in new world monkeys. Am J Phys Anthropol 88:525–562PubMedCrossRefGoogle Scholar
  57. Rosenberger AL (2002) Platyrrhine paleontology and systematics: the paradigm shifts. In: Hartwig WC (ed) The primate fossil record. Cambridge University, CambridgeGoogle Scholar
  58. Rosenberger AL, Kinzey WG (1976) Functional patterns of molar occlusion in platyrrhine primates. Am J Phys Anthropol 45:281–298PubMedCrossRefGoogle Scholar
  59. Rosenberger AL, Strier KB (1989) Adaptive radiation of the ateline primates. J Hum Evol 18:717–750CrossRefGoogle Scholar
  60. Rosenberger AL, Setoguchi T, Shigehara N (1990) The fossil record of callitrichine primates. J Hum Evol 19:209–236CrossRefGoogle Scholar
  61. Rosenberger AL, Halenar LB, Cooke SB, Hartwig WC (2008) Morphology and evolution of the spider monkey, genus Ateles. In: Campbell C (ed) Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University, New YorkGoogle Scholar
  62. Rosenberger AL, Tejedor MF, Cooke SB, Pekkar S (2009) Platyrrhine ecophylogenetics, past and present. In: Garber P, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American primates: comparative perspectives in the study of behavior, ecology and conservation. Springer, New YorkGoogle Scholar
  63. Rosenberger AL, Halenar LB, Cooke SB (2011) The making of platyrrhine semi-folivores: models for the evolution of folivory in primates. Anat Rec 294:2112–2130CrossRefGoogle Scholar
  64. Ross C, Ravosa M (1993) Basicranial flexion, relative brain size, and facial kyphosis in nonhuman primates. Am J Phys Anthropol 91:305–324PubMedCrossRefGoogle Scholar
  65. Ruff CB (2003) Long bone articular and diaphyseal structure in Old World monkeys and apes II: estimation of body mass. Am J Phys Anthropol 120:16–37PubMedCrossRefGoogle Scholar
  66. Schrago CG (2007) On the time scale of the New World primate diversification. Am J Phys Anthropol 132:344–354PubMedCrossRefGoogle Scholar
  67. Schultz AH (1955) The position of the occipital condyles and of the face relative to the skull base in primates. Am J Phys Anthropol 13:97–120PubMedCrossRefGoogle Scholar
  68. Sears KE, Finarelli JA, Flynn JJ, Wyss AR (2008) Estimating body mass in New World “monkeys” (Platyrrhini, Primates) from craniodental measurements, with a consideration of the Miocene platyrrhine, Chilecebus carrascoensis. Am Mus Novitates 3617:1–29CrossRefGoogle Scholar
  69. Setoguchi T (1980) Discovery of a fossil primate from the Miocene of Colombia. Monkey 24:64–69Google Scholar
  70. Setoguchi T, Rosenberger AL (1985) Miocene marmosets: first evidence. Intl J Primatol 6:615–625CrossRefGoogle Scholar
  71. Setoguchi T, Watanabe T, Mouri T (1981) The upper dentition of Stirtonia (Ceboidea, Primates) from the Miocene of Colombia, South America and the origin of the postero-internal cusp of upper molars of howler monkeys (Alouatta). Kyoto University Overseas Research Reports of New World Monkeys 3:51–60Google Scholar
  72. Stephan H (1972) Evolution of primate brains: a comparative anatomical investigation. In: Tuttle RH (ed) The functional and evolutionary biology of primates. Aldine, ChicagoGoogle Scholar
  73. Stephan H, Andy OJ (1964) Quantitative comparison of brain structures from insectivores to primates. Am Zool 4:59–74PubMedGoogle Scholar
  74. Stirton RA (1951) Ceboid monkeys from the Miocene of Colombia. Univ Calif Pub Geol Sci 28:315–356Google Scholar
  75. Strier KB (1992) Ateline adaptations: behavioral strategies and ecological constraints. Am J Phys Anthropol 88:515–524PubMedCrossRefGoogle Scholar
  76. Swofford DL (2002) PAUP. Phylogenetic analysis using parsimony. Version 4.0b10 (Altivec). Sinauer, SunderlandGoogle Scholar
  77. Szalay FS, Bock WJ (1991) Evolutionary theory and systematics: relationships between process and patterns. J Zool Syst Evol Res 29:1–39CrossRefGoogle Scholar
  78. Szalay FS, Delson E (1979) Evolutionary history of the primates. Academic, New YorkGoogle Scholar
  79. Tejedor MF (2002) Primate canines from the early Miocene Pinturas Formation, southern Argentina. J Hum Evol 43:127–141PubMedCrossRefGoogle Scholar
  80. Tejedor MF, Tauber AA, Rosenberger AL, Swisher CC, Palacios ME (2006) New primate genus from the Miocene of Argentina. Proc Natl Acad Sci U S A 103:5437–5441PubMedCentralPubMedCrossRefGoogle Scholar
  81. Tejedor MF, Rosenberger AL, Cartelle C (2008) Nueva especie de Alouatta (Primates, atelineae) del Pleistoceno tardío de Bahía, Brasil. Ameghin 45:247–251Google Scholar
  82. Wiley DF, Amenta N, Alcantara DA, Ghosh D, Kil YK, Delson E, Harcourt-Smith W, Rohlf FJ, St. John K, Hamann B (2005) Evolutionary morphing (extended abstract and associated video presentation). Proceedings of IEEE visualization conference 2005, pp. 1–8Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Alfred L. Rosenberger
    • 1
    • 2
    • 3
    • 4
  • Siobhán B. Cooke
    • 5
  • Lauren B. Halenar
    • 3
    • 6
  • Marcelo F. Tejedor
    • 7
    Email author
  • Walter C. Hartwig
    • 8
  • Nelson M. Novo
    • 7
  • Yaneth Muñoz-Saba
    • 9
  1. 1.Department of Anthropology and ArchaeologyBrooklyn College, The City University of New YorkBrooklynUSA
  2. 2.The Graduate Center, The City University of New YorkNew YorkUSA
  3. 3.New York Consortium in Evolutionary Primatology (NYCEP), The City University of New YorkNew YorkUSA
  4. 4.Department of MammalogyThe American Museum of Natural HistoryNew YorkUSA
  5. 5.Department of AnthropologyNortheastern Illinois UniversityChicagoUSA
  6. 6.Department of Biological Sciences, Bronx Community CollegeThe City University of New YorkBronxUSA
  7. 7.Centro Nacional Patagónico-CONICETPuerto MadrynArgentina
  8. 8.Department of Basic SciencesTouro University College of Osteopathic MedicineVallejoUSA
  9. 9.Instituto de Ciencias Naturales, Universidad Nacional de ColombiaBogotáColombia

Personalised recommendations