International Journal of Primatology

, Volume 19, Issue 5, pp 879–905 | Cite as

Scientific Nomenclature of the Red Howlers from the Northeastern Amazon in Brazil, Venezuela, and the Guianas

  • Anthony B. Rylands
  • Douglas Brandon-Jones
Article

Abstract

Cytogenetic and morphological studies have begun to reexamine the taxonomy of the red howlers Alouatta seniculus which live throughout the northern and western Amazon basin, in the Guianas, and from northern Colombia and Venezuela, south to Bolivia. We briefly review the current state of knowledge of the taxonomy and distributions of red howlers, in particular, that of the Guianan subspecies. Recently, two names have been applied to populations from this region, Simia straminea Humboldt, 1812, and Alouatta macconnelli Elliot, 1910. Allen (1911, 1916) unquestioningly accepted the validity of A. macconnelli from the Guyana coast, but most subsequent taxonomic revisions (Cruz Lima, 1945; Cabrera, 1957; Husson, 1978) have synonymized it with S. straminea. Tate (1939) and Hill (1962) listed Alouatta seniculus macconnelli, but both doubted its validity. Nevertheless, recent cytogenetic and morphological studies, without due consideration of the taxonomic history of the two scientific names, have led to the resurrection of A. macconnelli, as distinct from S. straminea. The use of the name Alouatta macconnelli has evidently arisen from a cursory reading of Hill (1962) or an uncritical interpretation of his provisional subspecific distribution map or both. There are also contradictory interpretations of a reciprocal translocation as indicating that Simia straminea and Alouatta macconnelli are separate species (Bonvicino et al., 1995) or the same subspecies (Sampaio et al., 1996). Doubts about the type locality of Simia straminea Humboldt, 1812, as given by Hill (1962), led us to research its original description and to conclude that Simia straminea is a synonym of Alouatta caraya and therefore unavailable for Alouatta seniculus. Before A. macconnelli is accepted as the next available name for the Guianan red howlers, however, we advocate a thorough review of Guianan, Venezuelan, and Colombian red howler subspeciation, with due consideration for the taxonomic status of Mycetes auratus and Mycetes laniger Gray, 1845. We note that Alouatta guariba (Humboldt, 1812) is a senior synonym of Alouatta fusca (Saint-Hilaire, 1812).

Alouatta seniculus taxonomy geographic distribution Guianas 

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REFERENCES

  1. Allen, J. A. (1904). Report on mammals from the district of Santa Marta, Colombia, collected by Mr. Herbert H. Smith, with field notes by Mr. Smith. Bull. Am. Mus. Nat. Hist. 20: 407–468.Google Scholar
  2. Allen, J. A. (1911). Mammals of Venezuela collected by Mr. M. A. Carriker, Jr., 1909–1911. Bull. Am Mus. Nat. Hist. 30: 239–273.Google Scholar
  3. Allen, J. A. (1914). New South American monkeys. Bull. Am. Mus. Nat. Hist. 33: 647–655.Google Scholar
  4. Allen, J. A. (1916). List of mammals collected in Colombia by the American Museum of Natural History Expeditions, 1910–1915. Bull. Am. Mus. Nat. Hist. 35: 191–238.Google Scholar
  5. Armada, J. L. A., Barroso, C. M. L., Lima, M. M. C., Muniz, J. A. P. C., and Seuánez, H. N. (1987). Chromosome studies in Alouatta belzebul. Am. J. Primatol. 13: 283–296.Google Scholar
  6. Bender, M. A., and Chu, E. H. Y. (1963). The chromosomes of primates. In Büttner-Janusch, J. (ed.), Evolutionary Biology and Genetic Biology of the Primates, Academic Press, New York, pp. 261–310.Google Scholar
  7. Bodini, R., and Pérez-Hernández, R. (1987). Distribution of the species and subspecies of cebids in Venezuela. Fieldiana Zool. New Ser. 39: 231–244.Google Scholar
  8. Bonvicino, C. R., Langguth, A., and Mittermeier, R. A. (1989). A study of the pelage color and geographic distribution in Alouatta belzebul (Primates, Cebidae). Rev. Nordestina Biol. 6(2): 139–148.Google Scholar
  9. Bonvicino, C. R., Fernandes, M. E. B., and Seuánez, H. N. (1995). Morphological analysis of Alouatta seniculus species group (Primates, Cebidae). A comparison with biochemical and karyological data. Hum. Evol. 10(2): 169–176.Google Scholar
  10. Cabrera, A. (1940). Los nombres cientificos de algunos monos Americanos. Ciencia Méx. 1: 402–405.Google Scholar
  11. Cabrera, A. (1957). Catálogo de los mamiferos de América del Sur. Rev. Argentino Cienc. Nat. ‘Bernardino Rivadavia’ 4(1): 1–307.Google Scholar
  12. Carvalho, C. T. de (1960). Sobre alguns mamlferos do sudeste do Pará. Arq. Zool. S. Paulo 11: 121–132.Google Scholar
  13. Carvalho, C. T. de (1965). Comentarios sôbre os mamiferos descritos e figurados por Alexandre Rodrigues Ferreira em 1790. Arq. Zool. S. Paulo 12: 7–70.Google Scholar
  14. Chu, E. H. Y., and Bender, M. A. (1961). Chromosome cytology and evolution in primates. Science 133: 1399–1405.PubMedGoogle Scholar
  15. Consigliere, S., Stanyon, R., Köhler, U., Agoramoorthy, G., and Wienberg, J. (1996). Chromosome painting defines genomic rearrangements between red howler monkey subspecies. Chromosome Res. 4: 264–270.PubMedGoogle Scholar
  16. Cruz Lima, E. da (1945). Mammals of Amazonia. General Introduction and Primates, Vol. 1. Contr. Museu Paraense Emílio Goeldi de Historia Natural e Etnografia, Belém, English ed.Google Scholar
  17. Elliot, D. G. (1910). Descriptions of new species of monkeys of the genera Galago, Alouatta, and Cercopithecus. Ann. Mag. Nat. Hist. 18(5): 77–83.Google Scholar
  18. Elliot, D. G. (1913). A review of primates. Monograph Series, Am. Mus. Nat. Hist., New York.Google Scholar
  19. Ferreira, A. R. (1972). Viagem Filosófica pelas Capitanias do Grāo Pará, Rio Negro, Mato Grosso e Cuiabá. Memórias. Zoologia Botânica (compiled by J. C. de M. Carvalho). Conselho Federal de Cultura, Rio de Janeiro.Google Scholar
  20. Figueiredo, W. B., Pinheiro, M., Oliveira, F. H. C., Langguth, A., Gregorin, R., Schneider, H., and Sampaio, I. (1997). Filogenia molecular e evoluçäo do gênero Alouatta. In Programa e Resumos. VIII Congresso Brasileiro de Primatoiogia e V Reuniäo Latino-Américano de Pnimatologia, Sociedade Brasileira de Primatologia, Joäo Pessoa, 10–15 Aug., p. 97.Google Scholar
  21. Figueiredo, W. B., Carvalho-Filho, N. M., Schneider, H., and Sampaio, I. (1998). Mitochondrial DNA sequences and the taxonomic status of Alouatta seniculus populations in northeastern Amazonia. Neotrop. Primates 6(3): 73–77.Google Scholar
  22. Fontes, G. M. D. N. de C. (1966). Alexandre Rodrigues Ferreira. Aspectos de sua vida e sua obra. Cadernos da Amazonia 10, Instituto Nacional de Pesquisas da Amazônia, Manaus.Google Scholar
  23. Goeldi, E. A. (1895). Ensaio sobre o Dr. Alexandre Rodnigues Ferreira mormente em Relaçäo às suas viagens na Amazônia e sua importância como naturalista, Editora Alfredo Silva & Cia, Pará.Google Scholar
  24. Gray, J. E. (1845). On the howling monkeys (Mycetes, Illiger). Ann. Mag. Nat. Hist. 16: 217–221.Google Scholar
  25. Groves, C. P. (1993). Order Primates. In Wilson, D. E., and Reeder, D. M. (eds.), Mammal Species of the World: A Taxonomic and Geographic Reference, 2nd ed., Smithsonian Institution Press, Washington, DC, pp. 243–277.Google Scholar
  26. Gumilla, P. J. (1758). Histoire naturelle, civile et géographique de l'Orénoqué, et des principales rivières qui s'y jettent, Traduite de l'Espagnol sur la seconde édition, par M. Eidous, Avignon.Google Scholar
  27. Hernández-Camacho, J., and Cooper, R. W. (1976). The non-human primates of Colombia. In Thorington, R. W., Jr., and Heltne, P. G. (eds.), Neotropical Primates: Field Studies and Conservation, National Academy of Sciences, Washington, DC, pp. 35–69.Google Scholar
  28. Hershkovitz, P. (1949). Mammals of northern Colombia. Preliminary report No. 4: Monkeys (Primates), with taxonomic revisions of some forms. Proc. U. S. Natl. Mus. 98: 323–427.Google Scholar
  29. Hershkovitz, P. (1963). Primates. Comparative anatomy and taxonomy, [volume] V, Cebidae, part B, A monograph, by W. C. Osman Hill. Edinburgh University Press. 1962, xxix +537 pp., 31 pls., 94 figs., 3 maps. $32.00. A critical review with a summary of the volumes on New World primates. Am. J. Phys. Anthropol. (N.S.)21: 391–398.Google Scholar
  30. Hershkovitz, P. (1977). Living New World Monkeys (Platyrrhini) with an Introduction to Primates, Vol. 1, University Press of Chicago, Chicago.Google Scholar
  31. Hill, W. C. O. (1960). Primates. Comparative Anatomy and Taxonomy IV. Cebidae, Part A, Edinburgh University Press, Edinburgh.Google Scholar
  32. Hill, W. C. O. (1962). Primates. Comparative Anatomy and Taxonomy V. Cebidae, Part B, Edinburgh University Press, Edinburgh.Google Scholar
  33. Hirsch, A., Landau, E. C., Tedeschi, A. C. de M., and Menegheti. J. O. (1991). Estudo comparativo das espécies do gênero Alouatta Lacépède, 1799 (Platyrrhini, Atelidae) e sua distribuiçäo geográfica na America do Sul. In Rylands, A. B., and Bernardes, A. T. (eds.), A Primatologia no Brasil—3, Fundaçäo Biodiversitas and Sociedade Brasileira de Primatologia, Belo Horizonte, pp. 239–262.Google Scholar
  34. Humboldt, [F. H.] A. (1805a). Mémoire sur l'os hyoïde et le larynx des oiseaux, des singes et du crocodile. In Humboldt, [F. H.] A., and Bonpland, A. [J. A.], Recueil d'observations de zoologie et d'anatomie comparée, faites dans l'océan Atlantique, dans l'intérieur du nouveau continent et dans la mer du sud pendant les années 1799[–]1803, Premier volume Deuxième partie, Observations de zoologie et d'anatomie comparée, Schoell and Dufour, Paris, pp. 1–13. [For date of publication, see Sherborn (1899).]Google Scholar
  35. Humboldt, [F. H.] A. (1805b). Mémoire sur une nouvelle espèce de singe, trouvée sur la pente orientale des Andes. In, Humboldt, [F. H.] A., and Bonpland, A. [J. A.], Recueil d'observations de zoologie et d'anatomie comparée, faites dans l'océan Atlantique, dans l'intérieur du nouveau continent et dans la mer du sud pendant les années 1799[–]1803, Premier volume, Deuxième partie, Observations de zoologie et d'anatornie comparée, Schoell and Dufous, Paris, pp. 14–16. [For date of publication, see Sherborn (1899).]Google Scholar
  36. Humboldt, [F. H.] A. (1812a). Sur les singes qui habitent les rives de l'Orénoque, du Cassiquiare et du Rio Negro. In Humboldt, [F. H.] A., and Bonpland, A. [J. A], Recueil d'observations de zoologie et d'anatomie comparée, faites dans l'océan Atlantique, dans l'intérieur du nouveau continent et dans la mer du sud pendant les années 1799[–]1803, Premier volume, Deuxième partie, Observations de zoologie et d'anatomie comparée, Schoell and Dufous, Paris, pp. 305–335. [For date of publication, see Sherborn (1899).]Google Scholar
  37. Humboldt, [F. H.] A. (1812b). Tableau synoptique des singes de l'Amérique. In: Humboldt, [F. H.] A., and Bonpland, A. [J. A.], Recueil d'observations de zoologie et d'anatomie comparée, faites dans l'océan Atlantique, dans l'intérieur du nouveau continent et dans la mer du sud pendant les années 1799[–]1803, Premier volume, Deuxième partie, Observations de zoologie et d'anatomie comparee, Schoell and Dufour, Paris, pp. 353–363. [For date of publication, see Sherborn (1899).]Google Scholar
  38. Husson, A. M. (1957). Notes on the primates of Suriname. Stud. Fauna Suriname Other Guianas 1: 13–40.Google Scholar
  39. Husson, A. M. (1978). The Mammals of Suriname. Zoologische Monographieën van het Rijksmuseum van Natuurlijke Historie (2), E. J. Brill, Leiden.Google Scholar
  40. Lima, M. M. C., and Seuánez, H. N. (1989). Cytogenetic characterization of Alouatta belzebul with atypical pelage coloration. Folia Primatol. 52: 97–101.PubMedGoogle Scholar
  41. Lima, M. M. C., and Seuánez, H. N. (1991). Chromosome studies in the red howler monkey, Alouatta seniculus straminea (Platyrrhini, Primates): description of an X1X2Y1Y2/X1X1X2X2 sex-chromosome system and karyological comparison with other subspecies. Cytogenet. Cell Genet. 57: 151–156.PubMedGoogle Scholar
  42. Lima, M. M. C., Sampaio, M. I. C., Schneider, M. P. C., Scheffrahn, W., Schneider, H., and Salzano, F. M. (1990). Chromosome and protein variation in red howler monkeys. Brazil. J. Genet. 13(4): 789–802.Google Scholar
  43. Lönnberg, E. (1941). Notes on the members of the genera Alouatta and Aotus. Ark. Zool. 33A(10): 1–44.Google Scholar
  44. Minezawa, M., Harada, M., Jordan, O. C., and Valdivia Borda, C. J. (1986). Cytogenetics of the Bolivian endemic red howler monkeys (Alouatta seniculus sara): Accessory chromosomes and Y-autosome translocation related numerical variations. Kyoto Univ. Overseas Res. Rep. New World Monkeys 5: 7–16.Google Scholar
  45. Napier, P. H. (1976). Catalogue of the Primates in the Bntish Museum (Natural History). Part 1: Families Callitrichidae and Cebidae, British Museum (Natural History), London.Google Scholar
  46. Oliveira, E. H. C. (1996). Estudos Citogenéticos e Evolutivos nas Espécies Brasileiras e Argentinas do Gênero Alouatta Lacépède, 1799 (Primates, Atelidae). Unpublished master's thesis, Universidade Federal do Parána, Curitiba.Google Scholar
  47. Rode, P. (1938). Catalogue des types des mammifères du Muséum National d'Histoire Naturelle: Ordre des Primates, sous-ordre des simiens. Bull. Mus. Natl. Hist. Nat. Paris (2)10: 202–251.Google Scholar
  48. Saint-Hilaire [É.], G. (1806). Mémoire sur les singes à main imparfaite ou les atéles. Ann. Mus. Hist. Nat. Paris 7: 260–273.Google Scholar
  49. Saint-Hilaire, [É.], G. (1812). Tableau des quadrumanes, ou des animaux composant le premier ordre de la classe des mammifères. Ann. Mus. Hist. Nat. Paris 19: 85–122.Google Scholar
  50. Saint-Hilaire, I. G. (1851). Catalogue méthodique de la collection des mammifères, de la collection des oiseaux et des collection annexes du Muséum d'Histoire Naturelle de Paris. Première partie. Mammifères. Catalogue des primates, Gide et Baudry, Paris.Google Scholar
  51. Sampaio, M. I. da C., Schneider, M. P. C., Barroso, C. M. L., Silva, B. T. F., Schneider, H., Encarnación, F., Montoya, E., and Salzano, F. M. (1991). Carbonic anhydrase II in New World monkeys. Int. J. Primatol. 12: 389–402.Google Scholar
  52. Sampaio, M. I. da C., Schneider, M. P. C., and Schneider, H. (1996). Taxonomy of the Alouatta seniculus group: Biochemical and chromosome data. Primates 37(1): 67–73.Google Scholar
  53. Sanderson, I. T. (1949). A brief review of the mammals of Suriname (Dutch Guiana), based upon a collection made in 1938. Proc. Zool. Soc. Lond. 119: 755–789.Google Scholar
  54. Sharpe, R.B. (1906). Birds. In The History of the Collections Contained in the Natural History Departments of the British Museum, Vol. 2. Separate Historical Accounts of the Several Collections Included in the Department of Zoology, Trustees of the British Museum, London, pp. 79–515.Google Scholar
  55. Sherborn, C. D. (1899). A note on the date and parts of “Humboldt and Bonpland's Voyage: Observations de Zoologie.” Ann. Mag. Nat. Hist. (7)3: 428.Google Scholar
  56. Spix, J. B. de (1823). Simiarum et vespertilionum brasiliensium species novae, Hübschmann, Monaco.Google Scholar
  57. Stanyon, R., Tofanelli, S., Morescalchi, M. A., Agoramoorthy, G., Ryder, O. A., and Wienberg, J. (1995). Cytogenetic analysis shows extensive genomic rearrangements between red howler (Alouatta seniculus Linnaeus) subspecies. Am. J. Primatol. 35: 171–183.Google Scholar
  58. Tate, G. H. H. (1939). The mammals of the Guiana region. Bull. Am. Mus. Nat. Hist. 76: 151–229.Google Scholar
  59. Thomas, O. (1913). New mammals from South America. Ann. Mag. Nat. Hist. (8)12: 567–574.Google Scholar
  60. Vassart, M., Guédant, A., Vié, J. C., Kéravec, J., Séguéla, A., and Volobouev, V. T. (1996). Chromosomes of Alouatta seniculus (Platyrrhini, Primates) from French Guiana. J. Hered. 87: 331–334.PubMedGoogle Scholar
  61. Vieira, C. da C. (1955). Lista remissiva dos mamíferos do Brasil. Arq. Zool. Säo Paulo 8: 341–474.Google Scholar
  62. von Ihering, H. (1914). Os bugios do genero Alouatta. Rev. Mus Paulista 9: 231–256.Google Scholar
  63. Watanabe, T. (1982). Mandible/basihyal relationships in red howler monkeys (Alouatta seniculus): A craniometrical approach. Primates 23: 105–129.Google Scholar
  64. Wolfheim, J. H. (1983). Primates of the World: Distribution, Abundance and Conservation, University of Washington Press, Seattle.Google Scholar
  65. Yunis, E. J., Torres de Caballero, O. M., Ramirez, C., and Ramirez, E. (1976). Chromosomal variation in the primate Alouatta seniculus seniculus. Folia Primatol. 25: 215–224.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1998

Authors and Affiliations

  • Anthony B. Rylands
    • 1
    • 2
  • Douglas Brandon-Jones
    • 3
  1. 1.Departamento de Zoologia, Instituto de Ciências BiológicasUniversidade Federal de Minas GeraisBelo Horizonte
  2. 2.Conservation International do BrasilBelo Horizonte, Minas GeraisBrazil
  3. 3.LondonUnited Kingdom

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