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Intra and Interspecific Variation in Cranial Morphology on the Southernmost Distributed Cebus (Platyrrhini, Primates) Species

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Abstract

Capuchin monkeys (Cebus) are one of the genera with the widest distribution among Neotropical primates (New World Monkeys, Platyrrhini), accompanied by an elevated genetic, phenotypic, behavioral, morphological, and ecological diversity, both at the interspecific and population levels. Despite being one of the most studied primate genera, this high diversity has led to a particularly complex and controversial taxonomy. In this contribution, we explored the patterns of skull size and shape variation among the southernmost distributed populations of Cebus using three-dimensional geometric morphometric techniques. Results showed a marked morphological differentiation (in size and shape) between previously recognized species (C. nigritus and southern C. libidinosus), and also among C. libidinosus populations, which were quantitatively related with the geographic distance between them. This pattern supports a differentiation between the northwestern Argentina and southern Bolivia and Paraguay forms. Other taxonomic implications are also discussed.

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References

  • Adams DC, Rohlf FJ, Slice DE (2004) Geometric morphometrics: ten years of progress following the ‘revolution.’ Ital J Zool 71: 5–16

    Article  Google Scholar 

  • Ascunce MS, Hasson E, Mudry MD (2002) Description of the cytochrome c oxidase subunit II gene in some genera of New World monkeys (Primates, Platyrrhini). Genetica 114(3): 253–267

    Article  CAS  PubMed  Google Scholar 

  • Avila I (2004) Morphological variation between two subspecies of Cebus libidinosus (Primates: Cebidae). Bol Mus Nac Hist Nat Par 15(1–2): 1–8

    Google Scholar 

  • Bookstein FL (1991) Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Brown AD (1986) Biogeografia historica y la diversificación de los primates. Historia biogeogrífica del noroeste Argentino. Bol Primat Arg 4: 53–85

    Google Scholar 

  • Cabrera A (1939) Los monos de la Argentina. Physis 16: 3–39

    Google Scholar 

  • Cabrera A (1957) Catalogo de los mamíferos de América del Sur. Rev Mus Argentino Cienc Nat 1: 1–307

    Google Scholar 

  • Cardini A, Jansson AU, Elton S (2007) A geometric morphometric approach to the study of ecogeographical and clinal variation in vervet monkeys. J Biogeography 34: 1663–1678

    Article  Google Scholar 

  • Casado F, Bonvicino CR, Nagle C, Comas B, Manzur TD, Lahoz MM, Seuánez HN (2010) Mitochondrial divergence between 2 populations of the hooded capuchin, Cebus (Sapajus) cay (Platyrrhini, Primates). J Hered 101(3): 261–9

    Article  CAS  PubMed  Google Scholar 

  • Chiari Y, Wang B, Rushmeier H, Caccone A (2008) Using digital images to reconstruct three-dimensional biological forms: a new tool for morphological studies. Biol J Linn Soc 95(2): 425–436

    Article  Google Scholar 

  • Di Bitetti MS (2003) Outlook for primate conservation in misiones. In: The Atlantic Forest of South America: biodiversity status, threats, and outlook. Island Press, Washington, pp 194–199

  • Endler JA (1977) Geographic Variation, Speciation, and Clines. Princeton University Press, Princeton

    Google Scholar 

  • Froehlich JW, Supriatna J, Froehlich PH (1991) Morphometric analyses of Ateles: systematic and biogeographic implications. Am J Primatol 25: 1–22

    Article  Google Scholar 

  • Groves CP (2001) Primate Taxonomy. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • 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

  • Hill WCO (1960) Primates: Comparative Anatomy and Taxonomy. IV Cebidae, Part A. Edinburgh University Press, Edinburgh

    Google Scholar 

  • IUCN (International Union for Conservation of Nature) (2012) IUCN Red List of Threatened Species. Versión 2011.2. Available at: http://www.iucnredlist.org

  • Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resourc 11: 353–357

    Article  Google Scholar 

  • Ludwig G, Aguiar LM, Rocha VJ (2005) Uma Avaliação da Dieta, da Área de Vida e das Estimativas Populacionais de Cebus nigritus (Goldfuss, 1809) em um Fragmento Florestal no Norte do Estado do Paraná. Neotrop primates 13 (3): 12–18

    Article  Google Scholar 

  • Lynch Alfaro JW, Boubli JP, Olson LE, Di Fiore A, Wilson B, Gutierrez-Espeleta GA, Chiou KL, Schulte M, Neitzel S, Ross V, Schwochow D, Nguyen MTT, Farias I, Janson CH, Alfaro ME (2012a) Explosive Pleistocene range expansion leads to widespread Amazonian sympatry between robust and gracile capuchin monkeys. J Biogeography 39:272–288

    Article  Google Scholar 

  • Lynch Alfaro JW, Silva J e S Jr, Rylands AB (2012b) How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. Am J Primatol 74:273–286

    Article  Google Scholar 

  • Mantecón M, Mudry de Pargament MD, Brown A (1984) Cebus apella de Argentina. Rev Mus Argentino Cienc Nat 13(41):399–408

    Google Scholar 

  • Marroig G (2007) When size makes a difference: allometry, life-history and morphological evolution of capuchins (Cebus) and squirrels (Saimiri) monkeys (Cebinae, Platyrrhini). BMC Evol Biol 7: 20

    Article  PubMed Central  PubMed  Google Scholar 

  • Marroig G, Cheverud JM (2001) A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of New World monkeys. Evolution 55(12): 2576–2600

    Google Scholar 

  • Marroig G, Cheverud JM (2005) Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World monkeys. Evolution 59(5): 1128–42

    Article  PubMed  Google Scholar 

  • Martinez R, Torres E, Nieves M, Szapkievich V, Rodrıguez S, Schinini A, Escurra M, Mudry MD (2004) Genetic variability in two captive colonies of Cebus apella paraguayanus (Primates: Platyrrhini) from eastern Paraguay. Caryologia 57–4: 332–336

    Article  Google Scholar 

  • Martinez RA, Giudice A, Szapkievich VB, Ascunce M, Nieves M, Zunino G, Mudry MD (2002) Parameters modeling speciogenic processes in Cebus apella (Primates: Platyrrhini) from Argentina. Mast Neotrop/J Neotrop Mammal 9(2):171–186.

    Google Scholar 

  • Masterson TJ (2001) Geographic cranial variation among three subspecies of Cebus apella. Am J Primatol 52:46–47

    Google Scholar 

  • Mittermeier RA, Rylands AB, Wilson DE, Martinez-Vilalta A (2013) Handbook of the Mammals of the World: Primates. Lynx Edicions, Barcelona

    Google Scholar 

  • Mudry MD (1990) Cytogenetic variability within and across populations of Cebus apella in Argentina. Folia Primatol 54:206–216

    Article  CAS  PubMed  Google Scholar 

  • Nieves M (2007) Heterocromatina y Evolución Cromosómica en Primates Neotropicales. Doctoral thesis, Universidad de Buenos Aires, Buenos Aires

  • Niewoehner WA (2001) Behavioral inferences from the Skhul/Qafzeh early modern human hand remains. Proc Natl Acad Sci USA 98(6): 2979–2984

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ponsà M, García M, Borell A, Garcia F, Egozcue J, Gorostiaga MA, Delprat A, Mudry MD (1995) Heterochromatin and cytogenetic polymorphisms in Cebus apella (Cebidae, Platyrrhini). Am J Primatol 37: 325–331

    Google Scholar 

  • Rohlf FJ, Marcus LF (1993) A revolution morphometrics. Trends Ecol Evol 8(4): 129–132

    Article  Google Scholar 

  • Rohlf FJ, Slice D (1990) Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59

    Article  Google Scholar 

  • Rosenberger AL (2012) New World monkey nightmares: science, art, use, and abuse (?) in platyrrhine taxonomic nomenclature. Am J Primatol 74(8): 692–695

    Google Scholar 

  • Rylands AB, Mittermeier RA (2009) The diversity of the New World primates: an annotated taxonomy. In: Garber PA, 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 York, pp 23–54

  • Rylands AB, Mittermeier RA, Silva J e S Jr (2012) Neotropical primates: taxonomy and recently described species and subspecies. Internatl Zoo Yb 46:11–24

  • Silva J e S Jr (2001) Especiação nos macacos-prego e caiararas, gênero Cebus Erxleben, 1777 (Primates, Cebidae). Doctoral thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro

  • Sundberg P (1989) Shape and size-constrained principal components analysis. Syst Zool 38:166–168

    Article  Google Scholar 

  • Torres C (1983) An ecological study of the primates of southeastern Brazil, with a reappraisal of Cebus apella races. Ph.D. thesis, University of Edinburgh, Edinburgh

  • Vieira C da C (1955) Lista remissiva dos mamíferos do Brasil. Arquivos de Zoologia São Paulo 8: 341–347

  • Wilson DE, Reeder DM (eds) (2005) Mammal Species of the World. A Taxonomic and Geographic Reference (3rd ed). Johns Hopkins University Press, Baltimore, 2,142 pp

    Google Scholar 

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Acknowledgments

We thank Dr. David Flores (Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”) and Dr. Diego Verzi (Museo de La Plata) for granting us access to the collections under their care. We also thank two anonymous reviewers whose comments helped improve this work. This research was supported by grants from CONICET (MDM PIP 112) and UBACyT (X154).

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Correspondence to Leandro Arístide.

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Arístide, L., Soto, I.M., Mudry, M.D. et al. Intra and Interspecific Variation in Cranial Morphology on the Southernmost Distributed Cebus (Platyrrhini, Primates) Species. J Mammal Evol 21, 349–355 (2014). https://doi.org/10.1007/s10914-013-9249-y

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