Primates

, Volume 56, Issue 2, pp 131–144 | Cite as

Re-description and assessment of the taxonomic status of Saguinus fuscicollis cruzlimai Hershkovitz, 1966 (Primates, Callitrichinae)

  • Ricardo Sampaio
  • Fábio Röhe
  • Gabriela Pinho
  • José de Sousa e Silva-Júnior
  • Izeni Pires Farias
  • Anthony B. Rylands
Review Article
First Online:
Received:
Accepted:

Abstract

Cruz Lima’s saddle-back tamarin Saguinus fuscicollis cruzlimai Hershkovitz, 1966, was described from a painting by Eládio da Cruz Lima in his book Mammals of Amazonia, Vol. 1, Primates (1945). The painting was of four saddle-back tamarins from the upper Rio Purus, one of them distinct and the inspiration for Hershkovitz to describe it as a new subspecies. Its exact provenance was unknown, however, and the specimen was lost. Surveys in the Purus National Forest in 2011 resulted in sightings of this tamarin along the north bank of the Rio Inauini, a left-bank tributary of the middle Purus, and also on the left bank of the Purus, north and south of the Rio Inauini. It is possible that it extends north as far as the Rio Pauini, and that S. f. primitivus Hershkovitz, 1977, occurs north of the Pauini as far the Rio Tapauá, both also left-bank tributaries of the Purus. Morphometric and molecular genetic analyses and the coloration of the pelage indicate that this tamarin differs from its neighbors sufficiently to be considered a full species. In his doctoral dissertation [2010, Taxonomy, Phylogeny and Distribution of Tamarins (Genus Saguinus Hoffmannsegg, 1807) Georg-August Universität, Göttingen], C. Matauschek found that saddle-back and black-mantle tamarins diverged from the tamarin lineage around 9.2 million years ago; time enough to warrant their classification in a distinct genus. Leontocebus Wagner, 1840, is the first name available. In this article we re-describe Cruz Lima’s saddle-back tamarin. We propose a neotype with a precise locality, and make it a full species in the genus Leontocebus.

Keywords

Callitrichidae Saddle-back tamarin Saguinus Leontocebus Distribution Western Amazon 
This is a preview of subscription content, log in to check access

Notes

Acknowledgments

The primate surveys were part of two field research projects: “Primates in Amazonian Protected Areas” and “Diversity and Hunting of Mammals in the Region of Boca do Acre/AM,” both financed and authorized (SISBIO #33582; #38186) by the Brazilian Government’s Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). The genetic analyses (IPF) were carried out within the SISBIOTA project of the Brazilian Science Council (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/AUXPE 3261/2013) and the Amazonas State Research Foundation (Fundação de Amparo à Pesquisa do Estado do Amazonas—FAPEAM). We are grateful to the Coordenação Geral de Pesquisa e Monitoramento da Biodiversidade (CGPEQ/DIBIO/ICMBio), the Centro Nacional de Pesquisa e Conservação de Primatas Brasileiros (CPB/ICMBio), and the Centro Nacional de Pesquisa e Conservação da Biodiversidade Amazônica (CEPAM/ICMBio). We sincerely thank also the ICMBio staff in Boca do Acre/AM for their support at all stages of the project; the Municipal Prefecture of Boca do Acre; and the invaluable help of Francisco Alves da Silva during the field work. We are indebted to the countless families that live along the Rio Inauini and those in the communities of the Arapixi Extractivist Reserve especially the family of Sr. Noel Humberto Dias Gomes and Solange Gonçalves, for help of all kinds during our field expeditions. Maria N. F. da Silva, Manoela Borges and Iracema Andrade, curators of the mammal collection at the Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, were so helpful and kind; Adriano C. S. Antunes (INPA) prepared the neotype, and Raimundo Rodrigues da Silva of the Emílio Goeldi Museum (MPEG) prepared the other specimens. The curators at MPEG were most helpful in allowing us to examine the specimens in their collection. We thank Victor Fonsêca da Silva and Michelle Pinto Mercês who helped in the morphometry of L. cruzlimai and L. w. melanoleucus. We thank Stephen D. Nash for his kindness and celerity in providing us with an illustration of Leontocebus cruzlimai and the digital images Figs. 1 and 2. Finally, we are most grateful to Sr. Eládio Malcher Lima and Sra. Ângela Pinheiro, Eládio da Cruz Lima’s son and granddaughter, for kindly allowing us to reproduce the Cruz Lima (1945) plate 38 (Fig. 1), and likewise to Maria Astrogilda Ribeiro Silva, Coordenadora CID, MCTI/MPEG/CID for the unpublished illustration of Goeldi (1907) (Fig. 2). We thank the reviewers Dr. Jessica Lynch Alfaro and Dr. Horácio Schneider for their excellent comments and suggestions.

References

  1. Brazil MMA (2014) Portaria No. 444, 445, de 17 de dezembro de 2014. Diário Oficial da União—Seção 1 (245):110–130. Ministério do Meio Ambiente (MMA), Brasilia. http://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?data=18/12/2014&jornal=1&pagina=110&totalArquivos=144
  2. Buckland ST, Anderson DR, Burnham KP, Laake JL (1993) Distance sampling: estimating abundance of biological populations. Chapman and Hall, LondonCrossRefGoogle Scholar
  3. Buckner JC, Lynch Alfaro J, Rylands AB, Alfaro ME (2015) Biogeography of the marmosets and tamarins (Callitrichidae). Mol Phylogenet Evol 82:413–425CrossRefPubMedGoogle Scholar
  4. Canavez FC, Moreira MAM, Simon F, Parham P, Seuánez HN (1999) Phylogenetic relationships of the Callitrichinae (Platyrrhini, Primates) based on ß2-microglobulin DNA sequences. Am J Primatol 48:225–236CrossRefPubMedGoogle Scholar
  5. Cheverud JM, Moore AJ (1990) Subspecific variation in the saddle-back tamarin (Saguinus fuscicollis). Am J Primatol 21:1–15CrossRefGoogle Scholar
  6. Cropp SJ, Larson A, Cheverud JM (1999) Historical biogeography of tamarins, genus Saguinus: the molecular phylogenetic evidence. Am J Phys Anthropol 108:65–89CrossRefPubMedGoogle Scholar
  7. Cruz Lima E da (1945) Mammals of Amazonia. Volume 1. General introduction and primates. Museu Paraense Emílio Goeldi de História Natural e Etnografia, Rio de JaneiroGoogle Scholar
  8. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefPubMedCentralPubMedGoogle Scholar
  9. Goeldi EA (1907) On some new and insufficiently known species of marmoset monkeys from the Amazonian region. Proc Zool Soc Lond 77(1):88–99Google Scholar
  10. Goodman M, Porter CA, Czelusniak J, Page SL, Schneider H, Shoshani J, Gunnell G, Groves CP (1998) Toward a phylogenetic classification of primates based on DNA evidence complemented by fossil evidence. Mol Phylogenet Evol 9:585–598CrossRefPubMedGoogle Scholar
  11. Groves CP (2001) Primate taxonomy. Smithsonian Institution Press, WashingtonGoogle Scholar
  12. Groves CP (2005) Order primates. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, 3rd edn. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  13. Hershkovitz P (1949) Mammals of northern Colombia. Preliminary report No. 4: Monkeys (Primates), with taxonomic revisions of some forms. Proc US Nat Mus 98:323–427CrossRefGoogle Scholar
  14. Hershkovitz P (1957) The systematic position of the marmoset, Simia leonina Humboldt (Primates). Proc Biol Soc Wash 70:17–20Google Scholar
  15. Hershkovitz P (1966) Taxonomic notes on tamarins, genus Saguinus (Callithricidae, Primates), with descriptions of four new forms. Folia Primatol 4:381–395CrossRefPubMedGoogle Scholar
  16. Hershkovitz P (1968) Metachromism or the principle of evolutionary change in mammalian tegumentary colors. Evolution 22:556–575CrossRefGoogle Scholar
  17. Hershkovitz P (1977) Living New World monkeys, with an introduction to primates, vol 1. Chicago University Press, ChicagoGoogle Scholar
  18. Hershkovitz P (1982) Subspecies and geographic distribution of black-mantle tamarins Saguinus nigricollis Spix (Primates: Callitrichidae). Proc Biol Soc Wash 95:647–656Google Scholar
  19. Heymann EW, Buchanan-Smith HM (2000) The behavioural ecology of mixed-species troops of callitrichine primates. Biol Rev 75:169–190CrossRefPubMedGoogle Scholar
  20. Matauschek C (2010) Taxonomy, phylogeny and distribution of tamarins (genus Saguinus Hoffmannsegg, 1807). Doctoral dissertation, Georg-August Universität, GöttingenGoogle Scholar
  21. Matauschek C, Roos C, Heymann EW (2011) Mitochondrial phylogeny of tamarins (Saguinus Hoffmannsegg, 1807) with taxonomic and biogeographic implications for the S. nigricollis species group. Am J Phys Anthropol 144:564–574CrossRefPubMedGoogle Scholar
  22. Peres CA (1999) General guidelines for standardizing line-transect surveys of Tropical Forest Primates. Neotrop Primates 7:11–16Google Scholar
  23. Peres CA, Patton JL, da Silva MNF (1996) Riverine barriers and gene flow in Amazonian saddle-back tamarins. Folia Primatol 67:113–124PubMedGoogle Scholar
  24. Röhe F, Silva-Júnior JS, Sampaio R, Rylands AB (2009) A new subspecies of Saguinus fuscicollis (Primates, Callitrichidae). Int J Primatol 30:533–551CrossRefGoogle Scholar
  25. Rylands AB, Mittermeier RA (2008a) Saguinus fuscicollis ssp. cruzlimai. In: IUCN 2013. IUCN red list of threatened species. Version 2013.2. URL:<http://www.iucnredlist.org>. Downloaded on 10 May 2014
  26. Rylands AB, Mittermeier RA (2008b) 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 23–54Google Scholar
  27. Rylands AB, Mittermeier RA (2013) Family Callitrichidae (marmosets and tamarins). In: Mittermeier RA, Rylands AB, Wilson DE (eds) Handbook of the mammals of the world, vol 3., PrimatesLynx Edicions, Barcelona, pp 262–346Google Scholar
  28. Rylands AB, Schneider H, Langguth A, Mittermeier RA, Groves CP, Rodríguez-Luna E (2000) An assessment of the diversity of New World primates. Neotrop Primates 8:61–93Google Scholar
  29. Rylands AB, Matauschek C, Aquino R, Encarnación F, Heymann EW, de la Torre S, Mittermeier RA (2011) The range of the golden-mantle tamarin, Saguinus tripartitus (Milne Edwards, 1878): distributions and sympatry of four tamarins in Colombia, Ecuador, and northern Peru. Primates 52:25–39CrossRefPubMedCentralPubMedGoogle Scholar
  30. Rylands AB, Mittermeier RA, Silva-Júnior JS (2012) Neotropical primates: taxonomy and recently described species and subspecies. Int Zoo Yearb 46:11–24CrossRefGoogle Scholar
  31. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, vol. I, 2nd edn. Cold Spring Harbor Laboratory PressGoogle Scholar
  32. Tagliaro CH, Schneider H, Sampaio I, Schneider MPC, Vallinoto M, Stanhope M (2005) Molecular phylogeny of the genus Saguinus (Platyrrhini, Primates) based on the ND1 mitochondrial gene and implications for conservation. Genet Mol Biol 28:46–53CrossRefGoogle Scholar
  33. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680CrossRefPubMedCentralPubMedGoogle Scholar
  34. Thorington RW Jr (1988) Taxonomic status of Saguinus tripartitus (Milne-Edwards, 1878). Am J Primatol 15:367–371CrossRefGoogle Scholar
  35. Van Roosmalen T, van Roosmalen, MGM (2003) Note on Saguinus (fuscicollis) cruzlimai (Callitrichinae)—Cruz Lima’s saddleback tamarin. Website: New species from Amazonia. URL: < http.www.amazonnewspecies.com>. Dated 16 August 2003. Accessed 26 September 2003
  36. Van Roosmalen MGM, Nash SD, Gozzaglio P (undated) Distributions and phylogeography of Neotropical primates: a pictorial guide to all known New-World monkeys. E-book. Published privately. p 69Google Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2015

Authors and Affiliations

  • Ricardo Sampaio
    • 1
    • 2
  • Fábio Röhe
    • 3
  • Gabriela Pinho
    • 4
  • José de Sousa e Silva-Júnior
    • 5
  • Izeni Pires Farias
    • 4
  • Anthony B. Rylands
    • 6
  1. 1.Floresta Nacional do PurusInstituto Chico Mendes de Conservação da Biodiversidade (ICMBio)Boca do AcreBrazil
  2. 2.Centro Nacional de Pesquisa e Conservação de Mamíferos Carnívoros (CENAP)Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio)AtibaiaBrazil
  3. 3.Wildlife Conservation SocietyManausBrazil
  4. 4.Laboratório de Evolução e Genética Animal (LEGAL), ICBUniversidade Federal do AmazonasManausBrazil
  5. 5.Coordenação de Zoologia, Museu Paraense Emílio GoeldiBelémBrazil
  6. 6.Conservation InternationalArlingtonUSA

Personalised recommendations