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International Journal of Primatology

, Volume 40, Issue 4–5, pp 553–572 | Cite as

Terrestrial Behavior in Titi Monkeys (Callicebus, Cheracebus, and Plecturocebus): Potential Correlates, Patterns, and Differences between Genera

  • João Pedro Souza-AlvesEmail author
  • Italo Mourthe
  • Renato R. Hilário
  • Júlio César Bicca-Marques
  • Jennifer Rehg
  • Carla C. Gestich
  • Adriana C. Acero-Murcia
  • Patrice Adret
  • Rolando Aquino
  • Mélissa Berthet
  • Mark Bowler
  • Armando M. Calouro
  • Gustavo R. Canale
  • Nayara de A. Cardoso
  • Christini B. Caselli
  • Cristiane Cäsar
  • Renata R. D. Chagas
  • Aryanne Clyvia
  • Cintia F. Corsini
  • Thomas Defler
  • Anneke DeLuycker
  • Anthony Di Fiore
  • Kimberly Dingess
  • Gideon Erkenswick
  • Michele Alves Ferreira
  • Eduardo Fernandez-Duque
  • Stephen F. Ferrari
  • Isadora P. Fontes
  • Josimar Daniel Gomes
  • Frederico P. R. Gonçalves
  • Maurício Guerra
  • Torbjørn Haugaasen
  • Stefanie Heiduck
  • Eckhard W. Heymann
  • Shannon Hodges
  • Rosario Huashuayo-Llamocca
  • Leandro Jerusalinsky
  • Carlos Benhur Kasper
  • Jenna Lawrence
  • Teresa Magdalena Lueffe
  • Karine G. D. Lopes
  • Jesús Martínez
  • Fabiano R. de Melo
  • Mariluce Rezende Messias
  • Mariana B. Nagy-Reis
  • Inés Nole
  • Filipa Paciência
  • Erwin Palacios
  • Alice Poirier
  • Grasiela Porfírio
  • Amy Porter
  • Eluned Price
  • Rodrigo C. Printes
  • Erika P. Quintino
  • Evandro Amato Reis
  • Alessandro Rocha
  • Adriana Rodríguez
  • Fábio Röhe
  • Damian Rumiz
  • Sam Shanee
  • Marina M. Santana
  • Eleonore Z. F. Setz
  • Francisco Salatiel C. de Souza
  • Wilson Spironello
  • Emérita R. Tirado Herrera
  • Luana Vinhas
  • Kevina Vulinec
  • Robert B. Wallace
  • Mrinalini Watsa
  • Patricia C. Wright
  • Robert J. Young
  • Adrian A. Barnett
Article

Abstract

For arboreal primates, ground use may increase dispersal opportunities, tolerance to habitat change, access to ground-based resources, and resilience to human disturbances, and so has conservation implications. We collated published and unpublished data from 86 studies across 65 localities to assess titi monkey (Callicebinae) terrestriality. We examined whether the frequency of terrestrial activity correlated with study duration (a proxy for sampling effort), rainfall level (a proxy for food availability seasonality), and forest height (a proxy for vertical niche dimension). Terrestrial activity was recorded frequently for Callicebus and Plecturocebus spp., but rarely for Cheracebus spp. Terrestrial resting, anti-predator behavior, geophagy, and playing frequencies in Callicebus and Plecturocebus spp., but feeding and moving differed. Callicebus spp. often ate or searched for new leaves terrestrially. Plecturocebus spp. descended primarily to ingest terrestrial invertebrates and soil. Study duration correlated positively and rainfall level negatively with terrestrial activity. Though differences in sampling effort and methods limited comparisons and interpretation, overall, titi monkeys commonly engaged in a variety of terrestrial activities. Terrestrial behavior in Callicebus and Plecturocebus capacities may bolster resistance to habitat fragmentation. However, it is uncertain if the low frequency of terrestriality recorded for Cheracebus spp. is a genus-specific trait associated with a more basal phylogenetic position, or because studies of this genus occurred in pristine habitats. Observations of terrestrial behavior increased with increasing sampling effort and decreasing food availability. Overall, we found a high frequency of terrestrial behavior in titi monkeys, unlike that observed in other pitheciids.

Keywords

Callicebinae Fruit availability Ground use Predation risk Sampling effort 

Notes

Acknowledgments

All authors thank the numerous sources that funded, helped, and supported the various research projects from which the data were compiled and analyzed. We are grateful the Joanna Setchell and two anonymous reviewers for the valuable consideration in the manuscript.

Author Contributions

JPS-A and AAB conceived and designed the experiments. RRH and IM analyzed the data. JPS-A and AAB wrote the first draft of manuscript. All the authors revised the manuscript.

Supplementary material

10764_2019_105_MOESM1_ESM.docx (73 kb)
ESM 1 (DOCX 73 kb)

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • João Pedro Souza-Alves
    • 1
    • 14
    Email author
  • Italo Mourthe
    • 2
  • Renato R. Hilário
    • 3
  • Júlio César Bicca-Marques
    • 4
  • Jennifer Rehg
    • 5
  • Carla C. Gestich
    • 6
  • Adriana C. Acero-Murcia
    • 7
  • Patrice Adret
    • 8
  • Rolando Aquino
    • 9
  • Mélissa Berthet
    • 10
  • Mark Bowler
    • 11
  • Armando M. Calouro
    • 12
  • Gustavo R. Canale
    • 13
  • Nayara de A. Cardoso
    • 14
  • Christini B. Caselli
    • 15
  • Cristiane Cäsar
    • 16
  • Renata R. D. Chagas
    • 14
  • Aryanne Clyvia
    • 17
  • Cintia F. Corsini
    • 18
  • Thomas Defler
    • 19
  • Anneke DeLuycker
    • 20
  • Anthony Di Fiore
    • 21
  • Kimberly Dingess
    • 22
  • Gideon Erkenswick
    • 23
  • Michele Alves Ferreira
    • 17
  • Eduardo Fernandez-Duque
    • 24
  • Stephen F. Ferrari
    • 25
  • Isadora P. Fontes
    • 26
  • Josimar Daniel Gomes
    • 27
  • Frederico P. R. Gonçalves
    • 28
  • Maurício Guerra
    • 29
  • Torbjørn Haugaasen
    • 30
  • Stefanie Heiduck
    • 31
  • Eckhard W. Heymann
    • 31
  • Shannon Hodges
    • 32
  • Rosario Huashuayo-Llamocca
    • 33
  • Leandro Jerusalinsky
    • 34
  • Carlos Benhur Kasper
    • 35
  • Jenna Lawrence
    • 36
  • Teresa Magdalena Lueffe
    • 31
  • Karine G. D. Lopes
    • 37
  • Jesús Martínez
    • 38
  • Fabiano R. de Melo
    • 39
    • 40
  • Mariluce Rezende Messias
    • 41
  • Mariana B. Nagy-Reis
    • 6
  • Inés Nole
    • 42
  • Filipa Paciência
    • 31
  • Erwin Palacios
    • 43
  • Alice Poirier
    • 44
  • Grasiela Porfírio
    • 45
  • Amy Porter
    • 46
  • Eluned Price
    • 47
  • Rodrigo C. Printes
    • 48
  • Erika P. Quintino
    • 49
  • Evandro Amato Reis
    • 17
  • Alessandro Rocha
    • 50
  • Adriana Rodríguez
    • 43
  • Fábio Röhe
    • 51
  • Damian Rumiz
    • 52
  • Sam Shanee
    • 53
  • Marina M. Santana
    • 54
  • Eleonore Z. F. Setz
    • 55
  • Francisco Salatiel C. de Souza
    • 56
  • Wilson Spironello
    • 57
  • Emérita R. Tirado Herrera
    • 58
  • Luana Vinhas
    • 59
  • Kevina Vulinec
    • 60
  • Robert B. Wallace
    • 38
  • Mrinalini Watsa
    • 61
  • Patricia C. Wright
    • 62
  • Robert J. Young
    • 63
  • Adrian A. Barnett
    • 64
    • 65
  1. 1.Programa de Pós-graduação em Biologia Animal, Departamento de ZoologiaUniversidade Federal de PernambucoRecifeBrazil
  2. 2.Programa de Pós-graduação em Biodiversidade e ConservaçãoUniversidade Federal do ParáAltamiraBrazil
  3. 3.Departamento de Meio Ambiente e DesenvolvimentoUniversidade Federal do AmapáMacapáBrazil
  4. 4.Escola de Ciências da Saúde e da VidaPontifícia Universidade Católica do Rio Grande do SulPorto AlegreBrazil
  5. 5.Department of AnthropologySouthern Illinois UniversityEdwardsvilleUSA
  6. 6.Programa de Pós-graduação em Ecologia, Instituto de BiologiaUniversidade Estadual de CampinasSão PauloBrazil
  7. 7.Programa de Pós-graduação em Ecologia e EvoluçãoUniversidade Federal de São PauloSão PauloBrazil
  8. 8.Museo de Historia Natural Noel Kempff MercadoSanta Cruz de La SierraBolivia
  9. 9.Universidad Nacional Mayor de San Marcos, Facultad de Ciencias BiológicasLimaPeru
  10. 10.Department of Comparative CognitionUniversity of NeuchâtelNeuchâtelSwitzerland
  11. 11.School of Science, Technology and EngineeringUniversity of SuffolkSuffolkUK
  12. 12.Centro de Ciências Biológicas e da NaturezaUniversidade Federal do AcreRio BrancoBrazil
  13. 13.Núcleo de Estudos da Amazônia MatogrossenseUniversidade Federal do Mato GrossoMato GrossoBrazil
  14. 14.Programa de Pós-graduação em Ciências Biológicas (Zoologia), Departamento de Sistemática e EcologiaUniversidade Federal da ParaíbaJoão PessoaBrazil
  15. 15.Departamento de BiologiaUniversidade Federal Rural de PernambucoRecifeBrazil
  16. 16.Museu de Ciências Naturais PUC MinasMinas GeraisBrazil
  17. 17.Bicho do Mato Meio AmbienteBelo HorizonteBrazil
  18. 18.Programa de Capacitação InstitucionalInstituto Nacional da Mata AtlânticaEspírito SantoBrazil
  19. 19.Departamento de BiologíaUniversidad Nacional de ColombiaBogotáColombia
  20. 20.Smithsonian-Mason School of ConservationSmithsonian Conservation Biology InstituteFront RoyalUSA
  21. 21.Department of AnthropologyUniversity of Texas at AustinAustinUSA
  22. 22.Department of AnthropologyIndiana UniversityBloomingtonUSA
  23. 23.Department of BiologyUniversity of Missouri-St. LouisSt. LouisUSA
  24. 24.Department of AnthropologyYale UniversityNew HavenUSA
  25. 25.Departamento de EcologiaUniversidade Federal de SergipeSão CristóvãoBrazil
  26. 26.Secretaria Municipal de Meio Ambiente de AracajuAracajuBrazil
  27. 27.Anglo American Minério de Ferro Brasil S/AMinas GeraisBrazil
  28. 28.Programa de Pós-graduação em Sustentabilidade e Tecnologia AmbientalInstituto Federal de Minas GeraisBambuíBrazil
  29. 29.Parques Nacionales Naturales de ColombiaParque Nacional Natural AmacayacuLeticiaColombia
  30. 30.Faculty of Environmental Sciences and Natural Resource ManagementNorwegian University of Life SciencesÅsNorway
  31. 31.Verhaltensökologie & Soziobiologie, Deutsches PrimatenzentrumGöttingenGermany
  32. 32.Department of AnthropologyTexas A&M UniversityCollege StationUSA
  33. 33.Proyecto Mono TocónMoyobambaPeru
  34. 34.Centro Nacional de Pesquisa e Conservação de Primatas BrasileirosInstituto Chico Mendes de Conservação da BiodiversidadeJoão PessoaBrazil
  35. 35.Laboratório de Biologia de Mamíferos e AvesUniversidade Federal do Pampa, Campus de São GabrielSão GabrielBrazil
  36. 36.Department of Ecology, Evolution, and Environmental BiologyColumbia UniversityNew YorkUSA
  37. 37.Programa de Pós-Graduação em ZoologiaPontifícia Universidade Católica do Rio Grande do SulPorto AlegreBrazil
  38. 38.Wildlife Conservation Society-BoliviaLa PazBolivia
  39. 39.Instituto de BiociênciasUniversidade Federal de Goiás, Regional JataíGoiâniaBrazil
  40. 40.Departamento de Engenharia FlorestalUniversidade Federal de ViçosaViçosaBrazil
  41. 41.Laboratório de Mastozoologia & Vertebrados Terrestres, Departamento de BiologiaUniversidade Federal de RondôniaPorto VelhoBrazil
  42. 42.Facultad de Medicina VeterinariaUniversidad Nacional Mayor de San MarcosLimaPeru
  43. 43.Conservation International-ColombiaBogotáColombia
  44. 44.Department of Life SciencesAnglia Ruskin UniversityCambridgeUK
  45. 45.Programa de Pós-Graduação em Ciências Ambientais e Sustentabilidade AgropecuáriaUniversidade Católica Dom BoscoCampo GrandeBrazil
  46. 46.Department of AnthropologyUniversity of CaliforniaDavisUSA
  47. 47.Durrell Wildlife Conservation TrustJerseyUK
  48. 48.Laboratório de Gestão Ambiental e Negociação de ConflitosUniversidade Estadual do Rio Grande do SulSão Francisco de PaulaBrazil
  49. 49.Laboratório de PrimatologiaPontifícia Universidade Católica do Rio Grande do SulPorto AlegreBrazil
  50. 50.Núcleo de BiodiversidadeInstituto Nacional de Pesquisas da AmazôniaManausBrazil
  51. 51.World Conservation Society BrazilManausBrazil
  52. 52.Fundación Simón I. PatiñoSanta Cruz de la SierraBolivia
  53. 53.Neotropical Primate Conservation UKManchesterUK
  54. 54.Departamento de Ecologia, Programa de Pós-graduação em Ecologia e ConservaçãoUniversidade Federal de SergipeSão CristóvãoBrazil
  55. 55.Departamento de Biologia AnimalUniversidade Estadual de CampinasSão PauloBrazil
  56. 56.Programa de Pós-graduação em Ecologia e Manejo de Recursos NaturaisUniversidade Federal do AcreAcreBrazil
  57. 57.Grupo de Pesquisa de Mamíferos da AmazôniaInstituto Nacional de Pesquisas da AmazôniaManausBrazil
  58. 58.Universidad Nacional de la Amazonía PeruanaIquitosPeru
  59. 59.Departamento de BiologiaUniversidade Católica do SalvadorBahiaBrazil
  60. 60.Department of Agriculture & Natural ResourcesDelaware State UniversityDoverUSA
  61. 61.Department of AnthropologyWashington University in Saint LouisSt. LouisUSA
  62. 62.Department of AnthropologyState University of New York at Stony BrookStony BrookUSA
  63. 63.Department of BiologyUniversity of SalfordManchesterUK
  64. 64.Grupo de Pesquisa de Mamíferos da AmazôniaInstituto Nacional de Pesquisas da AmazôniaManausBrazil
  65. 65.Centre for Research in Evolutionary AnthropologyRoehampton UniversityLondonUK

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