A high-diversity primate community in a mid-elevation flooded forest, the Jungla de Los Monos Community Reserve, Peru

Abstract

The Alto Mayo region in the Peruvian department of San Martin has one of the highest levels of deforestation and fragmentation in the country. Historically, San Martin was home to at least 20 primate species, of which at least 14 persist in the Alto Mayo Valley. We surveyed primate populations in the “Jungla de Los Monos”, a locally protected remnant of a naturally diverse primate community in one of the last remaining mid-elevation (800 m a.s.l.) seasonally flooded forests in the region. We recorded seven primate species, with a further two species reported to have been extirpated from the area. By far the most common species was Saimiri macrodon. Half of the primate biomass was made up of a single species, Alouatta seniculus, with S. macrodon accounting for another quarter. The endemic Plecturocebus oenanthe was only detected once in forest interior, but was observed in edge and riverine forest, as well as neighboring fragments. The area holds a surprisingly high diversity and density of primates considering its proximity to population centers, thanks primarily to self-imposed hunting bans and logging control by local communities.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Allgas N, Shanee S, Shanee N, Chambers J, Tello-Alvarado JC, Keeley K, Pinasco K (2017) Natural re-establishment of a population of a critically endangered primate in a secondary forest: the San Martin titi monkey (Plecturocebus oenanthe) at the Pucunucho Private Conservation Area, Peru. Primates 58:335–342

    PubMed  Google Scholar 

  2. Allgas N, Shanee S, Shanee N, Collongues de Palomino H (2018) Rapid survey of the primate density and biomass at Katakari, Pacaya Samiria National Reserve. Peru Primate Conservation, Peru, p 32

    Google Scholar 

  3. Aquino R, López L, García G, Heymann EW (2014) Diversity, abundance and habitats of the primates in the Río Curaray Basin. Peruv Amazonia Primate Conserv 1–8:8

    Google Scholar 

  4. Ayres J (1986) Uakaris and Amazonian flooded forest. Cambridge University, Cambridge

    Google Scholar 

  5. Balmford A, Green RE, Jenkins M (2003) Measuring the changing state of nature. Trends Ecol Evol 18:326–330

    Google Scholar 

  6. Benchimol M, Pere CA (2013) Anthropogenic modulators of species–area relationships in Neotropical primates: a continental-scale analysis of fragmented forest landscapes. Divers Distrib 19:1339–1352

    Google Scholar 

  7. Benchimol M, Peres CA (2014) Predicting primate local extinctions within “real-world” forest fragments: a pan-neotropical analysis. Am J Primatol 76:289–302

    PubMed  Google Scholar 

  8. Bergl RA, Oates JF, Fotso R (2007) Distribution and protected area coverage of endemic taxa in West Africa’s Biafran forests and highlands. Biol Conserv 134:195–208

    Google Scholar 

  9. Blanco V (2013) Does the tropical agricultural matrix bear potential for primate conservation? A baseline study from western Uganda. J Nat Conserv 21:383–393

    Google Scholar 

  10. Bodmer R, Aquino R, Puertas P (1997) Alternativas de manejo para la Reserva Nacional Pacaya-Samiria: Un análisis sobre el uso sostenible de la caza. In: Fang TG, Bodmer RE, Aquino R, Valqui M (eds) Manejo de la Fauna Silvestre en la Amazonía. Springer, La Paz, pp 65–74

    Google Scholar 

  11. Boinski S (1999) The social organizations of squirrel monkeys: Implications for ecological models of social evolution. Evol Anthropol 8:101–112

    Google Scholar 

  12. Buckland S, Plumptre A, Rexstad E (2010) Design and analysis of line transect surveys for primates. Int J Primatol 31:833–847

    Google Scholar 

  13. Buckland ST, Anderson DR, Burnham KP, Laake JL (1993) An introduction to distance sampling. Oxford University Press, Oxford

    Google Scholar 

  14. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  15. Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35

    Google Scholar 

  16. Crockett CM (1984) Emigration by female red howler monkeys and the case for female competition. In: Small MF (ed) Female primates: studies by women primatologists. Alan R. Liss, New York, pp 159–173

    Google Scholar 

  17. da Silva LG, Ribeiro MC, Hasui É, da Costa CA, da Cunha RGT (2015) Patch size, functional isolation, visibility and matrix permeability influences neotropical primate occurrence within highly fragmented landscapes. PLoS ONE 10:e0114025

    PubMed  PubMed Central  Google Scholar 

  18. da Silva MNF, Shepard GH, Yu DW (2005) Conservation implications of primate hunting practices among the Matsigenka of Manu National Park. Neotropical Primates 13:31–36

    Google Scholar 

  19. Endo W, Peres CA, Salas E, Mori S, Sanchez-Vega J-L, Shepard GH, Pacheco V, Yu DW (2010) Game vertebrate densities in hunted and nonhunted forest sites in Manu National Park, Peru. Biotropica 42:251–261

    Google Scholar 

  20. Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A, Nekaris KA-I et al (2017) Impending extinction crisis of the world’s primates: Why primates matter. Sci Adv 3:1600946

    Google Scholar 

  21. Ferrari SF, Iwanaga S, Messias MR, Ramos EM, Ramos PCS, Cruz Neto EH, Coutinho PEG (2000) Titi monkeys (Callicebus spp., Atelidae: Platyrrhini) in the Brazilian state of Rondônia. Primates 41:229–234

    Google Scholar 

  22. Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280

    Google Scholar 

  23. Ford SM (1994) Evolution of sexual dimorphism in body weight in platyrrhines. Am J Primatol 34:221–244

    PubMed  Google Scholar 

  24. Ford SM, Davis LC (1992) Systematics and body size: Implications for feeding adaptations in New World monkeys. Am J Phys Anthropol 88:415–468

    CAS  PubMed  Google Scholar 

  25. Freese C, Heltne P, Napoleon C, Whitesides G (1982) Patterns and determinants of monkey densities in Peru and Bolivia, with notes on distributions. Int J Primatol 3:53–90

    Google Scholar 

  26. García D, Quevedo M, Obeso JR, Abajo A (2005) Fragmentation patterns and protection of montane forest in the Cantabrian range (NW Spain). For Ecol Manag 208:29–43

    Google Scholar 

  27. Harcourt AH, Doherty DA (2005) Species–area relationships of primates in tropical forest fragments: a global analysis. J Appl Ecol 42:630–637

    Google Scholar 

  28. Haugaasen T, Peres CA (2005a) Mammal assemblage structure in Amazonian flooded and unflooded forests. J Trop Ecol 21:133–145

    Google Scholar 

  29. Haugaasen T, Peres CA (2005b) Primate assemblage structure in Amazonian flooded and unflooded forests. Am J Primatol 67:243–258

    PubMed  Google Scholar 

  30. Haugaasen T, Peres CA (2009) Interspecific primate associations in Amazonian flooded and unflooded forests. Primates 50:239–251

    PubMed  Google Scholar 

  31. IBC (2016) Mapa: Amazonía Peruana 2016. Deforestación 2001–2015. Instituto Bien Común, Lima, Peru

    Google Scholar 

  32. IUCN (2011) Callicebus oenanthe (San Martin titi monkey). IUCN Red List of threatened species. Accessed 28 May 2012

  33. IUCN (2017) IUCN Red List of Threatened Species. www.redlist.org. Accessed 05 Mar 2019.

  34. Janson C, Emmons L (1990) Ecological structure of the nonflying mammal community at Cocha Cashu Biological Station, Manu National Park, Peru. In: Gentry AH (ed) Four neotropical forests. Yale University Press, New Haven

    Google Scholar 

  35. Klein L, Klein D (1975) Social and ecological contrasts between four taxa of neotropical primates. In: Tuttle RH (ed) Socioecology and Psychology of Primates. Mouton Publishers, The Hague, pp 59–85

    Google Scholar 

  36. Krebs CJ (1999) Ecological methodology, 2nd edn. Benjamin Cummings, Menlo Park

    Google Scholar 

  37. Lawrence J (2003) Preliminary report on the natural history of brown titi monkeys (Callicebus brunneus) at Los Amigos Research Station. Am J Phys Anthropol Suppl 36:136

    Google Scholar 

  38. Leonardi R, Buchanan-Smith Hannah M, Dufour V, MacDonald C, Whiten A (2009) Living together: behavior and welfare in single and mixed species groups of capuchin (Cebus apella) and squirrel monkeys (Saimiri sciureus). Am J Primatol 72:33–47

    Google Scholar 

  39. Levi T, Silvius KM, Oliveira LFB, Cummings AR, Fragoso JMV (2013) Competition and facilitation in the capuchin–squirrel monkey relationship. Biotropica 45:636–643

    Google Scholar 

  40. Llactayo W, Salcedo K, Victoria E (2013a) Memoria Técnica de la Cuantificación de Cambios de la Cobertura de Bosque a no Bosque por Deforestación en el Ambito de la Amazonía Peruana Periódo 2009–2010-2011. Minesterio del Ambiente, Dirrecion General de Ordanamiento Territorial, Lima

    Google Scholar 

  41. Llactayo W, Salcedo K, Victoria E (2013b) Memoria Técnica de la Cuantificación de la Cobertura de Bosque y Cambio de Bosque a no Bosque de la Amazonia Peruana Periódo 2000–2005-2009. Ministerio del Ambiente, Direccion General de Ordanamiento Territorial, Lima

    Google Scholar 

  42. Lopes MA, Ferrari SF (2000) Effects of human colonization on the abundance and diversity of mammals in Eastern Brazilian Amazonia. Conserv Biol 14:1658–1665

    Google Scholar 

  43. Lu F (1999) Changes in subsistence patterns and resource use of the Huaorani Indians in the Ecuadorian Amazon PhD. University of North Carolina, North Carolina

    Google Scholar 

  44. Manzi M, Coomes OT (2009) Managing Amazonian palms foe community use: a case study of aguaje palms (Mauritia flexuosa) in Peru. For Ecol Manag 257:510–517

    Google Scholar 

  45. Margules CR, Pressey RL (2000) Systematic conservation planning. Nature 405:243–253

    CAS  PubMed  Google Scholar 

  46. Mark M (2003) Some observations on Callicebus oenanthe in the upper Río Mayo Valley, Peru. Neotropical Primates 11:183–187

    Google Scholar 

  47. Marsh LK, Chapman CA (2013) Primates in fragments: complexity and resilience. Springer, New York

    Google Scholar 

  48. Marshall AR, Jørgensbye HIO, Rovero F, Platts PJ, White PCL, Lovett JC (2010) The species–area relationship and confounding variables in a threatened monkey community. Am J Primatol 72:325–336

    PubMed  Google Scholar 

  49. Marshall AR, Lovett JC, White PCL (2008) Selection of line-transect methods for estimating the density of group-living animals: lessons from the primates. Am J Primatol 70:452–462

    PubMed  Google Scholar 

  50. Mittermeier RA, van Roosmalen MGM (1981) Preliminary observations on habitat utilization and diet in eight Surinam monkeys. Folia Primatol 36:1–39

    CAS  Google Scholar 

  51. Muench C, Martinez-Ramos M (2016) Can community-protected areas conserve biodiversity in human-modified tropical landscapes? The case of terrestrial mammals in southern Mexico. Trop Conserv Sci 9:178–202

    Google Scholar 

  52. Neville M, Castro N, Mármol A, Revilla J (1976) Censusing primate populations in the reserved area of the Pacaya and Samiria Rivers, Department Loreto, Peru. Primates 17:151–181

    Google Scholar 

  53. Paim FP, El Bizri HR, Paglia AP, Queiroz HL (2019) Long-term population monitoring of the threatened and endemic black-headed squirrel monkey (Saimiri vanzolinii) shows the importance of protected areas for primate conservation in Amazonia. Am J Primatol 81:e22988

    PubMed  Google Scholar 

  54. Peres CA (1990) Effects of hunting on western Amazonian primate communities. Biol Conserv 54:47–59

    Google Scholar 

  55. Peres CA (1993) Structure and spatial organization of an Amazonian terra firme forest primate community. J Trop Ecol 9:259–276

    Google Scholar 

  56. Podolsky RD (1990) Effects of mixed-species association on resource use by Saimiri sciureus and Cebus apella. Am J Primatol 21:147–158

    PubMed  Google Scholar 

  57. Pozo-R WE, Youlatos D (2005) Estudio sinecologico de nueve especies de primates del Parque Nacional Yasuni. Ecuad Politec Biol 6(26):83–107

    Google Scholar 

  58. Puertas P, Bodmer RE (1993) Conservation of a high diversity primate assemblage. Biodivers Conserv 2:586–593

    Google Scholar 

  59. Puertas PE, Bodmer RE, Aquino R (1995) Diversidad y conservación de primates en la Reserva Comunal Tamshiyacu Tahuayo, Loreto. Folia Amazonica 7:113–127

    Google Scholar 

  60. Rudran R, Fernandez-Duque E (2003) Demographic changes over thirty years in a red howler population in Venezuela. Int J Primatol 24:925–947

    Google Scholar 

  61. Rylands AB, Keuroghlian A (1988) Primate survival in forest fragments in central Amazonia: preliminary results. Acta Amazon 18:291–307

    Google Scholar 

  62. Sampaio DT, Ferrari SF (2005) Predation of an Infant Titi Monkey (Callicebus moloch) by a Tufted Capuchin (Cebus apella). Folia Primatol 76:113–115

    Google Scholar 

  63. Sampaio R, Lima AP, Magnusson WE, Peres CA (2010) Long-term persistence of midsized to large-bodied mammals in Amazonian landscapes under varying contexts of forest cover. Biodivers Conserv 19:2421–2439

    Google Scholar 

  64. Schluter D (1984) A variance test for detecting species associations, with some example applications. Ecology 65:998–1005

    Google Scholar 

  65. Shanee N (2012a) The dynamics of threats and conservation efforts for the tropical Andes hotspot in Amazonas and San Martin. Kent University, Canterbury

    Google Scholar 

  66. Shanee N (2012b) Trends in local wildlife hunting, trade and control in the Tropical Andes Hotspot, northeastern Peru. Endanger Species Res 19:177–186

    Google Scholar 

  67. Shanee N (2013) Campesino justification for self-initiated conservation actions: a challenge to mainstream conservation. J Polit Ecol 20:413–428

    Google Scholar 

  68. Shanee N (2019) reclaim conservation: conservation discourse and initiatives of the Rondas Campesinas, north-eastern Peru. Conserv Soc 17:270–282

    Google Scholar 

  69. Shanee N, Shanee S (2016) Land trafficking, migration, and conservation in the "no-man's land" of northeastern Peru. Trop Conserv Sci 9:1–16

    Google Scholar 

  70. Shanee S, Tello-Alvarado JC, Vermeer J, Boveda-Penalba AJ (2011) GIS risk assessment and GAP analysis for the Andean titi monkey (Callicebus oenanthe). Primate Conserv 26:17–23

    Google Scholar 

  71. Shanee S, Shanee N, Allgas-Marchena N (2013) Primate surveys in the Maranon-Huallaga landscape, northern Peru with notes on Conservation. Primate Conserv 27:3–11

    Google Scholar 

  72. Shanee N, Shanee S, Horwich RH (2015) Effectiveness of locally run conservation initiatives in north-east Peru. Oryx 49:239–247

    Google Scholar 

  73. Shanee S, Shanee N, Monteferri B, Allgas N, Alarcon Pardo A, Horwich RH (2017) Protected area coverage of threatened vertebrates and ecoregions in Peru: comparison of communal, private and state reserves. J Environ Manag 202:12–20

    Google Scholar 

  74. Soini P (1986) A synecological study of a primate community in the Pacaya-Samiria National Reserve, Peru. Primate Conserv 7:63–71

    Google Scholar 

  75. Stone AI, Lima EM, Aguiar GFS, Camargo CC, Flores TA, Kelt DA, Marques-Aguiar SA, Queiroz JAL, Ramos RM, Silva Júnior JS (2009) Non-volant mammalian diversity in fragments in extreme eastern Amazonia. Biodivers Conserv 18:1685–1694

    Google Scholar 

  76. Thomas L, Buckland ST, Rexstad EA, Laake JL, Strindberg S, Hedley SL, Bishop JRB, Marques TA, Burnham KP (2010) Distancesoftware: design and analysis of distance sampling surveys for estimating population size. J Appl Ecol 47:5–14. https://doi.org/10.1111/j.1365-2664.2009.01737.x

    Article  PubMed  Google Scholar 

  77. van Kuijk SM, García-Suikkanen C, Tello-Alvarado JC, Vermeer J, Hill CM (2015) estimating population density of the san martin titi monkey (Callicebus oenanthe) in Peru using vocalisations. Folia Primatol 86:525–533

    Google Scholar 

  78. Van Roosmalen MGM, Van Roosmalen T, Mittermeier RA (2002) A taxonomic review of the titi monkeys, Callicebus Thomas 1903. Neotrop Primates 10(Supplement):1–52

    Google Scholar 

  79. Vuohelainen AJ, Coad L, Marthews TR, Malhi Y, Killeen TJ (2012) The effectiveness of contrasting protected areas in preventing deforestation in Madre de Dios. Peru Environ Manag 50:645–663

    Google Scholar 

  80. Wilson DE, Mittermeier RA, Ruff S, Martinez-Vilalta A, Llobet T (2013) Handbook of the mammals of the world: primates. Buteo Books, Arrington

    Google Scholar 

  81. Yoccoz NG, Nichols JD, Boulinier T (2001) Monitoring of biological diversity in space and time. Trends Ecol Evol 16:446–453

    Google Scholar 

Download references

Acknowledgements

We wish to thank Yeissy Sarmiento, Stefania Sibille Grandez, Emily Pumatinco, Lorena Fernández Hidalgo, Lidia Jimenez, Timothee Osulf, Lena Trnski, our local guides Ursula, Adolfo, Audino and the Base de Ronda Campesina de El Tambo for their help in the field, as well as the people of El Tambo Village for allowing us to work in their forests and for the conservation work they do. This study was funded by Neotropical Primate Conservation thanks to grants from Primate Conservation Inc., the Primate Society of Great Britain, and the International Primatological Society. All research was carried out under Permit No 173–2016-SERFOR/DGGSPFFS.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sam Shanee.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

About this article

Verify currency and authenticity via CrossMark

Cite this article

Shanee, S., Allgas, N., Ocampo-Carvajal, C. et al. A high-diversity primate community in a mid-elevation flooded forest, the Jungla de Los Monos Community Reserve, Peru. Primates 62, 189–197 (2021). https://doi.org/10.1007/s10329-020-00833-2

Download citation

Keywords

  • Densities
  • Biomass
  • Distance sampling
  • Interspecies association
  • Habitat
  • Community conservation