Effect of historical logging pressure on squirrel monkey (Saimiri cassiquiarensis macrodon) population density and primate species richness in the Peruvian Amazon

John Rowland; Richard Bodmer; Miguel Antunez; Dave Seaman

doi:10.62015/np.2024.v30.800

Authors

John Rowland Durrell Institute of Conservation and Ecology, University of Kent
Richard Bodmer Durrell Institute of Conservation and Ecology, University of Kent; FundAmazonia
Miguel Antunez FundAmazonia, Museum of Amazonian Indigenous Cultures, 332 Malecon Tarapaca, Iquitos, Peru
Dave Seaman Durrell Institute of Conservation and Ecology, University of Kent

DOI:

https://doi.org/10.62015/np.2024.v30.800

Keywords:

Indigenous lands, anthropogenic disturbance, distance sampling, population density, primate communities

Abstract

Primates in the Amazon are threatened by the expansion of human activities, including logging. Here, we investigate how primate communities are affected by different forest use and disturbance histories in two adjacent indigenous territories. We assess how logging in the recent past has changed primate community composition. One of the territories was protected from selective commercial logging activities, whilst the other had decades of selective logging before starting the process of becoming an indigenous territory in 2012. The past logging has left forest gaps and secondary forests, and was accompanied by small agricultural plots. Using line transect surveys and distance sampling analysis, we compared primate species richness between the two territories, and the density of the ecologically dominant squirrel monkey species, Saimiri cassiquiarensis macrodon. Villa Belén, the territory with more recent and more intense logging supported a higher population density of squirrel monkeys (192 indiv./km²) than Jaldar (107 indiv./km²), the territory with a less intense and more distant logging history. We found no difference in squirrel monkey group size between the forests of Villa Belén and Jaldar. Primate species richness declined as logging pressure and anthropogenic disturbance increased with an estimated richness of seven primate species in Villa Belén, compared to 11 primate species in Jaldar. Our findings suggest that squirrel monkeys can persist in tropical forests with high levels of historical logging pressure and at greater densities than in less disturbed areas with higher overall primate species richness.

References

Almeida-Rocha, J. M. D., Peres, C. A. and Oliveira, L. C. 2017. Primate responses to anthropogenic habitat disturbance: a pantropical meta-analysis. Biol. Conserv. 215: 30–38. https://doi.org/10.1016/j.biocon.2017.08.018

Anaya, F. C. and Espírito-Santo, M. M. 2018. Protected areas and territorial exclusion of traditional communities. Ecol. Soc. 23(1): 8. https://doi.org/10.5751/ES-09850-230108

Balvanera, P., Pfisterer, A. B., Buchmann, N., He, J., Nakashizuka, T., Raffaelli, D. and Schmid, B. 2006. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol. Lett. 9: 1146–1156. https://doi.org/10.1111%2Fj.1461-0248.2006.00963.x

Bicknell, J. E., Struebig, M. J., Edwards, D. P. and Davies, Z. G. 2014. Improved timber harvest techniques maintain biodiversity in tropical forests. Curr. Biol. 24: R1119-R1120. https://doi.org/10.1016/j.cub.2014.10.067

Blackman, A., Corral, L., Lima, E. S. and Asner, G. P. 2017. Titling indigenous communities protects forests in the Peruvian Amazon. Proc. Natl. Acad. Sci. U.S.A. 114(16): 4123–4128. https://doi.org/10.1073/pnas.1603290114

Bodmer, R., Fang, T., Puertas, P., Antunez, M., Chota, K. and Bodmer, W. 2014. Cambio Climático y Fauna Silvestre en la Amazonía Peruana. Gráfica Biblos, Lima.

Bodmer, R., Puertas, P. and Fang, T. G. 2008. Co-managing wildlife in the Amazon and the salvation of the Pacaya-Samiria National Reserve in Peru. In: Wildlife and Society. The Science of Human Dimensions, M. Manfredo, J. Vaske, P. Brown, D. Decker, and E. Duke (eds.), p. 104–116, Island Press, Washington DC, USA.

Boinski, S. 1999. The social organizations of squirrel monkeys: implications for ecological models of social evolution. Evol. Anthropol. 8: 101–112. https://doi.org/10.1002/(SICI)1520-6505(1999)8:3%3C101::AID-EVAN5%3E3.0.CO;2-O

Boinski, S., Kauffman, L., Westoll, A., Stickler, C. M., Cropp, S. and Ehmke, E. 2003. Are vigilance, risk from avian predators and group size consequences of habitat structure? A comparison of three species of squirrel monkey (Saimiri oerstedii, S. boliviensis, and S. sciureus). Behaviour 140: 1421–1467. https://www.jstor.org/stable/4536101

Bousfield, C. G., Massam, M., Peres, C. and Edwards, D. 2023. Large‐scale impacts of selective logging on canopy tree beta‐diversity in the Brazilian Amazon. J. Appl. Ecol. 60(6): 1181–1193. https://doi.org/10.1111/1365-2664.14403

Buckland, S. et al. 2001. Introduction to Distance Sampling Estimating Abundance of Biological Populations. Oxford University Press, Oxford.

Campos, F. A. and Fedigan, L. M. 2009. Behavioral adaptations to heat stress and water scarcity in white‐faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. Am. J. of Phys. Anthropol. 138: 101–111. https://doi.org/10.1002/ajpa.20908

da Silva, L. B., Oliveira, G. L., Frederico, R. G., Loyola, R., Zacarias, D., Ribeiro, B. R. and Mendes-Oliveira, A.C. 2022. How future climate change and deforestation can drastically affect the species of monkeys endemic to the eastern Amazon, and priorities for conservation. Biodivers. and Conserv. 31: 971–988. https://doi.org/10.1007/s10531-022-02373-1

Estrada, A., Raboy, B. E. and Oliveira, L. C. 2012. Agroecosystems and primate conservation in the tropics: a review. Am. J. of Primatol. 74: 696–711. https://doi.org/10.1002/ajp.22033

Figueira, A. M. E. S., Miller, S. D., de Sousa, C. A. D., Menton, M. C., Maia, A. R., da Rocha, H. R. and Goulden, M. L. 2008. Effects of selective logging on tropical forest tree growth. J. Geophys. Res. 113: G00B05. https://doi.org/10.1029/2007JG000577

Hill, J., Hamer, K., Tangah, J. and Dawood, M. 2001. Ecology of tropical butterflies in rainforest gaps. Oecologia 128: 294–302. https://doi.org/10.1007/s004420100651

Irion, G. 1978. Soil infertility in the Amazonian rain forest. Naturwissenschaften 65: 515-519. https://doi.org/10.1007/BF00439791

Janson, C. H. and Goldsmith, M. L. 1995. Predicting group size in primates: Foraging costs and predation risks. Behav. Ecol. 6: 326–336. https://doi.org/10.1093/beheco/6.3.326

Laurance, W. F ., Carolina Useche, D., Rendeiro, J. et al. 2012. Averting biodiversity collapse in tropical forest protected areas. Nature 489: 290–294. https://doi.org/10.1038/nature11318

Leca, J. B., Gunst, N., Rompis, A., Soma, G., Arta Putra, I. G. A. and Nengah Wandia, I. 2013. Population density and abundance of ebony leaf monkeys (Trachypithecus auratus) in West Bali National Park, Indonesia. Primate Conserv. 26(1): 133–144. https://doi.org/10.1896/052.026.0106

Link, A., Palacios, E., de la Torre, S., Paim, F. P., Silva Júnior, J. S., Heymann, E. W., Moscoso, P., Lynch Alfaro, J. W., Ravetta, A. L. and Calouro, A. M. 2021. Saimiri cassiquiarensis ssp. macrodon (amended version of 2020 assessment). The IUCN Red List of Threatened Species 2021: e.T43971A192585245.

Mahabale, D., Bodmer, R., Pizuri, O., Uraco, P., Chota, K., Antunez, M. and Groombridge, J. 2025. Sustainability of hunting in community-based wildlife management in the Peruvian Amazon. Sustainability 17(3): 914. https://doi.org/10.3390/su17030914

Miranda, J. J., Corral, L., Blackman, A., Asner, G. and Lima, E. 2016. Effects of protected areas on forest cover change and local communities: evidence from the Peruvian Amazon. World Dev. 78: 288–307. https://doi.org/10.1016/j.worlddev.2015.10.026

Mitchell, C. L., Boinski, S. and van Schaik, C. P. 1991. Competitive regimes and female bonding in two species of squirrel monkeys (Saimiri oerstedi and S. sciureus). Behav. Ecol. Sociobiol. 28: 55–60. https://doi.org/10.1007/BF00172139

Mitchell, C. L. 1994. Migration alliances and coalitions among adult male South American squirrel monkeys (Saimiri sciureus). Behaviour 134(3-4): 169–190. https://www.jstor.org/stable/4535215

Oliveira-Silva, L. R. B., Campêlo, A. C., Lima, I. M. S., Araújo, A., Bezerra, B. M. and Souza-Alves, J. P. 2018. Can a non-native primate be a potential seed disperser? A case study on Saimiri sciureus in Pernambuco state, Brazil. Folia Primatol. 89(2): 138–149. https://doi.org/10.1159/000486413

Paim, F. P., El Bizri, H. R., Paglia, A. P. and Queiroz, H. L. 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. https://doi.org/10.1002/ajp.22988

Parolin, P., Ferreira, L. V., Albernaz, A. L. K. M. and Almeida, S. S. 2004. Tree species distribution in várzea forests of Brazilian Amazonia. Folia Geobot. 39: 371–383. https://doi.org/10.1007/BF02803209

Pereira, E. J. A. L., Ribeiro, L. C. S., Freitas, L. F. S. and Pereira, H. B. B. 2020. Brazilian policy and agribusiness damage the Amazon rainforest. Land Use Policy 92: 104491. https://doi.org/10.1016/j.landusepol.2020.104491

Piponiot, C., Rödig, E., Putz, F. E., Rutishauser, E., Sist, P., Ascarrunz, N., Blanc, L., Derroire, G., Descroix, L. and Guedes, M. C. 2019. Can timber provision from Amazonian production forests be sustainable? Environ. Res. Letters 14: 064014. https://doi.org/10.1088/1748-9326/ab195e

Putz, F. E., Sist, P., Fredericksen, T. and Dykstra, D. 2008. Reduced-impact logging: challenges and opportunities. For. Eco. Manage. 256: 1427–1433. https://doi.org/10.1016/j.foreco.2008.03.036

Räsänen, M. E., Salo, J. S. and Kalliola, R. J. 1987. Fluvial perturbance in the western Amazon Basin: regulation by long-term sub-Andean tectonics. Science 238: 1398–1401. https://doi.org/10.1126/science.238.4832.1398

Ruiz-García, M., Luengas-Villamil, K., Leguizamon, N. et al. 2015. Molecular phylogenetics and phylogeography of all the Saimiri taxa (Cebidae, Primates) inferred from mt COI and COII gene sequences. Primates 56(2): 145–161. https://doi.org/10.1007/s10329-014-0452-0

Sze, J. S., Carrasco, L. R., Childs, D. and Edwards, D.P. 2022. Reduced deforestation and degradation in indigenous Lands pan-tropically. Nat. Sustain. 5: 123–130. https://doi.org/10.1038/s41893-021-00815-2

Sze, J. S., Childs, D. Z., Carrasco, L. R. Fernández‐Llamazares, Á., Garnett, S. T. and Edwards, D. P. 2024. Indigenous peoples’ lands are critical for safeguarding vertebrate diversity across the tropics. Glob. Chang. Biol. 30: e16981. https://doi.org/10.1111/gcb.16981

Terborgh, J. and Janson, C. H. 1986. The socioecology of primate groups. Annu. Rev. Ecol. and Syst. 17: 111–136. https://www.jstor.org/stable/2096991

Thomas, L., Buckland, S. T., Rexstad, E. A., Laake, J. L., Strindberg, S., Hedley, S. L., Bishop, J. R. B., Marques, T. A. and Burnham, K. P. 2010. Distance software: 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

Touchton, J., Hsu, Y. C. and Palleroni, A. 2002. Foraging ecology of reintroduced captive-bred subadult harpy eagles (Harpia harpyja) on Barro Colorado Island, Panama. Ornitol. Neotrop. 13: 365–379. https://digitalcommons.usf.edu/ornitologia_neotropical/vol13/iss4/2

Ugland, K. I., Gray, J. S. and Ellingsen, K. E. 2003. The species–accumulation curve and estimation of species richness. J. Anim. Ecol. 72: 888–897. https://doi.org/10.1046/j.1365-2656.2003.00748.x

Watkins, E., Kitching, R. L., Nakamura, A. and Stork, N. E. 2017. Beetle assemblages in rainforest gaps along a subtropical to tropical latitudinal gradient. Biodivers. Conserv. 26: 1689–1703. https://doi.org/10.1007/s10531-017-1326-8

Young, H. S., McCauley, D. J., Galetti, M. and Dirzo, R. 2016. Patterns, causes, and consequences of Anthropocene defaunation. Annu. Rev. Ecol. Evol. Syst. 47: 333–358. https://doi.org/10.1146/annurev-ecolsys-112414-054142