Abstract
The intensive deforestation, together with the projections of climate change, indicates severe effects of human actions on biodiversity in the Amazon, especially on species that depend on forest cover, such as primates. In this research, we identified priority areas for the conservation of 12 primate species endemic to the eastern Amazon. We created habitat suitability models for each species based on climatic conditions and deforestation under current and future scenarios (2050). We compared possible losses or gains of potential distribution areas in the present and future, based on climate change and loss of forest cover. Our results show that 11 of the 12 species could lose an area of climate suitability in the future, and more than 30% of them might lose over 90% of their range. Considering both climate change and deforestation, 8 out of 12 endemic primate species from the eastern Amazon could have their distribution area reduced by over 90% by 2050. About 25% of these species could become extinct in the next 30 years, with a predicted decrease of more than 98% in their distribution. However, this pessimistic scenario could be assuaged with an increase of 2 to 10% of protected areas, placed in specific prioritized areas, as we defined in our study as a high conservation priority, especially in the northeast of the eastern Amazon. The current scenario of devastation in the Amazon needs to be immediately reversed in time to recover native environments that promote the conservation of biodiversity. Our research tries to point out a strategy directed to conserving the Amazon primates and their habitats.
Similar content being viewed by others
Data availability
The information used in the paper is available in the body of the text and in the supplementary materials.
Code availability
Not applicable.
References
Aiello-Lammens ME, Boria RA, Radosavljevic A, Vilela B, Anderson RP (2015) spThin: an R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography 38:541–545. https://doi.org/10.1111/ecog.01132
Andrade AF, Velazco SJ, De Marco JP (2020) ENMTML: an R package for a straightforward construction of complex ecological niche models. Environ Model Softw 125:104615. https://doi.org/10.1016/j.envsoft.2019.104615
Andresen E, Arroyo-Rodríguez V, Ramos-Robles M (2018) Primate seed dispersal: old and new challenges. Int J Primatol 39:443–465. https://doi.org/10.1007/s10764-018-0024-z
Anjos LJS, de Toledo PM (2018) Measuring resilience and assessing vulnerability of terrestrial ecosystems to climate change in South America. PLoS ONE 13:e0194654. https://doi.org/10.1371/journal.pone.0194654
Arroyo-Rodríguez V, Fahrig L, Tabarelli M et al (2020) Designing optimal human-modified landscapes for forest biodiversity conservation. Ecol Lett. https://doi.org/10.1111/ele.13535
Arvor D, Tritsch I, Barcellos C et al (2017) Land use sustainability on the South-Eastern Amazon agricultural frontier: recent progress and the challenges ahead. Appl Geogr 80:86–97. https://doi.org/10.1016/j.apgeog.2017.02.003
Barber CP, Cochrane MA, Souza CM, Laurance WF (2014) Roads, deforestation, and the mitigating effect of protected areas in the Amazon. Biol Conserv 177:203–209. https://doi.org/10.1016/j.biocon.2014.07.004
Barona E, Ramankutty N, Hyman G, Coomes OT (2010) The role of pasture and soybean in deforestation of the Brazilian Amazon. Environ Res Lett 5:024002. https://doi.org/10.1088/1748-9326/5/2/024002
Benchimol M, Peres CA (2014) Predicting primate local extinctions within “real-world” forest fragments: a pan-neotropical analysis. Am J Primatol 76:289–302. https://doi.org/10.1002/ajp.22233
Benchimol M, Peres CA (2015) Predicting local extinctions of Amazonian vertebrates in forest islands created by a mega dam. Biol Conserv 187:61–72. https://doi.org/10.1016/j.biocon.2015.04.005
Bolt LM, Schreier AL, Voss KA et al (2018) The influence of anthropogenic edge effects on primate populations and their habitat in a fragmented rainforest in Costa Rica. Primates 59:301–311. https://doi.org/10.1007/s10329-018-0652-0
Boyle SA, Smith AT (2010) Can landscape and species characteristics predict primate presence in forest fragments in the Brazilian Amazon? Biol Conserv 143:1134–1143. https://doi.org/10.1016/j.biocon.2010.02.008
Breiman L (2001) Random forests. Mach Learn 45:5–32. https://doi.org/10.1023/A:1010933404324
Buckland STE, Elston DA (1993) Empirical models for the distribution of wildlife. J Appl Ecol 30:478–495
Carvalho JS, Graham B, Rebelo H et al (2019) A global risk assessment of primates under climate and land use/cover scenarios. Glob Chang Biol 25:3163–3178. https://doi.org/10.1111/gcb.14671
Chapman CA, Bonnell TR, Gogarten JF et al (2013) Are primates ecosystem engineers? Int J Primatol 34:1–14. https://doi.org/10.1007/s10764-012-9645-9
Ciemer C, Boers N, Hirota M et al (2019) Higher resilience to climatic disturbances in tropical vegetation exposed to more variable rainfall. Nat Geosci 12:174–179. https://doi.org/10.1038/s41561-019-0312-z
Coetzee BWT (2016) Evaluating the ecological performance of protected areas. Biodivers Conserv 26:231–236. https://doi.org/10.1007/s10531-016-1235-2
Cook B, Zeng N, Yoon J-H (2012) Will Amazonia dry out? Magnitude and causes of change from IPCC climate model projections. Earth Interact 16:1–27. https://doi.org/10.1175/2011EI398.1
da Silva FA, Canale GR, Kierulff MCM et al (2016) Hunting, pet trade, and forest size effects on population viability of a critically endangered Neotropical primate, Sapajus xanthosternos (Wied-Neuwied, 1826). Am J Primatol 78:950–960. https://doi.org/10.1002/ajp.22565
de Solar RRC, Barlow J, Andersen AN et al (2016) Biodiversity consequences of land-use change and forest disturbance in the Amazon: a multi-scale assessment using ant communities. Biol Conserv 197:98–107. https://doi.org/10.1016/j.biocon.2016.03.005
Devillers R, Pressey RL, Grech A et al (2015) Reinventing residual reserves in the sea: are we favouring ease of establishment over need for protection? Aquat Conserv Mar Freshw Ecosyst 25:480–504. https://doi.org/10.1002/aqc.2445
Dillon ME, Wang G, Huey RB (2010) Global metabolic impacts of recent climate warming. Nature 467:704–707. https://doi.org/10.1038/nature09407
Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40(1):677–697. https://doi.org/10.1146/annurev.ecolsys.110308.120159
Emmons LH (1995) Mammals of rain forest canopies. In: Lowman MD, Nadkarni NM (eds) Forest canopies. Academic Press, New York, pp 199–223
Estrada A, Garber PA, Rylands AB et al (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3:e1600946. https://doi.org/10.1126/sciadv.1600946
Ferro VG, Lemes P, Melo AS, Loyola R (2014) The reduced effectiveness of protected areas under climate change threatens atlantic forest tiger moths. PLoS ONE 9:e107792. https://doi.org/10.1371/journal.pone.0107792
Fialho AS, Canale GR (2015) Avaliação do Risco de Extinção de Mico emiliae (Thomas, 1920) no Brasil. Processo de avaliação do risco de extinção da fauna brasileira. ICMBio. Available at http://www.icmbio.gov.br/portal/biodiversidade/fauna-brasileira/estado-de-conservacao/7215-mamiferos-mico-emiliae-sagui-de-snethlage.html
Fialho MS, Moura EF, Ravetta AL, et al. (2015) Avaliação do Risco de Extinção de Cebus kaapori (Queiroz, 1992) no Brasil. In: Process. avaliação do risco extinção da fauna Bras. ICMBio. Available at http://www.icmbio.gov.br/portal/biodiversidade/fauna-brasileira/lista-de-especies/7259-mamiferos-cebus-kaapori-cairara.html. Accessed 2 Apr 2020
Fleagle JG (2013) New world anthropoids. Primate adaptation and evolution, 3rd edn. Elsevier, Amsterdam, pp 89–118
Fourcade Y, Engler JO, Rödder D, Secondi J (2014) Mapping species distributions with MAXENT using a geographically biased sample of presence data: a performance assessment of methods for correcting sampling bias. PLoS ONE 9:e97122. https://doi.org/10.1371/journal.pone.0097122
Gatti LV, Basso LS, Miller JB et al (2021) Amazonia as a carbon source linked to deforestation and climate change. Nature 595:388–393. https://doi.org/10.1038/s41586-021-03629-6
Graham TL, Matthews HD, Turner SE (2016) A global-scale evaluation of primate exposure and vulnerability to climate change. Int J Primatol 37:158–174. https://doi.org/10.1007/s10764-016-9890-4
Grelle CEV (2005) Predicting extinction of mammals in the Brazilian Amazon. Oryx 39:347–350. https://doi.org/10.1017/S0030605305000700
Guillera-Arroita G, Lahoz-Monfort JJ, Elith J, Gordon A et al (2015) Is my species distribution model fit for purpose? Matching data and models to applications. Glob Ecol Biogeogr 24:276–292. https://doi.org/10.1111/geb.12268
Hopkins ME (2011) Mantled howler (Alouatta palliata) arboreal pathway networks: relative impacts of resource availability and forest structure. Int J Primatol 32:238–258. https://doi.org/10.1007/s10764-010-9464-9
Houle A (1997) The role of phylogeny and behavioral competition in the evolution of coexistence among primates. Can J Zool 75:827–846. https://doi.org/10.1139/z97-106
Huey RB, Kearney MR, Krockenberger A et al (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos Trans R Soc B 367:1665–1679. https://doi.org/10.1098/rstb.2012.0005
IPCC (2021) Climate change 2021: the physical science basis. In: Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M, Leitzell K, Lonnoy E, Matthews JBR, Maycock TK, Waterfield T, Yelekçi O, Yu R, Zhou B (eds) Contribution of Working Group I to the Sixth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
IUCN, 2020 International Union for Conservation of Nature—Red List of Threatened Species IUCN. Available at https://www.iucnredlist.org. Accessed 26 June 2021.
Jalkanen J, Toivonen T, Moilanen A (2020) Identification of ecological networks for land-use planning with spatial conservation prioritization. Landsc Ecol 35:353–371. https://doi.org/10.1007/s10980-019-00950-4
Jiménez-Valverde A, Peterson AT, Soberón J et al (2011) Use of niche models in invasive species risk assessments. Biol Invasions 13:2785–2797. https://doi.org/10.1007/s10530-011-9963-4
Joetzjer E, Douville H, Delire C, Ciais P (2013) Present-day and future Amazonian precipitation in global climate models: CMIP5 versus CMIP3. Clim Dyn 41:2921–2936. https://doi.org/10.1007/s00382-012-1644-1
Lacher TE, Davidson AD, Fleming TH et al (2019) The functional roles of mammals in ecosystems. J Mammal 100:942–964. https://doi.org/10.1093/jmammal/gyy183
Lehtomäki J, Moilanen A (2013) Methods and workflow for spatial conservation prioritization using Zonation. Environ Model Softw 47:128–137. https://doi.org/10.1016/j.envsoft.2013.05.001
Leroy B, Delsol R, Hugueny B et al (2018) Without quality presence–absence data, discrimination metrics such as TSS can be misleading measures of model performance. J Biogeogr 45:1994–2002. https://doi.org/10.1111/jbi.13402
Loyola R, Machado N, Vila Nova D et al (2014) Áreas prioritárias para conservação e Uso Sustentável da flora brasileira ameaçada de extinção. Rio de Janeiro
McLean KA, Trainor AM, Asner GP et al (2016) Movement patterns of three arboreal primates in a Neotropical moist forest explained by LiDAR-estimated canopy structure. Landsc Ecol 31:1849–1862. https://doi.org/10.1007/s10980-016-0367-9
Mendes-Oliveira AC et al (2017) (2017) Oil palm monoculture induces drastic erosion of an Amazonian forest mammal fauna. PLoS ONE 12:e0187650. https://doi.org/10.1371/journal.pone.0187650
Meyer ALS (2017) Climate change, forests, and primate conservation. The international encyclopedia of primatology. American Cancer Society, Atlanta, pp 1–6
Milton K (1981) Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. Am Anthropol 83:534–548. https://doi.org/10.1525/aa.1981.83.3.02a00020
Moilanen A, Pouzols FM, Meller L et al (2014) Spatial conservation planning methods and software ZONATION. V. 4. User Manual, vol 4. University of Helsinki, Helsinki
Monteiro L, Machado N, Martins E et al (2017) Conservation priorities for the threatened flora of mountaintop grasslands in Brazil. Flora. https://doi.org/10.1016/j.flora.2017.03.007
Nascimento N, West TAP, Börner J, Ometto J (2019) What drives intensification of land use at agricultural frontiers in the brazilian Amazon? Evidence from a decision game. Forests 10:1–16. https://doi.org/10.3390/f10060464
Oliveira ACM, Ferrari SF (2000) Seed dispersal by black-handed tamarins, Saguinus midas niger (Callitrichinae, Primates): implications for the regeneration of degraded forest habitats in eastern Amazonia. J Trop Ecol 16:709–716. https://doi.org/10.1017/S0266467400001668
Pacifici M, Visconti P, Butchart SHM et al (2017) Species’ traits influenced their response to recent climate change. Nat Clim Chang 7:1–5. https://doi.org/10.1038/nclimate3223
Paglia AP et al (2012) Annotated checklist of Brazilian mammals. Occasional papers in Conservation Biology. Conservation International, Arlington
Pearson RG, Stanton JC, Shoemaker KT et al (2014) Life history and spatial traits predict extinction risk due to climate change. Nat Clim Chang 4:217–221. https://doi.org/10.1038/nclimate2113
Peres CA (2000) Territorial defense and the ecology of group movements in small-bodied neotropical primates. In: Boinski S, Garbe P (eds) On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 100–123
Peres CA, Emilio T, Schietti J et al (2016) Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests. Proc Natl Acad Sci 113:892–897. https://doi.org/10.1073/pnas.1516525113
Peterson AT (2006) Uses and requirements of ecological niche models and related distributional models. Biodivers Inform 3:59–72
Phillips SJ, Dudík M (2008) Modeling of species distribution with Maxent: new extensions and a comprehensive evalutation. Ecography (Cop) 31:161–175. https://doi.org/10.1111/j.2007.0906-7590.05203.x
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Modell 190:231–259. https://doi.org/10.1016/J.ECOLMODEL.2005.03.026
Pinheiro TF, Escada MIS, Valeriano DM et al (2016) Forest degradation associated with logging frontier expansion in the Amazon: the BR-163 region in southwestern Pará, Brazil. Earth Interact 20:1–26. https://doi.org/10.1175/EI-D-15-0016.1
Pinto MP, de Silva-Júnior JS, de Lima AA, Grelle CEV (2014) Multi-scales analysis of primate diversity and protected areas at a megadiverse region. PLoS One 9:e105205. https://doi.org/10.1371/journal.pone.0105205
Port-Carvalho M, Fialho MS, Alonso AC, Veiga LM (2015) Avaliação do Risco de Extinção de de Chiropotes satanas (Hoffmannsegg, 1807) no Brasil. In: Process. avaliação do risco extinção da fauna Bras. ICMBio. Available at http://www.icmbio.gov.br/portal/biodiversidade/fauna-brasileira/estado-de-conservacao/7328-mamiferos-chiropotes-satanas-cuxiu-preto.html. Accessed 2 Apr 2020
Pressey RL, Visconti P, Ferraro PJ (2015) Making parks make a difference: poor alignment of policy, planning and management with protected-area impact, and ways forward. Phil Trans R Soc B 370:20140280. https://doi.org/10.1098/rstb.2014.0280
PRODES INPE (2021) Monitoring deforestation of the Brazilian Amazon forest by satellite. TerraBrasilis (inpe.br). Accessed on July 2021
Rangel TF, Loyola RD (2012) Labeling ecological niche models. Nat Conserv 10:119–126. https://doi.org/10.4322/natcon.2012.030
Rezende GC, Sobral-Souza T, Culot L (2020) Integrating climate and landscape models to prioritize areas and conservation strategies for an endangered arboreal primate. Am J of Primatol 82(12):e23202. https://doi.org/10.1002/ajp.23202
Ribeiro BR, Sales LP, De Marco P, Loyola R (2016) Assessing mammal exposure to climate change in the Brazilian Amazon. PLoS ONE 11:e0165073. https://doi.org/10.1371/journal.pone.0165073
Ribeiro BR, Sales LP, Loyola R (2018) Strategies for mammal conservation under climate change in the Amazon. Biodivers Conserv 27:1943–1959. https://doi.org/10.1007/s10531-018-1518-x
Richardson VA, Peres CA (2016) Temporal decay in timber species composition and value in Amazonian logging concessions. PLoS ONE 11:e0159035. https://doi.org/10.1371/journal.pone.0159035
Rylands AB, Mittermeier RA, Bezerra BM et al (2013) Family Cebidae (Squirrel Monkeys and Capuchins). In: Mittermeier RA, Rylands AB, Wilson DE (eds) Handbook of the mammals of the world. Lynx Editions, Barcelona, pp 348–413
Sales LP, Ribeiro BR, Pires MM et al (2019) Recalculating route: dispersal constraints will drive the redistribution of Amazon primates in the Anthropocene. Ecography (Cop) 42:1789–1801. https://doi.org/10.1111/ecog.04499
Sarania B, Devi A, Kumar A et al (2016) Predictive distribution modeling and population status of the endangered Macaca munzala in Arunachal Pradesh, India. Am J Primatol 9999:1–10. https://doi.org/10.1002/ajp.22592
Schwitzer C, Mittermeier RA, Rylands AB et al (2019) Primates in Peril: the world’s 25 most endangered primates 2018–2020. IUCN SSC Primate Specialist Group, International Primatological Society, Global Wildlife Conservation, and Bristol Zoological Society, Washington, DC
Silva CA, Santilli G, Sano EE, Laneve G (2021) Fire occurrences and greenhouse gas emissions from deforestation in the Brazilian Amazon. Remote Sens 13:376. https://doi.org/10.3390/rs13030376
Silva Junior CHL, Pessôa ACM, Carvalho NS et al (2021) The Brazilian Amazon deforestation rate in 2020 is the greatest of the decade. Nat Ecol Evol 5:144–145. https://doi.org/10.1038/s41559-020-01368-x
Soares-Filho BS, Nepstad DC, Curran LM et al (2006) Modelling conservation in the Amazon basin. Nature 440:520–523. https://doi.org/10.1038/nature04389
Soares-Filho B, Moutinho P, Nepstad D et al (2010) Role of Brazilian Amazon protected areas in climate change mitigation. Proc Natl Acad Sci 107:10821–10826. https://doi.org/10.1073/pnas.0913048107
Soares-Filho BS, Lima LS, Hissa LB et al (2013) OTIMIZAGRO: Uma Plataforma Integrada de Modelagem de Uso e Mudanças no Uso da Terra para o Brasil. Centro de Sensoriamento Remoto, Universidade Federal de Minas Gerais, Belo Horizonte
Soares-Filho B, Rajão R, Macedo M et al (2014) Cracking Brazil’s forest code. Science 344:363–364. https://doi.org/10.1126/science.1246663
Soberon J, Nakamura M (2009) Niches and distributional areas: concepts, methods, and assumptions. Proc Natl Acad Sci 106:19644–19650. https://doi.org/10.1073/pnas.0901637106
Sobral FL, Jardim L, Lemes P et al (2014) Spatial conservation priorities for top predators reveal mismatches among taxonomic, phylogenetic and functional diversity. Nat Conserv 12:150–155. https://doi.org/10.1016/j.ncon.2014.09.008
Souza-Filho PWM, de Souza EB, Silva Júnior RO et al (2016) Four decades of land-cover, land-use and hydroclimatology changes in the Itacaiúnas River watershed, southeastern Amazon. J Environ Manag 167:175–184. https://doi.org/10.1016/j.jenvman.2015.11.039
Tax DMJ, Duin RPW (2004) Support vector data description. Mach Learn 54:45–66
Tyukavina A, Hansen MC, Potapov PV et al (2017) Types and rates of forest disturbance in Brazilian Legal Amazon, 2000–2013. Sci Adv 3:e1601047. https://doi.org/10.1126/sciadv.1601047
Vieira RRS, Pressey RL, Loyola R (2019) The residual nature of protected areas in Brazil. Biol Conserv 233:152–161. https://doi.org/10.1016/J.BIOCON.2019.02.010
Zaniewski AE, Lehmann A, Overton JM (2002) Predicting species spatial distributions using presence-only data: a case study of native New Zealand ferns. Ecol Model 157:261–280
Zhang L, Ameca EI, Cowlishaw G, Pettorelli N, Foden W, Mace GM (2019) Global assessment of primate vulnerability to extreme climatic events. Nat Clim Chang 9(7):554–561. https://doi.org/10.1038/s41558-019-0508-7
Acknowledgements
To the National Council for Scientific and Technological Development (CNPq) for the research productivity Grant (PQ2-310184/2020-7) for the corresponding author and master’s scholarship granted for the first author. We thank the reviewers for the excellent suggestions that certainly have improved the quality of this manuscript. We also thank Jesse Carlton for proofreading English.
Funding
The first author received a grant from the National Council for Scientific and Technological Development (CNPq) during her academic master’s degree, when she developed this research work. The corresponding author received a research productivity grant (PQ2-310184/2020-7) also from CNPq.
Author information
Authors and Affiliations
Contributions
ACM-O, LBS, RGF and RL contributed to the study, conception and design. Material preparation, data collection and analysis were performed by LBdS, RGF, BRR, DZ and GLO. The first draft of the manuscript was written by LBS and ACM-O and all authors commented on previous versions of the manuscript. GLO played an essential contribution for the second written version. All authors approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest.
Ethical approval
Not applicable.
Consent to participate
All authors agreed with the content and all gave explicit consent to submit this manuscript.
Additional information
Communicated by Clinton Jenkins.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
da Silva, L.B., Oliveira, G.L., Frederico, R.G. et al. How future climate change and deforestation can drastically affect the species of monkeys endemic to the eastern Amazon, and priorities for conservation. Biodivers Conserv 31, 971–988 (2022). https://doi.org/10.1007/s10531-022-02373-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-022-02373-1