Abstract
Ecological niche models (ENMs) are widely used tools for predicting species geographic distribution as a function of environmental variables. The inclusion of biotic factors in the predictor suite can significantly increase the predictive power of such models, leading to a model closer to the realized niche for the species under investigation. In this study, we provide evidence of niche overlap between gray woolly monkeys (Lagothrix cana) and black-faced black spider monkeys (Ateles chamek) based on locality and ecological data covering their complete geographic range in the Amazon forests of Brazil, Peru and Bolivia. We also estimate the potential distribution of L. cana using environmental predictors, and the distribution of A. chamek as a biotic factor. Finally, we quantified current and future habitat loss and areas under legal protection. We found that only 39% of the L. cana area of occupancy is under legal protection and that the species could potentially lose up to 58% of habitat in the next 30 years. We also show that the use of a closely-related species that has a more robust dataset can improve ENMs of poorly studied, rare and/or cryptic species. The framework developed here can be applied to a wide range of sympatric species if they share similar ecological requirements. Since our focal species are the most frugivorous primates in our study region and especially vulnerable to habitat loss, the identification of highly suitable areas for both taxa can help to protect other forest-dwelling species, reducing the rate of overall biodiversity loss.
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References
Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43:1223–1232
Anderson RP, Peterson AT, Gómez-Laverde M (2002) Using niche-based GIS modeling to test geographic predictions of competitive exclusion and competitive release in South American pocket mice. Oikos 98:3–16
Ayres J, Clutton-Brock T (1992) River boundaries and species range size in Amazonian primates. Am Nat 140:531–537
Boubli JP, Di Fiore A, Rylands AB, Wallace RB (2008) Lagothrix cana. The IUCN Red List of Threatened Species 2008. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T39925A10288721.en. Accessed 05 July 2019
Boubli JP, Ribas C, Alfaro JWL, Alfaro ME, da Silva MNF, Pinho GM, Farias IP (2015) Spatial and temporal patterns of diversification on the Amazon: a test of the riverine hypothesis for all diurnal primates of Rio Negro and Rio Branco in Brazil. Mol Phylogenetics Evol 82:400–412
Boubli JP, Byrne H, da Silva MN, Silva-Júnior J, Araújo RC, Bertuol F, Gonçalves J, de Melo FR, Rylands AB, Mittermeier RA (2019) On a new species of titi monkey (Primates: Plecturocebus Byrne et al., 2016), from Alta Floresta, southern Amazon. Brazil Mol Phylogenetics Evol 132:117–137
Brancalion PH, Garcia LC, Loyola R, Rodrigues RR, Pillar VD, Lewinsohn TM (2016) A critical analysis of the Native Vegetation Protection Law of Brazil (2012): updates and ongoing initiatives. Nat Conserv 14:1–15
Brando P, Soares-Filho B, Rodrigues L, Assunção A, Morton D, Tuchschneider D, Fernandes E, Macedo M, Oliveira U, Coe M (2020) The gathering firestorm in southern Amazonia. Sci Adv 6:1–9. https://doi.org/10.1126/sciadv.aay1632
Cardillo M, Warren LD (2016) Analysing patterns of spatial and niche overlap among species at multiple resolutions. Glob Ecol Biogeogr 25:951–963
Cavalcante T, Gusmão AC, Ferrari SF (2018) Unexpected diversity: the potential role of privately-owned forest remnants in the conservation of the primates of the highly-impacted Rondônia center of endemism, southwestern Brazilian Amazonia. Neotrop Primates 24:82–85
Chapman CA, Chapman LJ (1990) Dietary variability in primate populations. Primates 31:121–128
Coyne J, Orr H (2004) Speciation. Sinauer Associates, Sunderland
da Silva JMC, Rylands AB, da Fonseca GA (2005) The fate of the Amazonian areas of endemism. Conserv Biol 19:689–694
Di Fiore A, Campbell CJ (2007) The Atelines: variation in ecology, behavior and social organization. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, New York, pp 155–185
Di Fiore A, Link A, Dew JL (2008) Diets of wild spider monkeys. In: Campbell CJ (ed) Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 81–137
Di Fiore A, Chaves PB, Cornejo FM, Schmitt CA, Shanee S, Cortes-Ortiz L, Fagundes V, Roos C, Pacheco V (2014) The rise and fall of a genus: complete mtDNA genomes shed light on the phylogenetic position of yellow-tailed woolly monkeys, Lagothrix flavicauda, and on the evolutionary history of the family Atelidae (Primates: Platyrrhini). Mol Phylogenet Evol 82:495–510
Fearnside PM (1999) Biodiversity as an environmental service in Brazil's Amazonian forests: risks, value and conservation. Environ Conserv 26:305–321
Fooden J (1963) A revision of the woolly monkeys (genus Lagothrix). J Mammal 44:213–247
Gascon C, Bierregaard RO Jr, Laurance WF, Rankin-de-Merona J (2001) Deforestation and forest fragmentation in the Amazon. In: Bierregaard RO, Gascon C, Lovejoy TE, Mesquita R (eds) Lessons from Amazonia: the ecology and conservation of a fragmented forest. Yale University Press, New Haven, pp 22–30
Godsoe W, Harmon LJ (2012) How do species interactions affect species distribution models? Ecography 35:811–820
Gonzalez M, Clavijo L, Betancur J, Stevenson PR (2016) Fruits eaten by woolly monkeys (Lagothrix lagothricha) at local and regional scales. Primates 57:241–251
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
Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009
Hansen MC, Stehman SV, Potapov PV, Loveland TR, Townshend JR, DeFries RS, Pittman KW, Arunarwati B, Stolle F, Steininger MK (2008) Humid tropical forest clearing from 2000 to 2005 quantified by using multitemporal and multiresolution remotely sensed data. Proc Natl Acad Sci USA 105:9439–9444
Hawes JE, Peres CA (2014) Ecological correlates of trophic status and frugivory in neotropical primates. Oikos 123:365–377
Iwanaga S, Ferrari SF (2001) Party size and diet of syntopic atelids (Ateles chamek and Lagothrix cana) in southwestern Brazilian Amazonia. Folia Primatol 72:217–227
Iwanaga S, Ferrari SF (2002) Geographic distribution and abundance of woolly (Lagothrix cana) and spider (Ateles chamek) monkeys in southwestern Brazilian Amazonia. Am J Primatol 56:57–64
Jerusalinsky L, Talebi MG, Melo FR (2011) Plano de ação nacional para a conservação dos muriquis. Instituto Chico Mendes de Conservaçao da Biodiversidade ICMBio, BrasÃlia
Juffe-Bignoli D, MacSharry B, Bingham H, Deguignet M, Kingston N (2015) World Database on Protected Areas User Manual 1.0. UNEP-WCMC, Cambridge
Legendre P, Legendre LF (2012) Numerical ecology. Elsevier, Amsterdam
Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003
Lovejoy TE, Nobre C (2018) Amazon tipping point. Sci Adv 4:1–2. https://doi.org/10.1126/sciadv.aat2340
Michalski F, Peres CA, Lake IR (2008) Deforestation dynamics in a fragmented region of southern Amazonia: evaluation and future scenarios. Environ Conserv 35:93–103
Monjeau A (2010) Conservation crossroads and the role of hierarchy in the decision-making process. Nat Conserv 8:112–119
Muscarella R, Galante PJ, Soley-Guardia M, Boria RA, Kass JM, Uriarte M, Anderson RP (2014) ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods Ecol Evol 5:1198–1205
Nepstad D, Schwartzman S, Bamberger B, Santilli M, Ray D, Schlesinger P, Lefebvre P, Alencar A, Prinz E, Fiske G (2006) Inhibition of Amazon deforestation and fire by parks and indigenous lands. Conserv Biol 20:65–73
Nobre CA, Sampaio G, Borma LS, Castilla-Rubio JC, Silva JS, Cardoso M (2016) Land-use and climate change risks in the Amazon and the need of a novel sustainable development paradigm. Proc Natl Acad Sci USA 113:10759–10768
Oliveira U, Paglia AP, Brescovit AD, de Carvalho CJ, Silva DP, Rezende DT, Leite FSF, Batista JAN, Barbosa JPPP, Stehmann JR (2016) The strong influence of collection bias on biodiversity knowledge shortfalls of Brazilian terrestrial biodiversity. Divers Distrib 22:1232–1244
Peres CA (1990) Effects of hunting on western Amazonian primate communities. Biol Conserv 54:47–59
Peres CA (1991) Humboldt's woolly monkeys decimated by hunting in Amazonia. Oryx 25:89–95
Peres CA (1996) Use of space, spatial group structure, and foraging group size of gray woolly monkeys (Lagothrix lagotricha cana) at Urucu, Brazil. In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiation of Neotropical primates. Plenum Press, New York, pp 467–488
Peres CA, van Roosmalen M (2002) Primate frugivory in two species-rich neotropical forests: implications for the demography of large-seeded plants in overhunted areas. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford, pp 407–421
Peterson A, Soberón J, Sánchez-Cordero V (1999) Conservatism of ecological niches in evolutionary time. Science 285:1265–1267
Phillips SJ, DudÃk M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rabelo RM, Goncalves JR, Silva FE, Rocha DG, Canale GR, Bernardo CSS, Boubli JP (2018) Predicted distribution and habitat loss for the Endangered black-faced black spider monkey (Ateles chamek) in the Amazon. Oryx. https://doi.org/10.1017/S0030605318000522
Renner IW, Elith J, Baddeley A, Fithian W, Hastie T, Phillips SJ, Popovic G, Warton DI (2015) Point process models for presence-only analysis. Methods Ecol Evol 6:366–379
Robinson JG, Redford KH (1986) Body size, diet, and population density of Neotropical forest mammals. Am Nat 128:665–680
Schloss AL, Kicklighter DW, Kaduk J, Wittenberg U (1999) Comparing global models of terrestrial net primary productivity (NPP): comparison of NPP to climate and the Normalized Difference Vegetation Index (NDVI). Glob Chang Biol 5:25–34
Shekelle M, Salim A (2009) An acute conservation threat to two tarsier species in the Sangihe Island chain, North Sulawesi, Indonesia. Oryx 43:419–426
Soares-Filho BS, Nepstad DC, Curran LM, Cerqueira GC, Garcia RA, Ramos CA, Voll E, McDonald A, Lefebvre P, Schlesinger P (2006) Modelling conservation in the Amazon basin. Nature 440:520–523
Soares-Filho BS, Rajão R, Macedo M, Carneiro A, Costa W, Coe M, Rodrigues H, Alencar A (2014) Cracking Brazil's forest code. Science 344:363–364
Soberón J, Nakamura M (2009) Niches and distributional areas: concepts, methods, and assumptions. Proc Natl Acad Sci USA 106:19644–19650
Sombroek W (2000) Amazon landforms and soils in relation to biological diversity. Acta Amazon 30:81–100
Stevenson PR (2014) Potential determinants of the abundance of woolly monkeys in neotropical forests. In: Defler TR, Stevenson PR (eds) The woolly monkey: behavior, ecology, systematics, and captive research. Springer, New York, pp 207–226
Stevenson PR, Aldana AM (2008) Potential effects of Ateline extinction and forest fragmentation on plant diversity and composition in the Western Orinoco Basin, Colombia. Int J Primatol 29:365–377
Thorn JS, Nijman V, Smith D, Nekaris K (2009) Ecological niche modelling as a technique for assessing threats and setting conservation priorities for Asian slow lorises (Primates: Nycticebus). Divers Distrib 15:289–298
van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353–377
Warton DI, Renner IW, Ramp D (2013) Model-based control of observer bias for the analysis of presence-only data in ecology. PLoS ONE 8:e79168. https://doi.org/10.1371/journal.pone.0079168
Acknowledgements
The authors would like to express sincere thanks to the Handling Editor and two anonymous reviewers for comments that greatly improved the manuscript. Carlos Augusto Tuyama and Marco Rodrigo are acknowledged for providing valuable occurrence records for this study. José de Sousa e Silva Júnior is also acknowledged for help in specimen’s identification from Museu Paraense EmÃlio Goeldi. RMR thanks the Brazilian National Research Council (CNPq, #142352/2017-9). ASJ would like to thank to the Fundação Amazônia de Amparo a Estudos e Pesquisa do Pará (FAPESPA), and DF thanks the logistical support provided by the Interligação Elétrica do Madeira—IEMAD and by Group Biocev Smart Projects Services. JV and ASJ thank the Grant Agreement for Instituto de Desenvolvimento Sustentável Mamirauá (#5344) of the Gordon and Betty Moore Foundation. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de NÃvel Superior - Brasil (CAPES) - Finance Code 001.
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Contributions to the early planning of the study were made by TC, ACG and DF. TC, ASJ and RMR developed the overall research framework and designed the methodology. TC, MRZ, JV, DF, ACG, ODS, LF provided new species occurrence data. All data was gathered by TC, ASJ and RMR. RMR performed all the statistical models and data analyses. TC, ASJ, RMR and AAB led the writing of the manuscript. All authors gave final revision and approval for publication and are accountable for all aspects of the work.
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Communicated by Mukunda Dev Behera.
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Cavalcante, T., de Souza Jesus, A., Rabelo, R.M. et al. Niche overlap between two sympatric frugivorous Neotropical primates: improving ecological niche models using closely-related taxa. Biodivers Conserv 29, 2749–2763 (2020). https://doi.org/10.1007/s10531-020-01997-5
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DOI: https://doi.org/10.1007/s10531-020-01997-5
Keywords
- Ateles chamek
- Biotic interactions
- Lagothrix cana
- Potential geographic distribution
- Predicted habitat loss