Abstract
Understanding the drivers of species distributions in human-dominated landscapes is crucial for proposing sound conservation strategies. Primates are the most studied terrestrial vertebrate taxa, yet still, their response to forest loss and fragmentation widely varies among species. In this paper, we assessed the relative influence of local vs landscape features on occupancy of two primate species—the black-fronted titi monkey and the black-pencilled marmoset, in a Brazilian fragmented region. We created detection histories by performing repeated auditory surveys on 25 native vegetation patches. Then, we fitted occupancy models using habitat and GIS-based data as site covariates and weather conditions as detection covariates. We found that forest-like canopy elements are important for the titi monkey, a canopy-dependent species. Occupancy of marmoset, an opportunistic species, was also related to local elements, but in a lesser extent. In addition, we found that ignoring detectability in playback call surveys created a 20 % difference in occupancy estimates for the marmoset. We conclude that drivers of primate occupancy at the studied landscape rely mainly on local key habitat elements, so that on-ground conservation actions should not focus on habitat amount alone. Furthermore, we reiterate that primate researchers should explicitly account for imperfect detection to avoid substantial detectability bias.
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References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723
Anderson J, Cowlishaw G, Rowcliffe JM (2007) Effects of forest fragmentation on the abundance of Colobus angolensis palliatus in Kenya’s coastal forests. Int J Primatol 28:637–655. doi:10.1007/s10764-007-9143-7
Arroyo-Rodríguez V, Dias PAD (2010) Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 72:1–16. doi:10.1002/ajp.20753
Arroyo-Rodríguez V, Fahrig L (2014) Why is a landscape perspective important in studies of primates? Am J Primatol 76:901–909. doi:10.1002/ajp.22282
Arroyo-Rodríguez V, Mandujano S (2009) Conceptualization and measurement of habitat fragmentation from the primates’ perspective. Int J Primatol 30:497–514. doi:10.1007/s10764-009-9355-0
Arroyo-Rodríguez V, Moral EC, Mandujano S et al (2013) Assessing habitat fragmentation effects on primates: the importance of evaluating questions at the correct scale. In: Marsh LK, Chapman CA (eds) Primates in fragments: complexity and resilience, 2nd edn. Springer New York, New York, pp 13–28
Baker LR, Arnold TW, Olubode OS, Garshelis DL (2011) Considerations for using occupancy surveys to monitor forest primates: a case study with Sclater’s monkey (Cercopithecus sclateri). Popul Ecol 53:549–561. doi:10.1007/s10144-011-0274-5
Barros M, Alencar C, Tomaz C (2004) Differences in aerial and terrestrial visual scanning in captive black tufted-ear marmosets (Callithrix penicillata) exposed to a novel environment. Folia Primatol 75:85–92. doi:10.1159/000076266
Bélisle CJP (1992) Convergence theorems for a class of simulated annealing algorithms on R. J Appl Probab 29:885–895
Benchimol M, Peres CA (2013) Anthropogenic modulators of species-area relationships in Neotropical primates: a continental-scale analysis of fragmented forest landscapes. Divers Distrib 19:1339–1352. doi:10.1111/ddi.12111
Benchimol M, Peres CA (2014) Predicting primate local extinctions within “real-world” forest fragments: a pan-Neotropical analysis. Am J Primatol 76:289–302. doi:10.1002/ajp.22233
Broadbent EN, Asner GP, Keller M et al (2008) Forest fragmentation and edge effects from deforestation and selective logging in the Brazilian Amazon. Biol Conserv 141:1745–1757. doi:10.1016/j.biocon.2008.04.024
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer New York, New York
Caselli CB, Setz EZF (2011) Feeding ecology and activity pattern of black-fronted titi monkeys (Callicebus nigrifrons) in a semideciduous tropical forest of southern Brazil. Primates 52:351–359. doi:10.1007/s10329-011-0266-2
Chapman CA, Peres CA (2001) Primate conservation in the new millennium: the role of scientists. Evol Anthrop 10:16–33
Coimbra-Filho AF, Mittermeier RA (1976) Exudate-eating and tree-gouging in marmosets. Nature 262:630
Da Silva LG, Ribeiro MC, Hasui É et al (2015) Patch size, functional isolation, visibility and matrix permeability influences Neotropical primate occurrence within highly fragmented landscapes. PLoS One. doi:10.1371/journal.pone.0114025
Dacier A, de Luna AG, Fernandez-Duque E, Di Fiore A (2011) Estimating population density of Amazonian titi monkeys (Callicebus discolor) via playback point counts. Biotropica 43:135–140. doi:10.1111/j.1744-7429.2010.00749.x
Dantas A, Carvalho L, Ferreira E (2007) Classificação e tendências climáticas em Lavras, MG. Cienc Agrotecnol 31:1862–1866
Dooley HM, Judge DS, Schmitt LH (2013) Singing by male and female kloss gibbons (Hylobates klossii) in the Peleonan Forest, Siberut Island, Indonesia. Primates 54:39–48. doi:10.1007/s10329-012-0326-2
Fiske IJ, Chandler RB (2011) Unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. J Stat Softw 43:1–23
Frazer G, Canham C, Lertzman K (1999) Gap light analyzer (GLA): imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs. User’s manual and program documentation, Version 2.0
Gu W, Swihart RK (2004) Absent or undetected? Effects of non-detection of species occurrence on wildlife–habitat models. Biol Conserv 116:195–203. doi:10.1016/S0006-3207(03)00190-3
Guillera-Arroita G, Lahoz-Monfort JJ, Milner-Gulland EJ et al (2010) Monitoring and conservation of the critically endangered alaotran gentle lemur Hapalemur alaotrensis. Madagascar Conserv Dev 5:103–109
Guillera-Arroita G, Lahoz-Monfort JJ, MacKenzie DI et al (2014) Ignoring imperfect detection in biological surveys is dangerous: a response to “Fitting and interpreting occupancy models.”. PLoS One 9:e99571. doi:10.1371/journal.pone.0099571
Hines JE, Nichols JD, Karanth KK (2010) Occurrence and distribution of Indian primates. Biol Conserv 143:2891–2899. doi:10.1016/j.biocon.2010.02.011
Júnior TA, Zara FJ (2007) Black-tufted-ear marmoset Callithrix penicillata (Primates: Callithrichidae) following the army ant Labidus praedator (Formicidae: Ecitonina) in the Cerrado and the Atlantic Forest, Brazil. Neotrop Primates 14:32–33
Keane A, Hobinjatovo T, Razafimanahaka HJ et al (2012) The potential of occupancy modelling as a tool for monitoring wild primate populations. Anim Conserv 15:457–465. doi:10.1111/j.1469-1795.2012.00575.x
Kinzey WG (1997) Part II: synopsis of new world primates. In: Kinzey WG (ed) New world primates – ecology, evolution, and behavior. Walter de Gruyter Inc., New York, NY, p 169–324
Lahoz-Monfort JJ, Guillera-Arroita G, Wintle BA (2014) Imperfect detection impacts the performance of species distribution models. Glob Ecol Biogeogr 23:504–515. doi:10.1111/geb.12138
Lawler RR, Ford SM, Wright PC, Easley SP (2006) The locomotor behavior of Callicebus brunneus and Callicebus torquatus. Folia Primatol 77:228–239. doi:10.1159/000091232
MacKenzie DI, Bailey LL (2004) Assessing the fit of site-occupancy models. J Agric Biol Environ Stat 9:300–318. doi:10.1198/108571104X3361
MacKenzie DI, Nichols JD, Lachman GB et al (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83:2248–2255
Mandujano S, Escobedo-Morales LA, Palacios-Silva R et al (2006) A metapopulation approach to conserving the howler monkey in a highly fragmented landscape in Los Tuxtlas, Mexico. In: Estrada A, Garber PA, Pavelka MSM, Luecke L (eds) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. Springer New York, New York, pp 513–538
Marsh LK, Chapman CA, Arroyo-Rodríguez V et al (2013) Primates in fragments 10 years later: once and future goals. In: Marsh LK, Chapman C (eds) Primates in fragments: complexity and resilience, 2nd edn. Springer New York, New York, pp 505–525
Mazerolle MJ (2015) Package “AICcmodavg”: model selection and multimodel inference based on (Q)AIC(c). www.cran.r-project.org/web/packages/AICcmodavg. Accessed 23 Aug 2015
Melo FR, Mendes SL (2000) Emissão de gritos longos por grupos de Callicebus nigrifrons e suas reações a playbacks. In: Alonso C, Languth A (eds) A primatologia no brasil. SBPr e Editora Universitária, João Pessoa, pp 215–222
Miller CT, Beck K, Meade B, Wang X (2009) Antiphonal call timing in marmosets is behaviorally significant: interactive playback experiments. J Comp Physiol A 195:783–789. doi:10.1007/s00359-009-0456-1
Mittermeier RA, Rylands AB, Wilson DE (2013) Handbook of the mammals of the world. Vol. 3. Primates. Lynx Edicions, Barcelona, Spain
Mustoe AC, Jensen HA, French JA (2012) Describing ovarian cycles, pregnancy characteristics, and the use of contraception in female white-faced marmosets, Callithrix geoffroyi. Am J Primatol 74:1044–1053. doi:10.1002/ajp.22058
Nichols JD, Bailey LL, O’Connell AF Jr et al (2008) Multi-scale occupancy estimation and modelling using multiple detection methods. J Appl Ecol 45:1321–1329. doi:10.1111/j.1365-2664.2008.01509.x
Norconk MA (2007) Sakis, uakaris and titi monkeys—behavioral diversity in a radiation of primate seed predators. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger MBS (eds) Primates in perspective. Oxford University Press, New York, pp 123–138
Norris D, Rocha-Mendes F, Marques R et al (2011) Density and spatial distribution of buffy-tufted-ear marmosets (Callithrix aurita) in a continuous Atlantic forest. Int J Primatol 32:811–829. doi:10.1007/s10764-011-9503-1
Oliveira-Filho AAT, Fontes MAL (2000) Patterns of floristic differentiation among Atlantic forests in Southeastern Brazil and the influence of climate. Biotropica 32:793–810
Oliveira-Filho A, Ratter J (2002) Vegetation physiognomies and woody flora of the Cerrado biome. In: Oliveira P, Marquis R (eds) The Cerrados of Brazil: ecology and natural history of a Neotropical savanna. Columbia University Press, New York, pp 91–120
Oliveira-Filho AT, Vilela EA, Gavilanes ML, Carvalho DA (1994) Comparison of the woody flora and soils of six areas of montane semideciduous forest in southern Minas Gerais. Edinbg J Bot 51:355–389
Passamani M, Rylands AB (2000) Feeding behavior of Geoffroy’s marmoset (Callithrix geoffroyi) in an Atlantic forest fragment of south-eastern Brazil. Primates 41:27–38
Pontin AJ (1962) A method for quick comparison of the total solar radiation incident on different microhabitats. Ecology 43:740. doi:10.2307/1933468
Pozo-Montuy G, Serio-Silva JC, Bonilla-Sánchez YM (2011) Influence of the landscape matrix on the abundance of arboreal primates in fragmented landscapes. Primates 52:139–147. doi:10.1007/s10329-010-0231-5
Ribeiro MC, Metzger JP, Martensen AC et al (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153. doi:10.1016/j.biocon.2009.02.021
Robinson JG (1981) Vocal regulation of inter- and intragroup spacing during boundary encounters in the titi monkey, Callicebus moloch. Primates 22:161–172
Ryan MJ, Kime NM (2003) Selection on long-distance acoustic signals. In: Simmons AM, Fay RR, Popper AN (eds) Acoustic communication. Springer, New York, pp 225–274
Rylands AB, Anzenberger G (2012) Introduction: new world primates. Int Zoo Yearb 46:4–10. doi:10.1111/j.1748-1090.2012.00182.x
Rylands AB, Mendes SL (2008) Callithrix penicillata. The IUCN red list of threatened species. Version 2015.3. www.iucnredlist.org. Accessed 23 Aug 2015
Rylands AB, Coimbra-Filho AF, Mittermeier RA (2009) The systematics and distributions of the marmosets (Callithrix, Callibella, Cebuella, and Mico) and callimico (Callimico) (Callithrichidae, Primates). In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: the Marmoset/Callimico radiation. Springer Science + Business Media, p 25–61. doi:10.1007/978-1-4419-0293-1_2
Schuster C, Förster M, Kleinschmit B (2012) Testing the red edge channel for improving land-use classifications based on high-resolution multi-spectral satellite data. Int J Remote Sens 33:5583–5599. doi:10.1080/01431161.2012.666812
Sharma N, Madhusudan MD, Sinha A (2014) Local and landscape correlates of primate distribution and persistence in the remnant lowland rainforests of the upper Brahmaputra Valley, Northeastern India. Conserv Biol 28:95–106. doi:10.1111/cobi.12159
Sussman RW, Kinzey WG (1984) The ecological role of the callitrichidae: a review. Am J Phys Anthropol 64:419–449. doi:10.1002/ajpa.1330640407
Tabarelli M, Aguiar AV, Ribeiro MC et al (2010) Prospects for biodiversity conservation in the Atlantic Forest: lessons from aging human-modified landscapes. Biol Conserv 143:2328–2340. doi:10.1016/j.biocon.2010.02.005
Tardif S, Smucny D (2003) Reproduction in captive common marmosets (Callithrix jacchus). Comp Med 53:364–368
Trevelin LC, Port-carvalho M, Silveira M et al (2007) Abundance, habitat use and diet of Callicebus nigrifrons Spix (Primates, Pitheciidae) in Cantareira State Park, São Paulo, Brazil. Rev Bras Zool 24:1071–1077
Umapathy G (2013) Research in habitat fragmentation: are we moving in the right direction? J Primatol. doi:10.4172/2167-6801.1000e119
Van Roosmalen MGM, Van Roosmalen T, Mittermeier RA (2002) A taxonomic review of the titi monkeys, genus Callicebus Thomas, 1903, with the description of two new species, Callicebus bernhardi and Callicebus stephennashi, from Brazilian Amazonia. Neotrop Primates 10:1–50
Veiga LM, Kierulff CM, de Oliveira MM, Mendes SL (2008) Callicebus nigrifrons. The IUCN red list of threatened species. Version 2015.3. www.iucnredlist.org. Accessed 23 Aug 2015
Vilela AA, Del-claro K (2011) Feeding behavior of the black-tufted-ear marmoset (Callithrix penicillata) (Primate, Callitrichidae) in a tropical Cerrado savanna. Sociobiology 58:1–6
Villela DM, Nascimento MT, Aragao LEOC, da Gama DM (2006) Effect of selective logging on forest structure and nutrient cycling in a seasonally dry Brazilian Atlantic forest. J Biogeogr 33:506–516. doi:10.1111/j.1365-2699.2005.01453.x
Wiley RH, Richards DG (1978) Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behav Ecol Sociobiol 3:69–94. doi:10.1007/BF00300047
Wintle BA, McCarthy MA, Parris KM, Burgman MA (2004) Precision and bias of methods for estimating point survey detection probabilities. Ecol Appl 14:703–712
Acknowledgments
We are sincerely thankful to all landowners who allowed us to work in their rural properties. Special thanks are given to Renan Macedo, Rayssa Faria Pedroso, Tiago Fogaça de Carvalho, and Ismael Aparecido da Silva for their valuable help in fieldwork. We also thank two anonymous referees for their valuable suggestions to the manuscript.
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Data collection was conducted under approval of the Brazilian Institute of the Environment (IBAMA process number 14083–1) and follows the Principles for the Ethical Treatment of Non-Human Primates of the American Society of Primatologists. Co-authors state their participation and agree with the resubmission in Mammal Research. The first author is financed by the Brazilian Federal Agency for Evaluation of Graduate Education (CAPES number 00.889.834/0001-08). The authors also declare that they have no conflict of interest.
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Communicated by: Emerson M. Vieira
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Sales, L.P., Hayward, M.W. & Passamani, M. Local vs landscape drivers of primate occupancy in a Brazilian fragmented region. Mamm Res 61, 73–82 (2016). https://doi.org/10.1007/s13364-015-0252-y
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DOI: https://doi.org/10.1007/s13364-015-0252-y