Local vs landscape drivers of primate occupancy in a Brazilian fragmented region
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.
KeywordsConservation Wildlife habitat Detection Callicebus nigrifrons Callithrix penicillata
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.
Compliance with ethical standards
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.
- 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 13–28CrossRefGoogle Scholar
- Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer New York, New YorkGoogle Scholar
- 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 2.0Google Scholar
- 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 5:103–109Google Scholar
- 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 14:32–33Google Scholar
- 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 169–324Google Scholar
- 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 513–538CrossRefGoogle Scholar
- 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 215–222Google Scholar
- Mittermeier RA, Rylands AB, Wilson DE (2013) Handbook of the mammals of the world. Vol. 3. Primates. Lynx Edicions, Barcelona, SpainGoogle Scholar
- 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 123–138Google Scholar
- 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 91–120Google Scholar
- 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
- 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 10:1–50Google Scholar
- 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 58:1–6Google Scholar