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Occurrence and Conservation of the Vulnerable Titi Monkey Callicebus Melanochir in Fragmented Landscapes of the Atlantic Forest Hotspot

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Occurrence and Conservation of the Vulnerable Titi Monkey Callicebus Melanochir in Fragmented Landscapes of the Atlantic Forest Hotspot Occurrence and conservation of the Vulnerable titi monkey Callicebus melanochir in fragmented landscapes of the Atlantic Forest hotspot R ODRIGO C OSTA-ARAÚJO,ANDRÉ L UIS R EGOLIN,FELIPE M ARTELLO J OÃO P EDRO S OUZA-ALVES,TOMAS H RBEK and M ILTON C EZAR R IBEIRO Abstract Tropical forest hotspots have a high diversity of are scarce and therefore we require baseline data to support species but have lost . % of their original vegetation conservation actions and management in small forest cover and are characterized by a multitude of small and iso- fragments. lated fragments. Paradoxically, conservation actions in these Keywords Atlantic Forest, Brazil, Callicebus melanochir, areas are still mainly focused on protection of large tracts of degradation, ecological modelling, fragmentation, habitat forests, a strategy now infeasible because of the small area of loss, titi monkey forest remnants. Here we use the Vulnerable black-handed titi monkey Callicebus melanochir as a model to study the Supplementary material for this article is available at effects of habitat loss, fragmentation and degradation on doi.org/./S arboreal mammals and to provide insights for science- driven conservation in fragmented landscapes in tropical forest hotspots. We surveyed Atlantic Forest fragments in Introduction Bahia State, Brazil and assessed the effects of patch area, quality and visibility, and landscape connectivity on the iodiversity conservation is essential for the mainten- occurrence of our model species. Patch area was the single Bance of ecosystem services that guarantee survival of best model explaining species occurrence. Nonetheless, patch wildlife and the quality of human life. To achieve biodiver- quality and visibility, and landscape connectivity, positively sity conservation, stakeholders must work under a com- affect occurrence. In addition to patch area, patch quality, mon agenda to put in place actions to protect biodiversity patch visibility and landscape connectivity are useful for (Bisseleua et al., ; Tilman et al., ). Effective conser- predicting the occurrence of arboreal mammals in the vation decision-making is guided by scientific information fragments of tropical forest hotspots. We encourage the on species (Mace et al., ), the currency of conservation assessment of habitat quality (based on remotely sensed (Rylands & Mittermeier, ). Baseline data on species is vegetation indices) and habitat visibility (based on digital therefore paramount for biodiversity conservation. elevation models) to improve discoverability of arboreal Deforestation is recognized as the major threat to terres- mammal populations and selection of fragments for con- trial mammals (IUCN, ). Forest loss and fragmentation servation purposes across fragmented landscapes of tropical reduce the habitat of forest-dependent mammals and re- forest hotspots. Large remnants of tropical forest hotspots strict their populations to small, isolated patches (Fahrig, ), leading to population declines and local extinctions (Estrada et al., ). Accordingly, conservation science RODRIGO COSTA-ARAÚJO* (Corresponding author, orcid.org/0000-0002-6092- 4892) and TOMAS HRBEK ( orcid.org/0000-0003-3239-7068) Laboratório de has focused on the impacts of deforestation on species dis- Evolução e Genética Animal, Universidade Federal do Amazonas, Avenida tributions and abundance, and one of the main practical Rodrigo Octavio Jordão Ramos 3000, CEP 69077-000, Manaus, Amazonas, Brazil. E-mail [email protected] outcomes has been the protection of large tracts of forests (e.g. Soulé & Simberloff, ): the patch area paradigm in ANDRÉ LUIS REGOLIN† ( orcid.org/0000-0003-1820-8400) and MILTON CEZAR RIBEIRO ( orcid.org/0000-0002-4312-202X) Laboratório de Ecologia Espacial conservation. e Conservação, Universidade Estadual Paulista, Rio Claro, Brazil Large tracts of forests, however, are currently rare in trop- FELIPE MARTELLO ( orcid.org/0000-0003-1243-9750) Universidade Federal de ical forest hotspots (areas with a high proportion of endemic São Carlos, São Carlos, Brazil plants and extensive vegetation loss; Myers et al., )and JOÃO PEDRO SOUZA-ALVES‡ ( orcid.org/0000-0002-8517-1276) Programa de the majority of remnants are small (, ha) and embedded Pós-graduação em Biologia Animal, Universidade Federal de Pernambuco, Recife, Brazil in human-modified landscapes (Turner & Corlett, ). In *Also at: Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil the absence of funding for large-scale reforestation, conser- †Also at: Department of Fish, Wildlife, and Conservation Biology, Colorado vation of mammals in tropical forest hotspots thus needs to State University, Fort Collins, USA focus on a multitude of small forest fragments. The synergis- ‡Also at: Laboratório de Ecologia, Comportamento e Conservação, Universidade Federal de Pernambuco, Recife, Brazil tic effects of habitat loss, degradation and fragmentation on Received May . Revision requested July . arboreal mammals need to be examined, to inform strate- Accepted December . gies for population management and species conservation This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, Downloadeddistribution, from https://www.cambridge.org/core and reproduction in any medium,. IP address: provided 170.106.35.234 the original work, on is 02 properly Oct 2021 cited. at 02:55:34, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, Page 1 of 8 © The Author(s),. https://doi.org/10.1017/S0030605319001522 2021. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319001522 2 R. Costa-Araújo et al. FIG. 1 Hypothesized influence of patch area, quality and visibility, and landscape connectivity, on the occurrence of the arboreal black-handed titi monkey Callicebus melanochir in a fragmented Atlantic Forest landscape (Fig. ): (a) relative contribution of univariate (black bars) and compound models (black, patch area contribution; white, additive variable contribution) in explaining species’ occurrence; (b) expected response of the species occurrence to predictor variables in univariate models; (c) expected response of species occurrence synthesized for the three compound models having patch area and an additive variable. (Cassano et al., ; Gestich et al., ), especially in small in a transition zone between coastal wet forests and inland de- forest fragments. ciduous forests within the Atlantic Forest domain (Thomas, Such information is fundamental for facilitating conser- ). Anthropogenic land-use conversion since the s vation actions beyond the creation of protected areas and has transformed the originally continuous wet forests of the for understanding how forest degradation affects arboreal interior of southern Bahia into small fragments embedded mammals in fragmented landscapes, a relationship little in a matrix of pastures for cattle ranching (Coimbra-Filho studied (Mortelliti et al., ). For mammals that depend &Câmara,;Landau,). The study area is therefore on high quality forests, the availability of well conserved similar to other landscapes in the Atlantic Forest (Landau, habitats may be critical (Henle et al., ). ; Ribeiro et al., ) and other tropical forest hotspots Here we investigate the influence of patch and landscape (Turner & Corlett, ) regarding past processes and current structure on the occurrence of the coastal black-handed patterns of forest loss and fragmentation. titi monkey Callicebus melanochir in the Atlantic Forest hotspot (sensu Myers et al., ), using this species as a Methods model for arboreal mammals inhabiting fragmented land- scapes in tropical forest hotspots. Neotropical primates are Model species The coastal black-handed titi monkey strictly forest-dependent (Cowlishaw & Dunbar, ), dir- Callicebus melanochir (Plate ) is endemic to the Atlantic ectly and negatively affected by deforestation (Estrada et al., Forest of north-east Brazil (Culot et al., ). It is an arbor- ), and thus are appropriate models to study the impacts eal species that occasionally moves on the ground and can of forest reduction and fragmentation on the occurrence of disperse over short distances in non-forested areas (Mason, forest-dependent mammals. ; Souza-Alves et al., ), lives in groups comprising a We hypothesize that () patch area, quality and visibility, monogamous pair and offspring, and occupies home ranges and landscape connectivity, affect the probability of occur- of – ha (Müller, ; Heiduck, ). The species is ca- rence of our model species, with patch area having the stron- tegorized on the IUCN Red List as Vulnerable to extinction gest influence (Fig. a); () all four patch–landscape metrics as a result of habitat loss and fragmentation (Veiga et al., positively influence the probability of the species’ occur- ) but the response of individuals to such habitat mod- rence (Fig. b); and () compound models (patch area plus ifications has not been studied. each of the other metrics) will significantly increase model weights (Fig. c). Based on our findings, we discuss the usefulness of patch–landscape metrics in predicting the Field surveys During March –December ( field occurrence of titi monkeys and potentially other arboreal days) surveys of the titi monkey were carried out in frag- mammals in tropical forest hotspots and the application ments using playback censuses and interviews (following
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