Fragment shape and size, landscape permeability and fragmentation level as predictors of primate occupancy in a region of Brazilian Cerrado

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Human activities and increasing rates of urbanization have led to the progressive degradation of the environment and the loss of natural vegetation, which converts continuous forest cover into a fragmented landscape dominated by small and isolated patches of forest (Soulsbury & White, 2015; Goudie, 2018). This process provokes ecological disturbance at different habitat scales (Lyra-Jorge, Ribeiro, Ciocheti, Tambosi, & Pivello, 2010). At a local scale, patches may be impoverished, for example, through edge effects, the simplification of the fauna, the loss or local extinction of plant species (Tabarelli, Silva, & Gascon, 2004) or also the homogenization of the composition of the vegetation (Lôbo, Leão, Melo, Santos, & Tabarelli, 2011). At the patch scale, habitat patches may become progressively smaller and more isolated, while at a landscape scale, they may disappear altogether (Fahrig, 2003). The occupation of these forest patches by animal populations will depend on the dynamics of the exploitation of the resources available in the patches themselves and the surrounding matrix (Santos, Chiarello, Ribeiro, Ribeiro, & Paglia, 2016), which will influence the resilience of the populations or their susceptibility to extinction (Arroyo-Rodríguez et al., 2017; Borges-Matos, Aragón, Silva, Fortin, & Magnusson, 2016; Brady, McAlpine, Possingham, Miller, & Baxter, 2011). Ultimately, the socioecology of the species may also influence patch occupation patterns. Depending on the social system and dispersal dynamics of the species, individuals may either disperse systematically from their natal group or disperse secondarily between groups (Izar et al., 2012; Jack & Fedigan, 2004).

Most primate populations are either already undergoing the synergistic effects of the process of landscape fragmentation or will do so in the not-too-distant future (Estrada et al., 2017). These impacts can modify the distribution of the primate populations within the landscape, and are influenced by both the composition of the landscape matrix and the vertical structure of the vegetation in the patches (Arroyo-Rodríguez & Dias, 2010; Boyle & Smith, 2010; Mbora & Meikle, 2004). A number of studies have highlighted the importance of features of the vegetation structure, such as basal area, and canopy cover and height for the distribution and abundance of primate populations (Arroyo-Rodríguez & Mandujano, 2006). The drivers of primate occupancy in any landscape may depend on key elements of the local habitat, such as the amount of canopy, which is especially important to forest-dwelling species, as observed by Sales, Hayward, and Passamani (2016) in Callicebus nigrifrons. Anzures-Dadda and Manson (2007) also found a positive correlation between the presence of Alouatta palliata and the abundance and size of patches, canopy height, and abundance of corridors. However, occupancy is not determined solely by the attributes of the patches themselves, but also by the characteristics of the surrounding matrix (Anderson, Rowcliffe, & Cowlishaw, 2007; Hasui et al., 2017), so the presence of primate populations appears to depend on the overall configuration of the landscape (Arroyo-Rodríguez & Fahrig, 2014). For example, Sales et al. (2015) assessed the effects of forest patch size and connectivity on changes in occupancy, extinction and colonization rates following environmental change over time in two native Brazilian primates. These authors found that the black-tufted marmoset (Callithrix penicillata) presented a rapid response to habitat change, given that its occupation of the landscape is best explained by its current attributes, especially connectivity, resulting in an equilibrium with the present-day landscape. On the other hand, the response of the black-fronted titi monkey (Callicebus nigrifrons), which is dependent on the forest canopy, suffered a time-lag effect, because current occupation patterns are related to the past attributes of the landscape (especially fragment size).

The structure and composition of the landscape matrix can also influence the dynamics of primate populations both within and among forest patches (Benchimol & Peres, 2013). Habitat loss limits the availability of resources in patches (Estrada & Coates-Estrada, 1996), and may stimulate the exploration of the matrix (Mandujano, Escobedo-Morales, & Palacios-Silva, 2004) by animals searching for resources and moving to new patches (Asensio, Arroyo‐Rodríguez, Dunn, & Cristóbal‐Azkarate, 2009). Thus, the exploitation of resources from the matrix may mitigate the effects of habitat loss and relativize the structural connectivity of the landscape, making it more functional (Pardini, Souza, Braga-Neto, & Metzger, 2005; Ricketts, 2001). The success of primate populations in a fragmented landscape may thus depend on the complex interaction of a range of factors at different spatial scales, including patch size, quality, and structure, the composition of the matrix, and the ability of the animals to exploit the patches (Arroyo-Rodríguez, Cuesta-del-Moral, Mandujano, Chapman, Reyna-Hurtado, & Fahrig, 2013a; Carretero-Pinzón, Defler, McAlpine, & Rhodes, 2017; Silva, Ribeiro, Hasui, Costa, & Cunha, 2015).

It is imperative to understand how different primate species respond to changes in the landscapes they occupy because the species–landscape relationship depends strongly on landscape variables and the regional context (Galán-Acedo, Arroyo‐Rodríguez, Estrada, & Ramos‐Fernández, 2018). The populations of coexisting primate species, in particular, constitute a challenge for the determination of the environmental predictors of their potential success or failure in a fragmented landscape (Arroyo-Rodríguez & Dias, 2010; Peres & Janson, 1999). It is also important to identify the specific factors and the most appropriate spatial scale of analysis applicable to each case (Arroyo-Rodríguez et al., 2013a; Arroyo-Rodríguez, González-Perez, Garmendia, Solà, & Estrada, 2013b; Arroyo-Rodríguez & Fahrig, 2014). The rural-urban landscape gradient is an opportune scenario, given that the intensity of the matrix has negative effects on the richness and abundance of mammals (Brady, McAlpine, Miller, Possingham, & Baxter, 2009; Brady et al., 2011; Estrada, Raboy, & Oliveira, 2012). The understanding of the factors that determine the patch occupancy permits the comprehension of the environmental demands of the primates found in fragmented landscapes and the more systematic identification of the local, patch and landscape scale attributes that are of the highest priority for the development of conservation strategies (Carretero-Pinzón et al., 2017; Pozo-Montuy, Serio-Silva, & Bonilla-Sánchez, 2011). This approach should provide more reliable guidelines for the development of effective conservation measures that include both the species themselves and specific features of the environment, to ensure the survival of populations over the medium to long term (Chapman & Peres, 2001; Marsh et al., 2003).

The syntopic primates of the Brazilian central Cerrado coexist in forest patches within a fragmented landscape, providing an appropriate context for the assessment of the issues on patch occupancy outlined above. Although little is known about the relationships established between these primates and the landscape and patch characteristics, we can propose a number of predictions on the characteristics of the behavioral ecology of these species. As a generalist species, the marmosets would be less sensitive to the landscape and local degradation and would not be affected by the anthropogenic matrix (Sales et al., 2015; Secco, Grilo, & Bager, 2018). As the capuchin monkeys live in large groups, they would need larger patches with a well-preserved structure (Fragaszy, Visalberghi, & Fedigan, 2004). Howler monkeys appear to tolerate small patches (Bicca-Marques, 2003), but because they are folivorous-frugivorous, they would also need well-structured patches. All three species would likely benefit from the greater proximity between the patches in the landscape, and greater permeability, which usually favors movements within the landscape (Martensen, Pimentel, & Metzger, 2008). Our general hypothesis is that habitat loss and fragmentation will affect differentially the occupation of patches by the different primate species. In the present study, we investigated the effects of local, patch, and landscape scale attributes on the occupancy of forests by the black-and-gold howler monkey (Alouatta caraya), the brown capuchin (Sapajus libidinosus), and the black-tufted marmoset (Callithrix penicillata) within a rural-urban gradient. We analyzed variables including vegetation structure (basal area, tree density), patch size and shape, and landscape composition/configuration (total area of forest, number of patches, matrix permeability, and patch proximity). We aimed to identify the habitat attributes and the spatial scale most relevant to the conservation of these primate populations.

We recorded the presence of all three primate species within the study landscape. The most common species was C. penicillata, which was recorded in 91% (n = 20) of the focal patches, followed by S. libidinosus and A. caraya, which were both found in 45% of the patches (n = 10) patches (Table 2). The analyses indicated that the patch (m2) and landscape (m3) models provided the most parsimonious explanation for the occupation of patches by A. caraya and S. libidinosus (Table 3; Table 4). In the case of occupancy by S. libidinosus, patch size and the permeability of the landscape matrix were the most important metrics, both having a positive effect. The occupancy of A. caraya was positively related to the number of forest patches in the landscape and to the focal patch shape, and negatively related to the amount of forest in the landscape. The focal patch shape and the amount of forest in the landscape had a marginally relationship (p value approximately 0.05). By contrast, none of the predictors had any clear influence on patch occupation by C. penicillata, which was presumably due to the widespread distribution of this species within the landscape.

Table 2
Area, Brazilian Cerrado phytophysiognomies, and primate occurrence records of the focal forest patches in the city of Goiânia, Goiás state, Brazil.

Table 3.
Models used to evaluate the predictability of forest patch occupancy by Alouatta caraya, Sapajus libidinosus and Callithrix penicillata in the landscape of Goiânia, Brazil, based on local, patch and landscape attributes. The best models are highlighted in bold types, and R² is only presented for the best models.

The three primate species presented distinct levels of occupancy within the study landscape in the Brazilian Cerrado. Howlers and capuchins were both encountered in less than half of the focal patches, whereas the marmosets were found in almost all of them. Within the rural-urban landscape gradient, the howlers and capuchin monkeys may have a more restricted occupation of the landscape in comparison with the marmosets, whose ample distribution and ecological plasticity has been documented in other urban centers (Duarte & Young, 2011; Goulart, Teixeira, & Young, 2010) and in remnants of the original forest (Hilário & Ferrari, 2015). This may indicate a significant difference in the landscape requirements of howlers and capuchins in the anthropogenic matrix of the Brazilian Cerrado, in comparison with the marmosets (Hoffman & O’Riain, 2012).

Table 4
Mean, standard deviation (SD), minimum (Min), and maximum (Max) values of local, patch and landscape attributes among the focal forest patches in the city of Goiânia, Goiás state, Brazil.

Specific patch metrics and landscape attributes influenced patch occupancy by howlers and capuchins. Patch size and matrix permeability were important predictors of capuchin occupancy. Under natural conditions, capuchins live in large groups (12 to 27 individuals), with relatively large home ranges, of 161 ha, on average ( Fragaszy et al., 2004). Where habitats have been fragmented and impoverished, larger patches may increase the potential for the occurrence and persistence of capuchin populations (Carretero-Pinzón et al., 2017; Mota, Leite, & Martins, 2018). Given the ability of capuchins to cross open areas in the landscape matrix (T. O. Grande, personal observation), in addition, a more permeable matrix would also facilitate access to adjacent forest patches, amplifying the range of resources available to a resident capuchin group (Hendges, Melo, Gonçalves, Cerezer, & Cáceres, 2017; Silva et al., 2015). In this scenario, dynamic capuchin groups would be able to exploit more effectively resources distributed heterogeneously or seasonally within the fragmented landscape.

Capuchins are likely to be prevalent and persist over the long term in more rural landscapes in comparison with less hospitable urban landscapes, given the greater potential for dispersal among patches and groups (Estrada et al., 2012), as well as their considerable behavioral and ecological flexibility. In an analysis of the similarity of mammal communities among isolated forest patches in the fragmented landscape of the southwestern Cerrado, medium- and large-sized mammals (including S. libidinosus) were able to move between patches regardless of the size, degree of isolation or vegetation structure of these forest remnants (Cáceres, Nápoli, Casella, & Hannibal., 2010). In this case, movement would be facilitated by the permeability of the pasture matrix. A number of other studies (Michalski & Peres, 2005; Sorensen & Fedigan, 2000) have also recorded other species of capuchins moving over large distances in fragmented landscapes, often along unconnected corridors in both grassland and degraded forest habitats.

For the howlers, patch shape and the number and area of forest patches appear to be the principal predictors of occupancy. The more irregular its shape, the greater the probability of the occurrence of howlers in the patch. In the study region, fragments of gallery forest tend to be the most irregularly shaped. Howlers may be associated with gallery forests due to both the resources they offer and their connectivity, given that the anthropogenic matrix tends to be less permeable (Arroyo-Rodríguez et al., 2013b). Howlers were prevalent in areas with a high level of fragmentation, but a smaller total area of forest. This may reflect the tolerance of these monkeys to habitat loss and fragmentation, which typically results in a reduction of the area of forest and an increase in the number of patches (Fahrig, 2003). While habitat fragmentation may limit the dispersal capacity of A. caraya (Oklander, Kowalewski, & Corach, 2010; Oklander & Corach, 2013), a larger number of more closely-spaced patches may facilitate movements by providing stepping-stones of habitat (Clarke, Collins, & Zucker, 2002; Pozo-Montuy et al., 2011), especially considering the ability of the howlers to move over the ground (Serio-Silva, Ramírez-Julián, Eppley, & Chapman, 2019). It is important to note, however, that this apparent tolerance of habitat loss and fragmentation may actually represent the delayed or time-lagged extinction of populations (Michalski & Peres, 2005; Sales et al., 2015). While howler populations may persist in the short term, then, even in disturbed patches, both occupancy and overall density may decline over the medium to long term (Zunino, Kowalewski, Oklander, & González, 2007).

In contrast with the other two species, no significant influence of any predictor was found on patch occupancy by C. penicillata. In patches of native vegetation of the Brazilian Atlantic forest and Cerrado, Sales et al. (2016) also observed a high occupancy level for marmosets, which did not exhibit a clear relationship with any predictors at either a local or landscape scale. This might be accounted for by the considerable ecological flexibility of the marmosets of this genus (Abreu, De la Fuente, Schiel, & Souto, 2016;Amora, Mendes, & Ferrari, 2013), which allows them to colonize successfully both open and disturbed forests. Black-tufted marmosets are highly opportunistic, and may maintain a high reproductive output, even in extremely degraded habits, which contributes to their adaptability to urban development (Vilela & Del-Claro, 2011). The ability of these marmosets to survive in urban habitats may be determined, in part, by their capacity to exploit readily-available resources, such as cultivated fruit trees and garbage (Goulart et al., 2010; Miranda & Faria, 2001; Secco et al., 2018; Vilela & Faria, 2002). This species also has a considerable dispersal capacity, being able to move short distance across the ground between forest patches or even individual trees, which may act as stepping-stones within the urban matrix.

The local scale attributes did not influence the probability of occupancy of any of the primate species. All three species used features of the anthropogenic matrix, such as gardens, orchards, and plantations, to obtain resources or move between patches (T. O. Grande, personal observation; Arroyo-Rodríguez et al., 2013b; Pozo-Montuy et al., 2011), which may contribute to their persistence in patches of varying structure and conditions (Cáceres et al., 2010; Michalski & Peres, 2005). The plant diversity or the variation in the availability of food sources in the rural-urban landscape (Arroyo-Rodríguez & Dias, 2010) may also contribute to patch occupancy in these primates (Boyle & Smith, 2010; Cristóbal-Azkarate, Veà, Asensio, & Rodríguez‐Luna, 2005; Zunino, González, Kowalewski, & Bravo, 2001). In this case, a more systematic analysis of the availability of resources in both the forest patches and the surrounding matrix would be essential for a more definitive understanding of the determinants of habitat use by primates in this landscape.

Restoring landscapes to compensate for habitat loss and fragmentation is a major challenge for conservation planning. A priori, conservation measures should focus on the current conditions that most favor the target species or group of organisms. While all the species analyzed in the present study are considered to be tolerant to habitat disturbance (Lessa, Alves, Geise, & Barreto, 2012), we demonstrated that certain specific features of the landscape may be potentially more important for the conservation of this group in the context of the rural-urban habitat gradient of the central Brazilian Cerrado. The results of the present study indicate clearly that the preservation of remaining patches, both large and small, and in particular the gallery forests, as well as ensuring matrix permeability, are priority measures for the conservation of all three primate species. If habitat loss and fragmentation continue at present rates, however, the persistence of populations in local patches will certainly be challenged (Arroyo-Rodríguez & Dias, 2010; Hendges et al., 2017).

The preservation of large forest patches would better safeguard wildlife habitat, and could eventually support reintroduction projects (Arroyo-Rodríguez & Mandujano, 2009; Chiarello, 2000), whereas smaller ones can play an important role as stepping stones, increasing landscape connectivity (Pardini et al., 2005; Tulloch, Barnes, Ringma, Fuller, & Watson, 2016). It will also be important to maintain legally-sanctioned areas, including obligatory areas of permanent preservation, such as gallery forests, which will be fundamental to the persistence of mammals associated with riparian forest, such as A. caraya, as shown in the present study (Galetti et al., 2010; Johnson, Saraiva & Coelho, 1999). Maintaining or even increasing the permeability of the matrix, which could be achieved by the planting of hedgerows or even isolated trees (Estrada et al., 2006), would contribute to the movement capacity and foraging potential of the species within the landscape (Arroyo-Rodríguez et al., 2013b; Arroyo‐Rodríguez et al., 2017; Kennedy, Zipkin & Marra, 2017). Our findings contribute to the development of landscape-specific management strategies that will guarantee the conservation of primate populations facing high levels of habitat fragmentation.

This study assessed the effects of local, patch, and landscape scale attributes on the occupancy of forests patches by the Alouatta caraya, Sapajus libidinosus, and Callithrix penicillata, in a fragmented landscape within the Cerrado, Brazil. The main results were that the occupancy of the A. caraya was influenced by the shape of the focal patches, the amount of forest and fragmentation level of the landscape. In S. libidinosus, focal patch size and the permeability of the matrix were the principal determinants of the occupation, while for the C. penicillata the occupancy was not determined by none of the predictors evaluated.

This research was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). We thank the Graduate Program in Ecology and Evolution of the Universidade Federal de Goiás, Brazil. R.M. Alencar, P.P. Ribeiro, U.Q. Costa, K.C. Neves, S.G.F. Neto, V.H.I. Ascoli and I.X. Barbosa provided essential assistance for data collection in the field. The Goiânia Municipal Environment Agency (AMMA) and the Secretariat of the Environment and Water Resources (SEMARH) of the state of Goiás authorized data collection in the public forest patches. We are also grateful for the cooperation of the residents of Goiânia who agreed to participate in the interviews.