We performed line transect surveys in two fishbone human settlements (defined as clearings cut through forests in a fishbone pattern, extending along secondary roads from a main road) in different vegetation types, as well as in one protected area. A total of 410 sightings of eight primate species were recorded in the three study areas. The mean total primate abundance was 3.28 groups/10 km walked, and there were significant differences between areas with different plant physiognomies. The abundance of the larger primate species Alouatta macconnelli and Ateles paniscus (Atelidae) was higher in the dense ombrophilous forests of the Entre Rios human settlement, whereas those of all the other species were higher in the forest mosaics of the Novo Paraíso human settlement and Viruá National Park. The habitat generalist Sapajus apella presented the highest abundances in all the areas. No significant differences were detected in relative biomass between study areas. Additionally, no significant differences were detected in the overall abundances or relative biomasses of the hunted species (Sapajus apella, Alouatta macconnelli, Ateles paniscus, and Chiropotes chiropotes) between study areas. Human impact has been recognized as shaping primate assemblages. However, in this study, primates were not part of the dietary repertoire of the non-Amazonian immigrants inhabiting the fishbone human settlements. Thus, although the primate assemblages varied considerably at the regional and local level, they were shaped by habitat heterogeneity, which allowed the competing species to coexist through habitat segregation.
Studies on primates in South America, India, and Africa (Hill et al., 1997; Plumptre & Johns, 2001; Naughton-Treves et al., 2003; Rist et al., 2009; Chapman et al., 2010; Levi et al., 2011; Pillay et al., 2011; Rovero et al., 2012) have shown that human impact can shape primate assemblages. It can cause the decline or even regional or local extinction, especially of larger-bodied species such as Ateles spp. (Bennett et al., 2001; Thoisy et al., 2005; Palminteri et al., 2011). In contrast, human activity may promote an increase in the abundance of the smaller, ‘weedy’ species, such as Saguinus spp., that can successfully use various forms of human-disturbed habitats (Naughton-Treves et al., 2003).
In central and western Brazilian Amazonia human disturbance, mainly through hunting, has been shown to be the main determinant of primate assemblage structure (Branch, 1983; Peres, 1997, 2000; Peres & Dolman, 2000), although in some cases in central Amazonia forest heterogeneity can be the most important variable shaping the assemblage, even if the area has been impacted by hunting and deforestation (Peres, 1997, 1999; Haugaasen & Peres, 2005; Kasecker, 2006).
In the comparatively fewer studies carried out in northernmost Brazilian Amazonia (Souza-Mazurek et al., 2000; Thoisy et al., 2005; Melo et al., 2015), hunting pressure has also been regarded as the main determinant of the structure of primate assemblages. Hunting particularly affects larger-bodied species such as Ateles paniscus, extirpating the species and making it impossible to assess the effects of logging and forest type and heterogeneity on their ecology (Sussman & Phillips-Conroy, 1995; Souza-Mazurek et al., 2000; Thoisy et al., 2005; Lehman et al., 2006). In such studies primates became less abundant near human settlements.
However, in all the studies mentioned above, hunters were Amerindians and native populations (mixed Indian and European ancestry). These are native peoples who since times immemorial have included primates in their feeding repertoire, and for whom primates are often among the mammal species most heavily harvested by them (Branch, 1983; Peres, 1997, 2000; Peres & Dolman, 2000; Souza-Mazurek et al., 2000; Thoisy et al., 2005). In a previous study (Melo et al., 2015), however, in fishbone human settlements the inhabitants were people from outside Amazonia. Primates were not among their harvested species, but were rather avoided due to taboos the settlers brought with them. Human impact on primate assemblages may, therefore, depend on the ethnic origin and consequently dietary preferences of the hunters.
In the absence of human impact primate assemblages should be shaped by habitat productivity, which is correlated with large-scale natural phenomena such as climate, tectonics, fluvial history, topography, and especially with geologically-induced edaphic heterogeneity (Tuomisto et al., 1995, 2003; Kristiansen et al., 2012; Pomara et al., 2012, 2014; Rossetti, 2014; Higgins et al., 2011, 2015). They should also be regulated by unpredictable, yet recurrent fluctuations, such as length of the dry season, variation in food supply and quality, which in turn regulates interference competition among the species for the available resources (Connell, 1980; Chesson & Huntley, 1989; Chesson & Rosenzweig, 1991).
In this scenario, habitat heterogeneity in northernmost Amazonia, with its highly heterogeneous mosaics of forests, campinaranas, campinas and rupununi savannas, plays an important role by greatly enhancing the opportunities for competing species to co-exist through niche segregation. Under such circumstances their respective population abundances may vary substantially between different environments (MacArthur & Levins, 1967; Diamond, 1975; Wiens, 1977; Chesson & Huntley, 1989; Chesson & Rosenzweig, 1991).
Factors determining the structure of primate assemblages can be assessed at different spatial scales (Kasecker, 2006). At the regional level (Peterson et al., 2011), most species can be regarded as occurring over their entire distributional range, such as in northernmost Amazonia (Sussman & Phillips-Conroy, 1995; Lehman, 2000, 2004; Lehman et al., 2006), whereas at the local level (Peterson et al., 2011) there can be a considerable degree of distributional patchiness as a mechanism to avoid direct spatial and temporal competition for the available resources (Mendes Pontes, 1997; Mendes Pontes et al., 2012). For instance, in a primate assemblage of eight species from northernmost Brazilian Amazonia, Mendes Pontes et al. (2012) showed that none of the species inhabited all forest types and that at least one of the forest types had virtually no primates.
These variations at a local scale may be a function of food availability, floristic composition and stratification, forest height, and the availability of water bodies, among other variables (Mendes Pontes, 1999; Lehman, 2004; Haugaasen & Peres, 2005; Kasecker, 2006; Mendes Pontes et al., 2012). As a result, some large-bodied frugivorous species, such as Ateles paniscus, may become habitat specialists and be present only in those tallest forests richest in fruits, whereas some smaller frugi-insectivores, such as Saguinus midas, may prefer shorter forest types highly entangled with vines and lianas, or, as is the case with Saimiri sciureus, may favor riverine forests and rarely be seen away from rivers, where they can find more insects (Sussman & Phillips-Conroy, 1995; Emmons & Feer, 1997; Mendes Pontes, 1997; Lehman, 2004; Lehman et al., 2006; Mendes Pontes et al., 2012).
In this study we wanted to investigate how habitat heterogeneity and hunting by immigrants in a fishbone human settlement may impact the primate assemblages. We, therefore, determined:
- (1)How abundance and relative biomass of the primate assemblages in northernmost Brazilian Amazonia vary at the regional scale (linear distance 200-2000 km; Peterson et al., 2011), taking into consideration regions with different vegetation types, which include dense ombrophilous forests vs. a mosaic of dense ombrophilous forest, ‘campinarana’ (transitional open-canopy forest) and ‘campina’ (open scrub);
- (2)How abundance and relative biomass of the primate assemblages vary at the local scale (linear distance 1-10 km; Peterson et al., 2011), along transects measuring from 3.7 to 5 km, according to density and absolute dominance of trees, average canopy height, the proportion of unflooded forest, the number of clearings, and number of water bodies;
- (3)How primate assemblage structure varies in areas subject to subsistence and also predatory (retaliation) hunting (Reyes, 2013; Melo et al., 2015), independent of the vegetation types, comparing two such human settlements formed by immigrants with a legally protected area with no human pressure. Since Melo et al. (2015) and Reyes (2013) showed that there is no significant direct hunting impact on primates, we tested if we could still detect any indirect impact on them.
Material and methods
The three sites of the study area are located in northernmost Brazilian Amazonia (fig. 1), as follows (impacted areas here meaning areas impacted by deforestation and hunting):
(1) Novo Paraíso settlement (NP): This settlement was founded in 1982 in the Caracaraí municipality in the state of Roraima, northern Brazil (01°13′24.59″N, 60°23′6.2″W; fig. 1). It has ca. 600 immigrant settlers. All are originally from regions outside the Amazonia, primarily from the north and northeast of Brazil, and were attracted by the free land offered by the Federal Government as part of an Amazonian colonization program initiated in the late 1970s (Governo do Estado de Roraima, 2005; Melo et al., 2015). The main activities are subsistence agriculture and extensive cattle production. Forested areas in the region are characterized by a vegetation mosaic formed by extensive campina (open scrub), campinarana (transitional open-canopy forest with short thin trees) and ombrophilous forest areas (closed-canopy forest with tall trees), resulting in high environmental heterogeneity (IBGE, 2009; Mendes Pontes et al., 2012). Three parallel transects measuring from 3.75 to 5 km were cut perpendicular to the settlement in campinarana/ombrophilous forest (table 1; IBGE, 2009).
Soils of the study transects were classified as (EMBRAPA, 2006): (1) Arenic Hydromorphic Ferrohumiluvic Spodisol, associated to Typical Distrophic Haplic Plinthosol and Argisolic Distrophic Haplic Gleisol; (2) Typical Orthic Quartzarenic Neosol, associated to Rock Outcrops.
In a previous study we also monitored hunting activity in Novo Paraíso (Melo et al., 2015) and found that hunting was influenced by cultural taboos mentioned by all respondents (). In the case of primates (22%, ), this was invariably positive. In some cases hunters avoided killing them (12%, ) because it would bring bad luck and in some others (10%, ), due to empathy or superstition based on this order’s similarity to humans. Consequently, only two (0.4%) Alouatta macconnelli, and two (0.4%) Ateles paniscus were killed during the study year (2010) out of 541 medium-sized and large mammals hunted.
Characteristics of the areas and the sampling effort for each transect in the three studied localities – Novo Paraíso (NP) settlement, Viruá National Park (PARNA Viruá) and Entre Rios (ER) settlement – in northernmost Brazilian Amazon.
(2) Entre Rios settlement (ER): This settlement was founded in 1980 in the Caroebe municipality of Roraima (0°47′49.2″N, 59°25′42.0″W; fig. 1). The forested areas in this region are covered entirely by dense ombrophilous forests (IBGE, 2009). ER has 1100 immigrant settlers from regions outside Amazonia. The main activities are subsistence agriculture, banana cultivation and extensive cattle production. Here three parallel transects measuring from 3.7 to 4 km were cut in ombrophilous forests (table 1).
Soils of the study transects were classified as (EMBRAPA, 2006): (1) Arenic Distrophic Red-Yellow Argisol, associated to Distrophic Litolic Neosol, Distrophic Red-Yellow Argisol, Cleyey Distrophic Yellow Latosol, and Cleyey Distrophic Yellow Argisol; (2) Distrophic Litolic Neosol, associated to Cleyey Distrophic Red-Yellow Argisol, and Rock Outcrops.
Hunting is practiced regularly in both ER and NP to complement protein obtained from domestic livestock, and focused only on ungulates: white-lipped peccary, Tayassu pecari (Tayassuidae), white-tailed deer, Mazama americana (Cervidae), and collared peccary, Pecari tajacu (Tayassuidae; Reyes, 2013; Melo et al., 2015). Settlers also practiced predatory (retaliation) hunting, shooting large cats (jaguars, Panthera onca, and pumas, Puma concolor (Felidae)) allegedly because they had preyed upon domestic livestock. Primates form a negligible percentage of game hunting (Reyes, 2013; Melo et al., 2015).
(3) Viruá National Park (PARNA Viruá): PARNA Viruá was decreed on 29 April 1998 and is also located in Caracaraí (01°42′25″N, 61°10′24″W; fig. 1). This park has an area of 2291 km2 and has the same vegetation types as at NP (IBGE, 2009; Mendes Pontes et al., 2012). Three parallel 5-km transects were chosen from the 25-km2 permanent grid of the Biodiversity Research Program – PPBio (www.ppbio.inpa.gov.br), located in campinarana/ombrophilous forest (table 1). All were in forests without hunting pressure (Mendes Pontes et al., 2012; Melo et al., 2015).
Soils of the study transects were classified as (EMBRAPA, 2006): (1) Arenic Hydromorphic Ferrohumiluvic Spodosol, associated to Typical Clayey Distrophic Haplic Gleisol and Typical Clayey Distrophic Fluvic Neosol; (2) Typical Orthic Quartzarenic Neosol, associated to Rock Outcrops.
In each area, seven diurnal primate species have been recorded, according to the IUCN Red List (IUCN, 2016): Brown capuchin, Sapajus apella Linnaeus, 1758 (Cebidae); red-backed bearded saki, Chiropotes chiropotes Humboldt, 1811 (Pitheciidae); common squirrel monkey, Saimiri sciureus Linnaeus, 1758 (Cebidae); red-handed tamarin, Saguinus midas Linnaeus, 1758 (Callithrichidae); Guyanan red howler, Alouatta macconnelli Elliot, 1910 (Atelidae); red-faced spider monkey, Ateles paniscus Linnaeus, 1758 (Atelidae); and white-faced saki, Pithecia pithecia Linnaeus, 1766 (Pitheciidae). In addition, one nocturnal species is present: northern night monkey, Aotus trivirgatus Humboldt, 1812 (Aotidae). Sampling was performed using the line transect method (Buckland et al., 1993), between 06:00 and 17:00 h and between 18:00 and 03:00 h during the dry season between December and January 2010, January and March 2011 and in October 2011.
The trails were walked simultaneously by two observers at an average speed of 1.5 km/h. We walked 100 km per transect during the day and 40 km per transect at night (table 1); the total distance walked was 1248.7 km (table 1).
For each transect, data on habitat characteristics were collected at 50-m intervals on the following variables: density and absolute dominance of trees with a diameter at breast height (DBH) equal to or greater than 10 cm; basal area of the forest and its mean diameter, calculated by the point-centered quarter (PCQ) method (Muller-Dombois & Ellenberg, 1974) with the aid of FITOPAC software (Shepherd, 2006); average canopy height (obtained from the canopy height visually estimated every 50 m along the transects); and the proportion of unflooded forest (obtained from the number of points of unflooded forest counted every 50 m along the transects). In addition, the number of clearings (natural or man-made) and the number of water bodies that crossed a trail were counted.
The type of forest was also determined as terra firme forest (unflooded forests lumped together), campinarana and campina, as in Mendes Pontes et al. (2012), who used Project-Radar-in-the-Amazonia (RADAMBRASIL) satellite images to identify the types. The number of clearings and water bodies was divided by each transect’s length such that the length would not interfere in the analysis. Therefore, these variables were considered proportionally to the size of each trail.
We calculated abundance as encounter rates (number of sighted groups/10 km walked; Chiarello, 1999) and relative biomass [obtained by multiplying the number of individuals of each species/10 km walked by the species’ body mass, expressed as kg/10 km, as in Galetti et al. (2009)]. To obtain the number of individuals/10 km, the encounter rate was multiplied by the average group size. The body mass for each species was obtained from the mean of the masses provided by Emmons & Feer (1997) and Eisenberg & Redford (2000).
We tested the normality of the sampled data with the Shapiro-Wilk test. When the data were not normally distributed, they were transformed with a 10log function. When the data remained non-normal after the transformation, the analysis was performed using non-parametric tests. Only two-tailed P values ⩽ 0.05 were considered significant. Assuming normality and homoscedasticity, we undertook analyses of variance (ANOVA) to evaluate whether there were differences between the environmental parameters in the three study areas. The basal area and average diameter were correlated with dominance and were excluded from the analyses.
Assemblage structure at the regional level
We carried out a two-way ANOVA for both abundance and relative biomass of the species in the three studied areas to test whether the primate assemblage structure varied at the regional level. In order to determine if this potential variation was a function of the different plant physiognomies, human pressure in the settlements, or the interaction of both factors, we subsequently carried out a Tukey test. All of the structural parameters of the assemblages were 10log-transformed.
Although Melo et al. (2015) showed that hunting has only a negligible direct effect on primates, they also showed that its impact on the vertebrate assemblages in the studied human settlements is considerable, even driving white-lipped peccaries Tayassu pecari close to local extinction. Thus, we decided to compare the abundance and relative biomass of those species mentioned as hunted in other scenarios in the Neotropics (Peres, 2000; Bennett et al., 2001; Thoisy et al., 2005; Palminteri et al., 2011), or in Melo et al. (2015) (Alouatta macconnelli, Ateles paniscus, Chiropotes chiropotes and Sapajus apella), between areas with the same forest type but different human impacts: NP (impacted area: campinarana/ombrophilous forest) vs. PARNA Viruá (protected area: campinarana/ombrophilous forest) by means of a t-test (independent samples) to test if there could be any indirect human impact on each of the studied species individually, and a t-test (dependent samples) for the four hunted species together. Again, both the abundance and relative biomass of the various species were 10log-transformed.
Assemblage structure at the local level
Non-metric multidimensional scaling (NMDS) was used to determine whether there were differences in the abundances of the primate species within assemblages (among transects) and between the three areas studied. NMDS was performed using a Bray-Curtis similarity matrix with 100 random restarts. The data were standardized and square-root-transformed.
To determine whether the local habitat structure variables explained the variation in the abundance of primate species in the three areas and whether any species were associated with any of these environmental variables, a canonical correspondence analysis (CCA) was conducted. The relationship between environmental variables and species with the scores of CCA ordination axes were examined using nonparametric Kendall’s ranked correlations.
Primate assemblage structure at the regional level
A total of 410 sightings of the eight primate species were recorded in the three study areas ( at PARNA Viruá; at ER; at NP). Mean total primate abundance was 3.28 groups/10 km walked (3.79 groups/10 km at PARNA Viruá, 3.08 groups/10 km at ER and 2.98 groups/10 km at NP; table 2). There were significant differences in the abundances between the areas (ANOVA: , ). These differences were detected between areas with different plant physiognomies: ER (dense ombrophilous forest) vs. NP (campinarana/ombrophilous forest) (Tukey test: , ), and ER vs. PARNA Viruá (campinarana/ombrophilous forest) (Tukey test: , ). No significant differences were detected, however, between areas with the same forest type and different human pressure (PARNA Viruá vs. NP; Tukey test: , ns).
Structural parameters of the primate community at Novo Paraíso (NP) settlement, Viruá National Park (PARNA Viruá) and Entre Rios (ER) settlement in northernmost Brazilian Amazon.
Accordingly, the absolute dominance (m2/ha) of trees with a DBH ⩾ 10 cm (ANOVA: , ) and the number of clearings (ANOVA: , ) showed significant differences between the study areas with different plant physiognomies (ER vs. NP and PARNA Viruá; table 3). The dominance at the ER settlement of dense ombrophilous forest was over two times greater than in areas occupied by campinarana/ombrophilous forest (table 3), which is likely to be the result of an increase in the amount of resources, especially fruits, available to the mammalian assemblages.
Environmental variables at Novo Paraíso (NP) settlement, Viruá National Park (PARNA Viruá) and Entre Rios (ER) settlement.
Large-bodied primate species, Ateles paniscus and Alouatta macconnelli, were more abundant in the dense ombrophilous forests of the impacted ER settlement (0.7 groups/10 km and 0.6 groups/10 km, respectively). In contrast, the small-bodied species, Saguinus midas, was more abundant in the impacted areas, independent of the forest type (dense ombrophilous forests of ER settlement: 1 group/10 km, and campinarana/ombrophilous forests of NP settlement: 0.8 groups/10 km), and Aotus trivirgatus and Saimiri sciureus (the latter, the least abundant of all species) were more abundant in the campinarana/ombrophilous forests, especially in the impacted NP settlement (0.7 groups/10 km and 0.1 groups/10 km, respectively; table 2; fig. 2).
The medium-sized species, Sapajus apella, had the highest abundance in all areas, and, together with Chiropotes chiropotes, had its highest abundance in the campinarana/ombrophilous forests of the protected area PARNA Viruá (2.5 groups/10 km and 0.5 groups/10 km, respectively); the highest abundance of Pithecia pithecia also occurred in campinarana/ombrophilous forests, but contrary to the previous species, in those impacted by the NP settlement (table 2; fig. 2).
The mean total primate relative biomass in this area was 67.23 kg/10 km (96.8 kg/10 km at PARNA Viruá; 55.1 kg/10 km at the ER settlement and 49.8 kg/10 km at the NP settlement). There were no significant differences in the relative biomass between areas (ANOVA: , ), even though the relative biomass in the protected area was almost two times greater than that in the areas subjected to human pressure (NP and ER; table 2).
The large-bodied primate species, Ateles paniscus and Alouatta macconnelli, had the highest relative biomasses in the impacted area ER settlement (21.3 kg/10 km and 12.1 kg/10 km, respectively), with Ateles paniscus having the overall highest relative biomass in the dense ombrophilous forest close to this settlement. Contrastingly, the small-bodied Saguinus midas, Saimiri sciureus and Aotus trivirgatus had their highest relative biomasses in the mosaics of campinarana/ombrophilous forests, Saguinus midas and A. trivirgatus in the impacted NP settlement (2.3 kg/10 km and 0.7 kg/10 km, respectively), and S. sciureus in the protected area PARNA Viruá (7.7 kg/10 km; table 2; fig. 3).
The medium-sized species, Sapajus apella, Chiropotes chiropotes, and Pithecia pithecia also had their highest relative biomasses in the mosaics of campinarana/ombrophilous forests. Sapajus apella and C. chiropotes had their highest relative biomasses in the protected area PARNA Viruá (50.8 kg/10 km and 19.1 kg/10 km, respectively), with S. apella having the overall highest relative biomasses in all the study areas but ER. Pithecia pithecia, in turn, had the highest relative biomass in the impacted area NP settlement (2.7 kg/10 km; table 2; fig. 3).
Primate assemblage structure at the local level
Ordination analyses detected differences in the primate assemblage structures both between the different study areas and within a particular area (fig. 4). Two distinct groups were observed: one for the transects located at the ER settlement (dense ombrophilous forest) and another for the transects at the NP settlement and PARNA Viruá (campinarana/ombrophilous forest), even though at PARNA Viruá, the transects were more dispersed along the ordination axes (fig. 4).
For the CCA results, the first two axes explained 48% of the variation in primate abundance. The environmental variables that best explained this variation were the absolute dominance of trees with a DBH ⩾ 10 cm for CCA axis 1 (Kendall’s ranked correlation: , ), and the number of clearings for CCA axis 2 (Kendall’s ranked correlation: , ; fig. 5). The ER settlement transects had a stronger relationship with a greater dominance and number of clearings. No pattern was observed for the transects located in areas of campinarana/ombrophilous forest.
In the CCA results, Ateles paniscus showed a significant positive association with absolute dominance of trees with DBH ⩾ 10 cm (Kendall’s ranked correlation: , ) and the number of clearings (Kendall’s ranked correlation: , ), whereas Aotus trivirgatus was negatively associated with the vegetation height (Kendall’s ranked correlation: , ; fig. 5).
None of the other primate species, Alouatta macconnelli, Sapajus apella, Chiropotes chiropotes, Pithecia pithecia, Saguinus midas, and Saimiri sciureus, were significantly associated to any of the studied environmental variables, although some tendencies could be detected: A. macconnelli and S. midas were weakly associated with forest clearings; C. chiropotes positively, and P. pithecia, negatively associated with forest height; and S. sciureus, with water bodies. S. apella was the closest to the centroid, and the only species not to present any tendencies.
Primate assemblage structure at hunted vs. unhunted sites
When the abundances of the hunted species in the settlements were compared between PARNA Viruá and the NP settlement (same forest type but different human pressure), no significant differences were found: Ateles paniscus: Student’s t-test: , df = 4, ; Alouatta macconnelli: Student’s t-test: , df = 4, ; Chiropotes chiropotes: Student’s t-test: , df = 4, ; and Sapajus apella: Student’s t-test: , df = 4, (fig. 6), suggesting that forest type was the main determinant of their abundance. No difference was detected either when we compared the overall abundance of these species between areas (Student’s t-test: , df = 3, ).
Species’ relative biomasses also showed no significant differences between NP and the protected area: Ateles paniscus (Student’s t-test: , df = 4, ); Alouatta macconnelli (Student’s t-test: , df = 4, ); Chiropotes chiropotes (Student’s t-test: , df = 4, ); Sapajus apella (Student’s t-test: , df = 4; ; fig. 6). Additionally, no difference was detected when we compared the overall relative biomass of these species between areas (Student’s t-test: , df = 3, ).
Although no significant differences were detected between the protected area PARNA Viruá and NP, Sapajus apella, Chiropotes chiropotes and Ateles paniscus showed a reduction in abundance and, especially, relative biomass at NP (fig. 6).
Primate assemblage structure at the regional level
There is a considerable variation in primate abundance and biomass within Amazonia (Peres, 1999; Thoisy et al., 2005; Palminteri et al., 2011), although a general pattern can be seen, with abundance and biomass being lower in the northernmost areas (Mendes Pontes, 1997, 1999; Lehman, 2000, 2004; Brum, 2011), compared to the rest of the basin (Peres, 1999; Bennett et al., 2001; Haugaasen & Peres, 2005; Kasecker, 2006; Palminteri et al., 2011). Even within the northernmost region, however, primate abundance can be highly variable (Sussman & Phillips-Conroy, 1995; Mendes Pontes, 1997, 1999; Lehman, 2000, 2004; Lehman et al., 2006).
Hunting pressure and forest productivity have been considered to be the main drivers of the variation in primate assemblage composition, abundance and biomass in Amazonia (Peres, 2000; Peres & Dolman, 2000), although there may be considerable interregional differences. In central Amazonia habitat characteristics were the most important variable defining primate assemblages (Haugaasen & Peres, 2005; Kasecker, 2006), while hunting was the most important in western (Palminteri et al., 2011) and northeastern Amazonia (Thoisy et al., 2005). In this study, we show that forest type was the most important variable defining the structure of all primate species assemblages at the regional level.
The largest primate species, Ateles paniscus, is generally considered to be restricted to the primary high evergreen open forests where it inhabits mainly the upper canopy of tall trees. The species tends to disappear quickly from disturbed areas due to deforestation and hunting (Sussman & Phillips-Conroy, 1995; Emmons & Feer, 1997; Lehman 2004; Thoisy et al., 2005; Lehman et al., 2006; IUCN, 2016). Accordingly, in this study they appeared to prefer high ombrophilous forests due to their dependence on tall trees.
Contradicting the assumption that A. paniscus disappears from disturbed sites, however, these high ombrophilous forests are located in the Entre Rios fishbone human settlement. This suggests that even if under considerable human impact, if hunting is not affecting them directly (Reyes, 2013; Melo et al., 2015), these primates should still prefer high ombrophilous forests located in disturbed scenarios over those forest mosaics with a reduced proportion of tall trees even if they are located in a strictly protected area, such as PARNA Viruá. Even more striking is the fact that these primates also occurred in the forests surrounding the NP fishbone human settlement, which comprises a mosaic of campinarana/ombrophilous forest in a disturbed fishbone human settlement, revealing a considerable resilience to such impacts.
According to the literature Alouatta macconnelli is found most often in forests with tall trees, but it also inhabits a variety of primary and disturbed forest types, including high evergreen and seasonal forests, lowland and riverine forests, semi-deciduous, dry deciduous forests, savanna and liana forests, among others, where they primarily exploit the middle to upper canopy (Sussman & Phillips-Conroy, 1995; Emmons & Feer, 1997; Mendes Pontes, 1997; Lehman, 2004; IUCN, 2016). Despite their highly generalist habitat preferences and their ability to thrive in disturbed habitats (Naughton-Treves et al., 2003), they preferred the high ombrophilous forests of the Entre Rios settlement, since they favor tall trees in high forests, and hunting impacts there were negligible (Reyes, 2013; Melo et al., 2015).
Sapajus apella is one of the most commonly seen primate species in Amazonia, being found in almost any forest type, due to their highly generalist habitat preferences allied to a wide dietary repertoire, which makes them one of the most successful primates in the Neotropics (Emmons & Feer, 1997; Siemers, 2000). They can be found in high and low rainforests, seasonally flooded forests, palm forests, white sand and scrub savannas, riverine, mangrove and swamp forests, among many others, and also in secondary and disturbed formations (Sussman & Phillips-Conroy, 1995; Emmons & Feer, 1997; Mendes Pontes, 1997; IUCN, 2016).
In this study S. apella was the most abundant primate species at all three study sites, but appeared to favor the mosaics of campinarana/ombrophilous forest of PARNA Viruá and Novo Paraíso settlement, since they do not depend on tall trees to survive. Their habitat and feeding plasticity should allow them to benefit from most or all of the available habitats.
The fact, however, that the highest S. apella abundances were in PARNA Viruá, a protected area, suggests that they may have benefitted from the total absence of human disturbances. Supporting this assumption is the fact that in French Guyana, in a similar scenario, although they were much less harvested than the other game species, S. apella were still much less abundant around human settlements, possibly due to the impact of other factors related to human disturbance (Thoisy et al., 2005), such as selective logging, and roads bisecting the forest, among others.
Chiropotes chiropotes inhabits terra firme forests, including high and low forests, savanna, and mixed semi-deciduous forests, as well as palm forests, such as Mauritia flexuosa clumps (Sussman & Phillips-Conroy, 1995; Emmons & Feer, 1997; Mendes Pontes et al., 2010; IUCN, 2016). Nevertheless, Chiropotes chiropotes were more abundant in the mosaics of campinarana/ombrophilous forest of the protected area, and of Novo Paraíso, suggesting that they favored the high heterogeneity of these forests. The fact that C. chiropotes was considerably more abundant in the protected area, and that it is described in the literature as typically inhabiting mature, undisturbed forests (Emmons & Feer, 1997; IUCN, 2016), suggests that human impact may ultimately limit their abundance in the disturbed areas (as in Thoisy et al., 2005).
Pithecia pithecia is considered to be chiefly a mature-forest primate, preferring tall primary forests, where they use most intensively the middle and lower levels (Emmons & Feer, 1997), although they can be found in lowland, terra firme and riverine forests, of closed or open canopy, and in secondary and disturbed forests (Sussman & Phillips-Conroy, 1995; Emmons & Feer, 1997). In northernmost Brazilian Amazonia, Mendes Pontes (unpublished data) found them to prefer shorter forest types such as campinarana. Here, they were frequently seen in entangled, viny forest patches.
In this study P. pithecia appeared to prefer the forests around NP which contain all the features of their preferred habitat, including high heterogeneity, frequent edge habitats, and man-made, secondary growth vegetation. This emphasizes P. pithecia’s ability to benefit from all the environmental and anthropogenic aspects of the forest, and predicts their ultimate survival in a changing landscape, as far as they are not a target for hunters.
Saguinus midas can be found in mature and secondary growth forests, and disturbed habitats; in montane, high, and lowland forests, campinaranas, white-sand and savanna forests, although they prefer open forests, as well as edge and disturbed habitats (Sussman & Phillips-Conroy, 1995; Emmons & Feer, 1997; Eisenberg & Redford, 2000; Mendes Pontes et al., 2012; IUCN, 2016). Accordingly, their highest abundances occurred in the impacted areas of Novo Paraíso and Entre Rios, independent of the forest type, suggesting that the main determinant for the occurrence of S. midas was the availability of human-modified habitats. In fact, extensive tracts of this type of habitat can be seen on Project-Radar-in-the-Amazon (RADAMBRASIL) satellite images (see also fig. 1).
Saimiri sciureus occurs primarily in riverine forests, floodplains, and seasonally flooded forests, but can also be found in palm, gallery, and low forests, in both mature and disturbed habitats (Sussman & Phillips-Conroy, 1995; Emmons & Feer, 1997; Mendes Pontes 1997, 1999; Lehman, 2004; IUCN, 2016). Accordingly, the lowest overall regional abundances of this species occurred where the proportion of flooded forests and water bodies was lowest. They preferred the forest mosaics of the protected area, PARNA Viruá, which had the highest percentage of seasonally flooded forests.
Aotus trivirgatus occur in primary and secondary forests, submontane, terra firme, seasonally flooded and lowland forests, seasonally dry and dry forests, although they prefer open canopy and riverine forests (Emmons & Feer, 1997; IUCN, 2016). At Maracá Ecological Station in northernmost Brazilian Amazonia, however, they were seen exclusively in the much shorter vine-rich habitats of the edge of the seasonally dry forests with the rupununi savannas and in the riverine forests (Mendes Pontes et al., 2010). In the current study they occurred only in Novo Paraíso and PARNA Viruá, suggesting that they favored the edge habitats that are common in these highly heterogeneous mosaics of campinarana/ombrophilous forest, especially in Novo Paraíso, where human-modified habitats have been added.
Primate assemblage structure at the local level
Primate abundance and biomass in this region also vary considerably at the local level (Mendes Pontes, 1997, 1999; Kasecker, 2006), and, as shown in this study, vary even when overall abundance varied little between nearby areas. This occurred primarily because of the considerable changes in vegetation structure that occur even over a few meters (as in Mendes Pontes, 1997, 1999; Mendes Pontes et al., 2012). There was, nevertheless, a greater similarity in assemblage structure between nearby transects with the same forest type. Environmental variables, such as vegetation height and forest stratification (Mendes Pontes, 1997, 1999; Lehman, 2004, this study) shaped the primate assemblages on a smaller spatial scale.
Ateles paniscus is considered to be extremely dependent on tall trees, preferring the highest forest strata (Sussman & Phillips-Conroy, 1995; Emmons & Feer, 1997; Lehman, 2004; Thoisy et al., 2005; Lehman et al., 2006; IUCN, 2016), and, as expected, in this study the species had a statistically significant positive association with those transects with the highest absolute dominance of the tallest trees. The species also appeared to be negatively associated with tree density, supporting the argument that A. paniscus prefers open forests, which most possibly facilitate their form of locomotion (Emmons & Feer, 1997).
Despite being regarded as one of the first primate species to disappear from areas that become degraded (Peres, 2000; Bennett et al., 2001; Thoisy et al., 2005; Palminteri et al., 2011; Mittermeier et al., 2015), in the settlements studied here A. paniscus was associated with clearings (natural or as a result of deforestation), and could regularly be seen even in the borders of the forest with the open fields of small holdings. This suggests that if hunting is not affecting them directly (Melo et al., 2015), A. paniscus may show some resilience in disturbed areas. Alternatively, it could be the case that the impact of the settlement is still small for the species.
Due to their ability to adapt and even increase their abundances in disturbed habitats (Sussman & Phillips-Conroy, 1995; Emmons & Feer, 1997; Mendes Pontes, 1997; Lehman, 2004; IUCN, 2016), Alouatta macconnelli and Saguinus midas were weakly associated with those transects with the highest number of forest clearings, which may have more appropriate microhabitats in which they can find more food (Lehman, 2004).
Aotus trivirgatus prefers the denser areas of highly entangled lianas and vines of short vegetation and open areas (Emmons & Feer, 1997; Mendes Pontes et al., 2010, 2012; IUCN, 2016). At Maracá Ecological Station, a site with a vegetation similar to that of the current study, A. trivirgatus was sighted almost exclusively in the vine tangles on the borders of seasonally dry forests with the rupununi savannas of Roraima (Mendes Pontes et al., 2010), and was significantly and negatively associated with those transects with highest mean tree height. This trend, although not significant, was also observed in Pithecia pithecia, which was most frequently sighted in the campinarana forest, quietly hiding in the massive entanglements of lianas and vines of the middle canopy.
Sapajus apella, despite a slight tendency to associate with those transects with the highest tree density, appeared to be one of the most generalist species, confirming its high ability to exploit all the habitats available (Emmons & Feer, 1997; Mendes Pontes, 1997; Mendes Pontes et al., 2010; Siemers, 2000; IUCN, 2016).
Records for Saimiri sciureus confirmed its preference for riverine and flooded forests, along which they travel and where they can find more invertebrates, their main food source (Mendes Pontes, 1997, 1999; Emmons & Feer, 1997; Lehman, 2004; IUCN, 2016). It was weakly associated with those transects with the highest proportions of water bodies.
In the case of Chiropotes chiropotes, besides favoring the forest mosaics of the protected area PARNA Viruá, it also had a weak association with those transects with the highest mean tree height. This confirms its ability to exploit various forest types, although within those particular habitats it still preferred the tallest trees, as in Emmons & Feer (1997).
There might nevertheless be a more subtle, positive effect of the human disturbance on those primates that tend to favor shorter, highly entangled, edge habitats, such as Aotus trivirgatus and Saguinus midas, that should benefit much from additional secondary growth, disturbed habitats. Further studies should shed light on this assumption, and also on the ultimate fate not only of primates, but of the entire mammalian assemblages surrounding these relatively young fishbone human settlements. Landscape fragmentation analysis could shed light on the question whether certain primate species benefit from the presence of the settlement or if they just do not mind it.
Primate assemblages around these fishbone human settlements, as much as in the protected area, were, therefore, shaped by habitat heterogeneity at both regional and local level. Thus, even Ateles paniscus, recognized as one of the most sensitive species, and generally the first to disappear from disturbed sites, was widespread around the fishbone human settlements, even in the borders of the forest with the secondary growth vegetation and open fields of the small holdings.
We thank Fundação O Boticário de Proteção à Natureza for financing this study; Conselho Nacional de Desenvolvimento Científico-CNPq for granting graduate scholarships to JRG (No. 472401/2008-4), MNDS (No. 130986/2010-0) and APSJ (No. 552207/2008-8) and a research grant to ARMP (No. 472401/2008-4); Pro-Reitoria de Pesquisas-PROPESQ of the Universidade Federal de Pernambuco for providing a grant for field work; Instituto Chico Mendes de Conservação da Biodiversidade-ICMBio and Parque Nacional do Viruá for allowing this study to be performed at the grids of the Programa de Pesquisas em Biodiversidade-PPBio. We also thank Marcelo Luna for the species illustrations and William E. Magnusson for useful comments. The research adhered to the legal requirements of Brazil, where the research was conducted, and did not violate the ethical treatment of nonhuman primates. Adrian Barnett corrected the English. This manuscript was evaluated via Peerage of Science before submission to this journal. We are also indebted to Joris M. Koene and an anonymous reviewer for very useful corrections for the final version.
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