ABUNDANCE OF TREES USED AS FOOD BY PRIMATES IN FRAGMENTS OF ATLANTIC FOREST

Forest fragmentation favours the propagation of some arboreal primate species that can alter the floristic composition of a community. This process may be associated with the loss of seed dispersants. In this work we propose to identify if the presence of frugivorous primates of medium and large size (Sapajus flavius and Alouatta belzebul) can influence forest diversity and structure. Further, we ask if the size of the fragment affects the availability of resources for these primates. Three fragments were studied in the Atlantic Forest of the State of Paraíba, Brazil, located in the municipalities of Sapé, Mamanguape, Rio Tinto, and Mataraca. In each area 25 plots of 50 x 4 m were delimited, randomly distributed along trails and transects. All trees with chest-high circumferences (CAP) above 12 cm found within the plots were marked with ribbons, and numbered continuously. A total of 114 plant species were documented in the Pacatuba Forest, 79 in the Asplan Forest, and 97 in the “Guaribas” (Sema III) Biological Reserve (REBIO) Forest. According to the Chao and Jacknife estimators, the REBIO Guaribas Forest can present more species than recorded in the present Environ. Smoke SILVA et al. v. 1, n. 1, 2018 21 investigation. Species Tapirira guianensis, Protium giganteum and Protium heptaphyllum are the most abundant in the Asplan, Pacatuba and Sema III Forests, respectively. In the REBIO Guaribas Forest, the Shannon diversity index was (H') = 3.75, the Alpha-Fisher index was = 26.57 and the Simpson index (1-D) was = 0.90. Pacatuba was the forest fragment with the highest index of diversity (H') = 375, Alpha-Fischer = 33.74 and Simpson (1-D) = 0.95. Pacatuba and REBIO Guaribas Forsts possess greater Beta diversity. The results suggest that local and historical factors possibly increase Beta diversity, contributing to the increase in resources used as food by primates. Therefore, the presence of primates of medium and large size in the Pacatuba Forest may affect the diversity of resources, contributing to the dispersion of large fruits and seeds. The presence of primates of medium and large size can thus contribute to the preservation of floristic diversity in forest fragments.

investigation.Species Tapirira guianensis, Protium giganteum and Protium heptaphyllum are the most abundant in the Asplan, Pacatuba and Sema III Forests, respectively.In the REBIO Guaribas Forest, the Shannon diversity index was (H') = 3.75, the Alpha-Fisher index was = 26.57and the Simpson index (1-D) was = 0.90.Pacatuba was the forest fragment with the highest index of diversity (H') = 375, Alpha-Fischer = 33.74 and Simpson (1-D) = 0.95.Pacatuba and REBIO Guaribas Forsts possess greater Beta diversity.The results suggest that local and historical factors possibly increase Beta diversity, contributing to the increase in resources used as food by primates.Therefore, the presence of primates of medium and large size in the Pacatuba Forest may affect the diversity of resources, contributing to the dispersion of large fruits and seeds.The presence of primates of medium and large size can thus contribute to the preservation of floristic diversity in forest fragments.
Key words: Forest fragmentation; Availability of resources; Diversity.

INTRODUCTION
The rate of destruction of tropical forests is presently alarming (PUIG, 2008).Tha Atlantic Forest in particular has been drastically reduced and fragmented due to excessive exploration, deforestation and fires, being presently restricted to less than 7% of its original area (CHIARELLO, 1994;DALPONTE, LIMA, 1999).The destruction of tropical forests and their deforestation reduce forested areas, transforming them into fragments known as patches or islands.Such a process of reduction and isolation of the natural vegetation affects the structure and functioning of plant communities, resulting in loss of biological biodiversity, death of trees in bordering areas, among other changes (CERQUEIRA et al., 2003).
Fragmentation causes isolation among the surviving forested áreas.According to Laurance and Vasconcelos (2009), the distance between two forest fragments or the distance existing between a fragment and a continuous area of forest may affect the displacement of animals and of plant propagules.Deforestated areas measuring from 15 to 100 m in width may act as barriers for the displacements of several species, including arboreal mammals (GILBERT; SETZ, 2001;LAURANCE;VASCONCELOS, 2009).
In Northeastern Brazil, Bonvicino (1989) observed that some species of trees provided more than one food item.For example, the species Guapira sp furnishes leaves, flowers and fruits as food items.In that research, 47 species of plants were used as food by the guaribamonkeys.Thirty-six percent of these plants were consumed by Callithrix jacchus (the Whitetuft Marmoset) and 12,7% were consumed by some species of bats.Camargo et al. (2008) observed a reduction in the consumption of fruits during the dry season and an increase in the consumption of the other food items such as leaves and flowers, due to the reduction of the availability of fruit during the periods of lower precipitation.Tabarelli et al. (2010) reinforced that the borders resulting from fragmentation stimulate the proliferation of pioneer species and a constant reduction in the abundance of species with lower growth rates.This occurrs because most of these species have large seeds and their dispersal agents, the frugivorous animals, are unable to become established in their original habitat and thus search for other more favourable areas.This breaks existing links previously existing with the plants that depend on animals for dispersal.The pioneer species, which do not necessarily depend on animals for dispersal, tend to dominate, because their seeds are small and may be transported by physical agents such as water and wind.They gradually replace species which are late to arrive.This affects the whole community in the long run.Even strongly resilient forests, when fragmented, reduce their availability of resources, demanding many years to recover and to furnish the same resources which were available previously (GUREVITCH; SCHEINER; FOX, 2009).
Primates are important agents for the regeneration of fragmented forests, because they are effective dispersants of large seeds (IZAR, 2008;MOURA;McCONKEY, 2007).Thus, forest fragments that possess large primates are possibly more diverse in trees used as food resources.This hypothesis is based on three premises: i) The size of the primate affects the species composition of plants in the forest, because when a primate chooses between fruit of small seeds or of large seeds belonging to different species, it is in fact selecting the species which it will disperse; ii) The size of the primate affects the composition and distribution of species because the selected fruit are ingested and dispersed during their daily locomotion; iii) The size of the primate affects the composition, the distribution of species, and consequently the forest structure.Depending on the type of seed dispersed, the fragment will have emergent species or species tolerant of shade.In this paper we evaluate if (1) the size of a forest fragment indeed affects the availability of resources for non-human primates in the Atlantic Forest in the State of Paraíba and if (2) the presence of frugivorous primates of median and large size (Sapajus flavius and Alouatta belzebul) influence the diversity and structure of the forest.

Study area
Three forest fragments were studied, two located in the northern coast of the State of Paraíba, and the third located about 50 km inland (Fig. 1).The forest of Pacatuba Farm is a Private Reserve of the Natural Heritage (RPPN) with 266.53 ha, located in the Municipality of Sapé.
The forst of ASPLAN (Sugar Cane Planters Association of Paraíba), with 96.5 ha, is a Legal Reserve located between the Municipalities of Mamanguape and Mataraca.The Biological Reserve (REBIO) "Guaribas" SEMA III (327.0 ha), also known as "Mata do Maracujá", is located in the Municipality of Rio Tinto.The three areas share an AS-type climate, that is, a humid tropical climate, with rains in the fall-winter (KÖPPEN, 1948).The rainy season begins during the month of March, at the beginning of Fall, and continues until July, just after the onset of Winter.Between 2008 and 2011, the maximum rainfall in Asplan and Sema III occurred in the month of April, with 279.6 mm and 282.5 mm, respectively.Lowest precipitation occured in November, with 18.9 mm and 11.0 mm, respectively.In Pacatuba, maximum precipitation (236.2 mm) occurred in the month of July and minimum rainfall, 7.4 mm, occurred in October (Fig. 2).
In each area 25 plots measuring 50 x 4 meters were delimited.These plots were located along trails and transects within the forest fragments (Fig. 3).Some of these trails measured up to 2 km long.Along the longest trails, points were established by draws to determine the beginning of each vegetation plot.The side in which a plot was positioned was selected at ramdom with the through of a coin.Plots were rectangular, a shape that may contain more species than a square or circular plot of the same size (GUREVITCH; SCHEINER; FOX, 2009), and may thus better sample the vegetation.These plots were delimited by string.All trees located within each plot, with a circumference at the height of the chest (CAP) ≥ 12 cm were marked with a ribbon and numbered consecutively.Later, the values of CAP were transformed into diameters at chest height (DAP), using the formula DAP = CAP / π, where (π = 3.14).The height of all marked trees were estimated visually using a scaled stick of 6 meters.Each study area that contained at least 5% of the total number of individuals was considered abundant.The REBIO Guaribas (SEMA III) Forest is located about one km away from an urban area.Altitudes vary from 20 to 134 m above sea level (GOOGLE EARTH, 2018), having a brook flowing through it.The Pacatuba Farm Forest has altitudes that vary from 75 m to 150 m, being drained by several permanent streams (DE SOUZA, 2005).In the localities with more water available the forest is larger and the vegetations is denser.At higher altitudes the soil varies from sand to clay, with a vegetation of the Savanna type, trees being of small to median size.The ASPLAN Forest is unike in not having water streams.Its relief is not very steep, altitudes varying from 96 to 136 m (GOOGLE EARTH, 2018).All three fragments are surrounded by sugar-cane plantations or pastures.The REBIO Guaribas Forest is further surrounded by an urban area.Some plant species were identified in situ.For the identification of the remaining species, samples of the vegetative structures (leaves) and, when possible, of the reproductive structures (flowers and fruits) were obtained.Exicatae were prepared from the collected samples and compared to those deposited in the Herbarium Lauro Pires Xavier (JPB) of the Federal University of Paraíba (UFPB/Campus I), in order to confirm identifications.The new exicatae were deposited in this herbarium.

Data analyses
The data were inserted into electronic spredsheets for preliminary analyses.They were later analysed in different programs.The statistic program "Past" (version 3.13) was used to evaluate the alfa diversity of the communities.Indices of Shannon-Wiener (H'), Simpson (1-D) and Alpha-Fisher were used.
Beta diversity, corresponding to the dissimilarity between species of two or more communities (BARROS, 2007), represents the dissimilarity between species of two or more communities.Beta diversity was estimated for the three studied areas.As lowest similarities indicate highest dissimilarities; the Beta diversity ndicates few shared species.
The "Jaccard" similarity index was used in the three study areas.The advantage of this index is that it is not influenced by the more abundant species.Furthermore, areas with a history of environmental perturbations are more susceptible to the appearance of pioneer species, and the abundance of these species would also be able to influence the similarity.

RESULTS AND DISCUSSION
A total of 1339 trees were recorded in the Asplan Forest, belonging to 79 species.In the Pacatuba Forest we recorded 956 trees, while in REBIO Guaribas (Sema III) Forest (alternatively named the Psiion-Fruit Forest), a total of 996 individuals belonging to 97 species were recorded.The Asplan Forest has the highest abundance of trees with a height of uto to 10 m; trees with Heights up to 50 m were only found in Pacatuba Farm Forest.At REBIO Guaribas Forst, the maximum height of the trees reached 35 m (Fig. 4A).Regarding tee diameter, Pacatuba Forest differs from the remaining ones for having trees with a large diameter, such as of an individual of Parkia pendula that has 171.02 cm; in REBIO Guaribas and Asplan, the largest diameters did not overreach 82.74 cm (Fig. 4B).REBIO Guaribas further presented the largest number of trees with up to 15 cm in diameter.The mean diameter in Pacatuba is higher than for the remaining areas (Tab.1).Seven species of highest occurrence were indicated for Asplan Forest, four in Pacatuba Forest, and three in REBIO Guaribas Forest (Fig. 5).The most abundant species in Pacatuba Forest was Protium giganteum, while the species Protium heptaphyllum was most frequent in REBIO Guaribas Forest.In Asplan Forest, Eschweilera ovata was the species of highest occurrence.The collector curve, or cumulative species curve, indicates a gradual increase in the number of species for the Asplan Forest, indicating that further species may be found.On the other hand, the REBIO Guaribas Forest and the Pacatuba Forest show a graph line that is close to stabilization, which theoretically indicates that most species have been sampled.The collector curve may not be the best indicator for the total number of species from a given locality, because even after stabilization there is always the possibility that unsampled species will appear.Thus, the use of estimators permits more precision in the evaluation of total species numbers in the studied areas.
Estimates of species richness are very useful, when different communities are compared, or even when comparing the number of species or individuals per sample.Such measurements permit the estimation of the total number of species present in a community on the basis of the sampled data.
According to the estumators Chao1 and Jacknife1, the REBIO Guaribas or Passion-Fruit Forest was possibly subsampled, indicating that a larger sampling effort may possibly increase the number or recorded species (Fig. 6).Pacatuba Forest has a larger number of species of fruit trees consumed by primates (31 consumed species).REBIO Guaribas (Sema III) Forest has fewest species consumed by primates (19 species).In Asplan Forest, Tapirira guianensis, a species common in secondary forests or in forests subject to recovery, stands out (e.g.LORENZI, 2002).This species may also be common in fragmented areas, as the Asplan Forest is being subject to stages of regeneration.Other species that have the fruits consumed by primates are: Licania sp., Guatteria sp., and Inga sp.In Pacatuba Forest, the species with fruits eaten by primates were:
The species T. guianensis, Licania sp., Guatteria sp. and Inga sp. were the most abundant in the Asplan Forest.Species such as Cecropia sp., Myrcia sp. and Piptadenia were not found in the plots of the Pacatuba Forest, although they occur in the region, having been found in the Asplan Forest (Fig. 7).

Beta Diversity
In the Asplan Forest, the mean similarity between plots is much larger.Consequently, Beta diversity is smaller.On the other hand, Pacatuba Forest has least similarity among areas, and consequently presents a higher Beta diversity (Fig. 9).A similar situation afflicted the REBIO Guaribas (Sema III) Forest, before it became a Biological Reserve, but deforestation was less pronounced here.The Pacatuba Forest, due to its greater distance from urban areas, and due to its belonging to the Japungu Sugar-Plant, presents a better state of preservation.
De Souza (2005) recorded 56 species consumed by primates in the Pacatuba Forest, while we found 31 fruit trees consumed by primates in this same area.Our results are similar to the 34 fruit trees recorded by Bonvicino (1989).The larger number indicated in De Souza Fragmentation favours the appearance of species with small seeds and fruits, whose proliferation is more efficient.This results in the increase of species with small seeds or with seeds disopersed by wind.In the long run, species with delayed growth and with larger fruits and seeds become replaced by the smaller-seed pioneer species.The REBIO Guaribas (Sema III) Passion-Fruit Forest does not have primates of medium or large size, such as S. flavius and A. belzebul, and has the smallest number of plant species consumed by primates.It is also possible that the proximity of this area to urban settlements has negatively affected the diversity of species, as a result of its history of perturbation.Furthermore, the low declivity of this area does not favour the formation of microhabitats, resulting in an environment of low heterogeneity.The Asplan Forest had three plant species in addition to those found in the REBIO Guaribas Forest.Perhaps the presence of the primate S. flavius is reponsible for the permanence of these species, through the dispersion of its seeds.One example of this is the genus Inga, consumed and apparently dispersed by S. flavius, which was found relatively frequently in the Asplan Forest, while in the REBIO Guaribas (Sema III) Forest, not a single individual of the genus Inga was found.
The pioneer plant species T. guianensis is dominant in the Asplan Forest.This species ie relatively common in fragmented areas, indicating that this forested area is in a stage of regeneration.In the Pacatuba Forest, the species D. guianensis presents a large number of individuals, while in the Asplan and REBIO Guaribas Forests, in which there are no guariba monkeys, the seeds have a mean size of 9 mm, which is close to the mean of large-seed species (10 mm).This correlates strongly with the presence of the primate A. belzebul, apparently the main dispersant of this plant, accounting for its abundance.On the other hand, the species P. heptaphyllum is more abundant in the REBIO Guaribas Forest, due to the great annual production of viable seeds by this species, which are dispersed by birds of several species, that appreciate the soft tissue surrounding these seeds (GUARIM NETO, 1991; LIMA, 2012).
In the three studied areas the primates (C.jacchus, A. belzebul and S. flavius), apparently influenced the distribution of species in all or most plots.Of the species consumed by primates, T. guianensis, P. giganteum and P. heptaphyllum are the most common species in Asplan, Pacatuba and Sema III Forests, respectively.The environmental relief of the Pacatuba Forest may also have influenced the higher diversity, due to the presence of more microhabitats in the region.Environments with a constant supply of water guarantee the presence of species that strive in more humid habitats.The occurrence of rare or uncommon species, such as Hamelia patens, Rauia resinosa, and Sarcaulus brasiliensis in the Pacatuba Forest (DIONÍSIO, 2002) is a consequence of the availability of humid environments.
Furthermore, in these environments with a larger water availability the forest becomes higher and the vegetation becomes more dense.Although the REBIO Passion-Fruit Forest also has a stream, the primate A. belzebul does not occur there.This primate species is responsible for the dispersion of large-seed plants.Its absence may result, in the long run, in the disappearance of large-seed species, and in the reduction of the oversall plant diversity in the area.

CONCLUSIONS
Pacatuba is the forest area with the highest availability of food resoruces for primates.It is also the forest with most species of large seeds and fruits.The Pacatuba and REBIO Guaribas (Sema III) Forests present the largest Beta diversity.The history of anthropic perturbations may explain the pattern of species richness observed between these two areas.The presence of large-body seed dispersants may have had an important influence on the diversity of tree species observed in the Pacatuba Forest.

Figure 1 .
Figure 1.Location of study areas, in the State of Paraíba, Northeastern Brazil.Source: National Water Agency.

Figure 4 .
Figure 4. "Box-Plot" graphs of the measurements of trees (in meters) in the three studied areas.A. Differences in height; B. Variations in diameter.

Figure 5 .
Figure 5. Species with highest abundance in individuals in the sampled areas.

Figure 6 .
Figure 6.Estimate of the total number of species relative to species effectively sampled.

Figure 7 .
Figure 7. Abundance of trees used as feeding resources by primates in the three studied areas.

Figure 8 .
Figure 8. Abundance and distribution of tree species used as food resources (predominantly fruits) by primates in plots in the three areas.

Figure 9 .
Figure 9. Mean similarity among plots in the studied areas.

( 2005 )
is due to the inclusion of liana plants and arboreal trees, whose leaves and sprouts are also consumed by primates, and to the inclusion of exotic fruit trees, such as Mangifera indica.Tabarelli et al. (2010)  state that the forest fragmentation leads to profound changes in the structure of the forest, affecting the morphology and phenology of the plant species.

Table 1 .
Differences in means and standard deviation of height and diameter of trees in the studied forests.

Table 2 .
Variation in diversity indexes in the three studied areas.
(IZAR, 2008;LUCAS;CORLETT, 1998;e primates such as the guariba monkeys (A.belzebul) in the Pacatuba Forest contribute to the dispersal of the larger seeds (> 10.0 mm), such as the plant species P. giganteum (11.8It is probable that the difference in body size among these primates determines the potential for ingestion of seeds of different sizes(IZAR, 2008;LUCAS;CORLETT, 1998; UNGAR, 1995), thus affecting the structure of the forests.For example, D. guianensis occurs only in the Pacatuba Forest and apparently represents the only seed dispersant within this forested area.
CAZETTA, 2003;avia grandis (12.0 mm)(SOUSA, 2013).Perhaps the presence of these animals are in part responsible for the greater diversity found in Pacatuba Forest, for the presence of large-seed species, and for the more homogeneous distribution of these species within the sampled plots.Frugiverous animals disperse seeds of several species, exerting a key role in the regeneration of forested areas.Primates may spit, regurgitate, defecate or simply carry fruits away from the mother-plant, enhancing the probability of survival and germination of seeds (GALETTI; ALVES-COSTA;CAZETTA, 2003; SOUSA, 2013).In the Asplan Forest we found the primates S. flavius and C. jacchus.In the Pacatuba Forest, we found A. belzebul and C. jacchus.In the REBIO Guaribas Forest only a single species was found (C.jacchus).