Foraging density for squirrel monkey Saimiri sciureus in two forests in Puerto

Objective. Forest remnants were analyzed to determine the density of squirrel monkeys (Saimiri sciureus) and the degree of alteration of the forest, by selecting areas for the conservation and maintenance of the species in natural environments. Materials and methods. Linear transects were conducted on two wooden fragments, “La Reforma” and “Campo Hermoso” farms (Puerto Lopez, Meta, Colombia), recording sightings of squirrel monkeys and identifying the tree species used by the primates. Results. The fragments studied correspond to trails at the edge of water bodies with low connectivity. Highest density values were observed on the second transect of La Reforma, a possible consequence of an overcrowding phenomenon due to the high degree of isolation of the fragment. The species preferentially used as refuge and food source were: Bellucia grossularioides, Eugenia jambos, Inga alba, Mauritia flexuosa, Pseudolmedia laevis and Rollinia edulis. Conclusions. The phenology of the plant species allows for a dynamic food supply, considering the constant availability of food for the primates. Therefore, despite the evident ecological problem of these forests, it is possible to use active restoration programs to strengthen the existing dynamics and balance the biogeochemical dynamics of the ecosystem, so that socioeconomic human activities are not in conflict with conservation efforts and vice versa.


INTRODUCTION
The squirrel monkey (Saimiri sciureus, Cebidae) is a primate species with a wide distribution in Colombia.Reports for the region of Llanos Orientales indicate that they are located in the foothills of the East Andes, from 1500 m.a.s.l. to the Colombian Amazon forest and the banks of the Orinoco River (1).
Defler (1) has reported that the species occupies different types of forests, mainly gallery forests and even palm groves.Within these it frequently uses all arboreal strata for moving, foraging and refuge.
While the classification for the species by the IUCN (2) is of low risk and it is found in appendix II in the CITES, there is still a large concern in the department of Meta since this species has the highest rates of illegal capture within primates, from their natural sites to be sold as pets.Likewise, the threat of the implementation of agricultural crops, livestock activities, tourism development, human settlements and forest fragmentation has been noted (3).
In the year 1970 5,563 individuals were legally exported from Colombia to other sites of the world, illegal exports could double this number (4).Hence the need to study them in the field, in order to know their phylogeographic, ecological aspects and the composition of the habitat necessary for their survival (5).
Under these conditions, the research was developed in two forest remnants, La Reforma and Campo Hermoso farms in the vicinity of the municipality of Puerto Lopez (Meta, Colombia), I order to learn population-related aspects and the habitat of the squirrel monkey Saimiri sciureus, as a tool for the selection of areas for their conservation (Figure 1).

MATERIALS AND METHODS
Data collection.The density of the squirrel monkey in each forest was estimated using the method of linear transects of variable width (6).Two trenches were placed in each of the forest, La Reforma and Campo Hermoso, separated by a minimum of 500 m (Table 1).
The access roads, human settlements and soil uses were identified in each forest (Figure 1).A sampling point was established in each observation, which was demarcated during the walks for the estimation of density.
Se identificaron en cada bosque, vías de acceso, asentamientos humanos y usos del suelo (Figura 1).Se procedió a establecer en cada observación un punto de muestreo, el cual fue demarcado durante los recorridos para la estimación de la densidad.The journeys to the samplings sites were carried out three days a week, twice a day, at 0500 HR and at 1000 HR and between 1400 HR and 1600 HR, since the activity peaks of the squirrel monkey occur at these hours (3.7).The walks were made at an average speed of 0.5 km/hour.
The following information was recorded on each journey: perpendicular distance (P): animal detected to the transect line; radial distance (S): distance of the observer when detecting the animal (Figure 2); time of detection; distance in the transect; number of individuals and number of troops.
Statistical analysis.The size and shape of the patches, degree of isolation, scattering, interaction and heterogeneity were evaluated through digital cartographic analysis of the vegetation cover map of the IGAC (8) and Landsat images (Figure 1) in order to estimate the degree of alteration in each forest.
Each of the above named features were calculated through indexes: shape index (Di) that connects the size and shape of patches; isolation index of a patch (ri) which connects the distance between patches; isolation index of all patches (ai) which shows the degree of isolation of all patches and also the interaction index between patches (Ii), all such calculated according to the formulas proposed by Gonzalez et al (9).

Identification of flora.
The tree species used by primates and the plant composition they were feeding from (fruit, young leaves or flowers) were marked and identified using the methodology employed by Dueser and Shugart Jr (10), the species preferentially used as refuge were also identified.The height in the tree or shrub at which the animals were found and the activity carried out at the time of the observation (11) were noted in each sighting.Some trees that provided food were marked to perform phonological follow-up.

RESULTS
The forest fragments studied were limited to small trails on the edge of water bodies that, in most cases, were not even within the provisions of the Law in terms of conservation and maintenance of vegetation around streams as provided for by Decree 877/1976 issued by the Ministry of Agriculture of Colombia.The patches showed irregular shapes mainly due to the high intervention to which they are subjected in addition to the low connectivity between the same (Figure 1).In the vicinity of these forests, the land is mainly used for cattle ranching and the cultivation of African palm.In addition, in the Los recorridos para los muestreos se realizaron tres días a la semana, dos veces por día, de las 0500 HR a las 1000 HR y entre las 1400 HR y 1600 HR, debido a que en estas horas se registran los picos de mayor actividad del tití (3,7).Los recorridos fueron realizados a una velocidad media de 0.5 km/hora.

RESULTADOS
Los fragmentos de bosque estudiados se limitaron a pequeños senderos a la vera de los cuerpos de agua que en la mayoría de ocasiones ni siquiera se encontraban dentro de las disposiciones de Ley en términos de conservación y mantenimiento de la vegetación en rondas de caños tal como lo prevé el Decreto 877 de 1976 del Ministerio de Agricultura de Colombia.Los parches presentaron formas irregulares principalmente por la alta Astwood -Foraging density for squirrel monkey Saimiri sciureus proximity to the forest of La Reforma there is an hydrocarbon processing plant.
The results for the rate of encounters (ER), estimated density of the troops (DS) and density of animals per hectare in each sampling area (D) are listed in figure 3. The highest values for the three variables were observed in transect number two of La Reforma.However, it is possible that there is some overpopulation phenomenon occurring there.
Al analizar las tasas de encuentro de tropas o grupos calculados para cada zona, se evidenció una tendencia a aumentar de manera proporcional a la distancia perpendicular en metros.
Es importante destacar que durante el transcurrir del tiempo, la mayoría de especies van cambiando su estado fenológico de manera asincrónica, por tal razón, el abastecimiento de alimento para los primates es dinámico en términos de la parte de la planta disponible en una época determinada (Flor, fruto, hoja), pero constante en el sentido de que los animales siempre cuentan con algún recurso para su alimentación, que es además, relativamente abundante.When analyzing the rates of encounter of troops or groups calculated for each area, a tendency to increase in proportion to the perpendicular distance in meters was observed.
Within the alteration indices of forest fragments, the shape index (Di) showed that the fragments analyzed had an irregular shape and were far from Euclidean parameters (Table 2).In terms of the isolation between patches (ri), it was observed that the fragment where transect 1 of La Reforma is located showed the greatest separation with neighboring patches (Figure 4).
However, the isolation index of all patches (ai) showed that the area with the greatest isolation with all patches within the landscape is the fragment where transect 2 of La Reforma is located.Finally, the index of interaction between patches (Ii) allowed detecting that the fragment  of Campo Hermoso had the greatest degree of interaction with its neighboring patches when compared with other fragments analyzed.
During the walks of the transects it was found that the species preferentially used as refuge and as food source were: Bellucia grossularioides, Eugenia jambos, Inga alba, Mauritia flexuosa, Pseudolmedia laevis and Rollinia edulis (Table 3).
It is worth noting that during the passing of time, most species are changing their phenological condition asynchronously, for this reason, the supply of food for primates is dynamic in terms of the part of the plant available at a given time (flower, fruit, leaf), but constant in the sense that animals always have some resource for feeding, which is also relatively abundant.

DISCUSSION
Due to the low degree of conservation of the fragments, transects were established within vegetation strips round a body of water.Despite the fact that Buckland et al (6) recommend that transects are established perpendicularly to avoid having a bias toward the greater abundance of resources in said strips, it was not performed in this way because transects are located in open areas of grasslands where it is not possible to collect data related to the density of primates.Similarly, the area was not enough to locate the five trenches proposed, separated at least by 500 meters.
With regard to the conditions of conservation of the forests, the establishment of cattle farms in the area of La Reforma typifies the area as of high intervention with forest presence between 11-20% of the landscape and in the area of the farm Campo Hermoso, and as of low intervention with forest presence of 31-40%.Such information is consistent with what was observed in the results obtained during

Mauritia flexuosa 2 3
Pseudolmedia laevis 2 2 Virola sebifera 0 5 Xylopia aromatica 3 0 this study, being directly related to the density values obtained (Figure 3).Thus, the density of specimens per hectare in two transects of Campo Hermoso (21.6 and 29 animals/Ha) is more in line with the amounts of the available habitats than in the area of La Reforma (20.6 and 72.7 animals/Ha) if taking into account that the area of the latter is substantially smaller.

Zygia
If strictly observing the numbers of the rates of encounters and density in the area of La Reforma, especially in the transect 2, it may be possible to think that by having a density close to and/or above that of Campo Hermoso, the condition of the populations is more favorable; however, the high values for the shape index (Di), the isolation index with respect to a patch and all patches (ai) and the interaction index (Ii) (Table 2), allow observing the little connectivity of vegetation fragments in La Reforma and therefore argue that rather than a higher density of individuals per area unit, what is observed is a clear process of overcrowding due to the high reproduction capacity of Saimiri sciureus (12,13).As the gaps of small forests grow larger, there is an increase in the rates of extinction and a decrease in the recolonization by fragmentation of the habitat (14).Even under unfavorable conditions; this is a phenomenon that could trigger, in the short term, health problems within the population, with a potential risk for human beings in terms of public health The troops of primates registered in transect 2 of La Reforma showed a higher average in the perpendicular distance of troop detection, this phenomenon may be related to increased competition for resources (12) and possible stress levels that this produces on animals, which are more cautious when there are humans walking through the forest floor, therefore they keep themselves farther away.
Las tropas de primates registradas en el transecto (Flacourtiaceae), Xylopia (Annonaceae) and Zygia (Fabaceae), alternate their phenological stages, allowing the primate troops to enjoy a variety of food resources over time in Gallery forests with a lot of obstacles to predators and a adequate supply of insects, bats and lizards (15), as it occurs in agricultural landscapes (Table 3).
Coupled to this and although the graphics show, at first glance, some differences in the availability of food resources and shelter, no significant differences were found (p>0.05) in the means of any of the variables.This means that S. sciuerus uses all resources available on an equitable basis and for the results of this study there is no trend or marked preference towards any of them, neither for food nor shelter.
T h e r e l a t i o n s h i p b e t w e e n a b u n d a n c e , frequency, dominance and basal area is proportional, which indicates that all species have a significant degree of importance to the structure of the patches and each species is therefore fundamental for the maintenance of the populations of S. sciureus.
The disappearance or isolation of primates entails important consequences since in their trophic niche they are important dispersers of seeds and modify the composition and distribution of forests.In addition, they have a very important role as insect controllers (3).
The serious transformation and fragmentation processes to which the forests and ecosystems of the area have been subject to were evident during the development of this study.This aspect is a neuralgic point and must be the epicenter of the conservation efforts, i.e. the permanence and health of the species' population, not only of primates, but the rest of the fauna and flora inhabiting these forests, depends mainly on the implementation of strategies for the restoration of connectivity and the reestablishment of biological corridors that allow the networks for the transfer of energy and biomass of the system to work properly.
The size of squirrel monkey troops is positively associated with the percentage of the tree component, fruit supply, wet areas and the density of the edges in the ecotone and negatively with the presence of other primates, predators or the absence of insects (3).By preferring the secondary habitat, the mix of forests in different succession stages increases the vulnerability of the species by the presence of man and the indiscriminate use of agrochemicals.
Sumado a esto, y aunque en los gráficos citados se encuentren, a primera vista, algunas diferencias en cuanto a la disponibilidad de recursos de alimento y refugio, no se encontraron diferencias significativas (p>0.05),en las medias de alguna de las variables.
La relación entre abundancia, frecuencia, dominancia y área basal es proporcional, lo que índica que todas las especies presentan un grado significativo de importancia para la estructura de los parches y por tanto cada especie es fundamental para el mantenimiento de las poblaciones de S. sciureus.
Durante el desarrollo del presente estudio se evidenciaron los procesos graves de transformación y fragmentación a los que se ha sometido a los bosques y ecosistemas de la zona.Dicho aspecto constituye un punto neurálgico y debe ser el epicentro de los esfuerzos de conservación, es decir, la permanencia y salud poblacional de las especies, no sólo de primates, sino del resto de la fauna y flora que habita en estos bosques, depende principalmente de la implementación de estrategias de restauración de la conectividad y el reestablecimiento de corredores biológicos que permitan que las redes de transferencia de energía y biomasa del sistema funcionen correctamente.
Finally, the results obtained in terms of phenological and structural dynamics in the forest fragments under study allow establishing that despite the obvious ecological problem of these forests, it is still possible to induce nature through active restoration programs for strengthening the existing dynamics and balance the biogeochemical dynamics of the ecosystem in a relatively short period of time, so that the socioeconomic human activities already established supporting the population are not contrary to the conservation efforts and vice versa.

Figure 1 .
Figure 1.Location of the study area in Colombia and transects analyzed in the region under study.

Figure 3 .
Figure 3. Densities calculated for populations of Saimiri sciureus in the transects made.

Table 1 .
Location and length of the transects established in two forest remnants: La Reforma and Campo Hermoso.

Table 2 .
Degree of landscape alteration through the analysis of satellite images.

Table 3 .
Number of trees used as food sources and/ or refuge in the fragments analyzed.