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15 Comparisons of population density and group structure for the variegated spider monkey (Ateles hybridus),

Serranía de San Lucas (Bolivar)

Comparaciones de la Densidad Poblacional y Estructura Grupal de la Marimonda Café o del Magdalena (Ateles hybridus), Serranía de San Lucas (Bolivar)

Néstor Roncancio, Karem Gómez-Cadenas, Fredy Quintero

ABSTRACT

The brown spider monkey, Ateles hybridus, found in both Colombia and Venezuela, is classified as Critically Endangered in the IUCN red list and is one of the 25 most endangered primates in the world. Little is known about the species’ natural history, its population trends or its response to habitat fragmentation. The main objective of this study was to estimate population density and compare the results with those from other sites, and to determine the group structure of A. hybridus at a point where the deforestation front meets continuous forest in the Serranía de San Lucas, in southwest of Bolívar department, Colombia. From May to September 2010 line transect distance sampling was used to estimate population density. Data were analyzed with DISTANCE 6.0 software. Population densities of 32 individuals/km2 (IC95%=19.3-52.9) and 10.5 groups/km2 (IC95%=6.6-16.7) were obtained. The population density of A. hybridus at the Serranía de San Lucas was not significantly different from other locations. The adult sex ratio (M:F) was 1:1.63, while the female-immature ratio was 1:0.45. The mean subgroup size, 3 individuals (IC95%=2.4-3.7), is similar to other reports for the species. This size corresponds to the fission-fusion social organization system characteristic of the genus. The study area is probably the most preserved area where surveys of A. hybridus have been done in the last 30 years.

Key words: Ateles hybridus, fragmentation, population density, Serranía de San Lucas

RESUMEN

La marimonda del magdalena, Ateles hybridus, está distribuida en Colombia y Venezuela; se encuentra categorizada como especie en Peligro Crítico (CR) según la UICN y es una de las 25 especies de primates más amenazadas del mundo. Se conoce muy poco acerca de la historia natural, las tendencias poblacionales y la respuesta a la fragmentación de esta especie. El objetivo principal de este estudio fue estimar la densidad poblacional de esta especie en un frente de deforestación de la Serranía de San Lucas (Sur de Bolívar, Colombia), compararlo con otros estimados y determinar su estructura de grupo. Durante 5 meses (entre mayo y septiembre del 2010) se empleó el método de muestreo a distancia con transectos lineales para estimar la densidad poblacional. Posteriormente, los datos fueron analizados con el programa

Roncancio, N., Gómez-Cadenas, K. & Quintero, F. (2013). Comparisons of population density and group structure for the variegated spider monkey (Ateles hybridus), Serranía de San Lucas (Bolívar). En: T. R. Defler, P. R. Stevenson, M. L. Bueno & D. C. Guzmán-Caro

(Eds.), Primates Colombianos en Peligro de Extinción, (pp. 235-248). Asociación Primatológica Colombiana, Bogotá D. C.

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DISTANCE 6.0. Se obtuvo una densidad poblacional de 32 individuos/km2 (IC95%=19.3-52.9) y 10.5 grupos/km2 (IC965= 6.6-16.7). La densidad poblacional de A. hybridus en la Serranía de San Lucas no fue significativamente distinta a la de las otras localidades. La proporción entre machos y hembras adultas fue de 1:1.63, mientras que la proporción de hembras adultas e inmaduros fue de 1:0.45. El tamaño promedio de subgrupo de 3 individuos (IC95% = 2.4-3.7) es similar al registrado para la especie en otros estudios. Este tamaño corresponde al sistema de organización social fisión-fusión característico del género. El área de estudio es probablemente una de las zonas prioritarias para la conservación de esta especie.

Palabras claves: densidad poblacional, estructura de grupo, fragmentación, Ateles hybridus, Serranía de San Lucas, muestreo a distancia con transectos lineales

INTRODUCTION

Populations show temporal and spatial variations according to resource availability or environmental factors (Davidson y Andrewartha, 1948; Turchin, 1995; Rudran y Fernández-Duque, 2003; Begon et al., 2006). These variations are mainly reflected in changes in birth and survival rates (Smith y Smith, 2006). When a population is negatively affected by events that diminish its growth rate, population size is a crucial factor that can determine its probability of extinction (Miller y Lacy, 2003; Rockwood, 2006); because large populations can recover more easily than small populations (Shaffer, 1981; Rieman y Allendorf, 2001). The loss of genetic diversity due to genetic drift and endogamy is a potential cause of extinction in small populations, reducing a population’s ability to adapt to new diseases, predators and environmental changes (Wright, 1929; Estrada y Coates-Estrada, 1996; Grativol et al., 2001; Chapman et al., 2005; Futuyma, 2006; Hartl y Clark, 2007; Kliman et al., 2008). Also, the social structure of species with complex behavior can break down, altering patterns of mating, foraging and defense against predators (Storz, 1999; Dobson et al., 2004). At the same time, in low density conditions declines in reproduction and survival would be expected due to the Allee effect (Allee, 1931; Courchamp et al., 2008; Somers et al., 2008).

Given its body mass (7-9 kg), diet (up to 85% of their diet is ripe fruit), population density (9-30 ind./km2), reproduction (1 birth every 3-4 years), activity patterns (1.5-3.5 km traveled per day) and home range (60-350 ha), the brown spider monkey Ateles hybridus is an extremely vulnerable species to the loss, reduction and fragmentation of its habitat; moreover, it is a key species for ecosystem functions (Chapman y Onderdonk, 1998; Stevenson et al., 2002; Defler et al., 2003; Link y Di Fiore, 2006; Takahashi, 2008; Urbani et al., 2008; Palacios et al., 2009; Defler, 2010).

Ateles hybridus is a species that is found both in Colombia and Venezuela (Defler, 2010). Its Colombian distribution extends from the lower Cauca river region and the Magdalena river to the Eastern Cordillera on the frontier with Venezuela, where it continues along the Cordillera (Hernández-Camacho y Cooper, 1976; Defler, 2010) and its original habitat is highly fragmented (Defler et al., 2003). Of the 164.463 km2 of potential distribution area

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for the species, just 18.8% still has forests remaining and only half of this area is continuous forest. Of this remaining area, just 0.67% is in National Natural Parks (Morales, 2004) (Fig. 1). For this reason, A. hybridus is categorized as Critically Endangered (CR) (Urbani et al., 2008) and as one of the 25 most threatened primates in the world (Mittermeier et al., 2009). In Colombia the species resides in two separate populations on either side of the Magdalena River. The two populations represent two different subspecies: A. hybridus hybridus on the right bank and A. h. brunneus on the left. Although both subspecies are Critically Endangered, A. h. brunneus is most at risk because, besides the common threats to both subspecies, brunneus´ area of distribution is small and no national protected areas contains confirmed populations of this endemic Colombian primate.

Figure 1. Study site. The location of the study site and other studies compared is represented with black dots. Only 0.67% of the actual distribution area of Ateles hybridus is protected in National Natural Parks.

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To make decisions about the management and conservation of A. hybridus, it is necessary to know the current status of the remaining populations and the factors that affect it. However, there are few studies and no conservation programs in Colombia for this primate (Defler, 2010). In the Serranía de San Lucas just two surveys of the population density of the species have been done (Bernstein et al., 1976; Green, 1978), and these date back more than thirty years. Since then, no research on the species was carried out until the beginning of the last decade (Morales, 2004; Díaz-Cubillos, 2007; Guerrero, 2007; Aldana et al., 2008; Ramírez, 2008; Alfonso, 2009; Arango, 2009; Roncancio et al., 2010a, 2010b). These studies revealed that the situation of A. hybridus is even more critical than thirty years ago. Some of the populations studied are virtually condemned to extinction, because they live in small isolated patches with limited possibilities of genetic flow and low population numbers. In this study A. hybridus was found only in undisturbed continuous forest, making clear the species’ vulnerability to fragmentation.

Despite this recent research, there is still widespread ignorance in Colombia about the abundance and other ecological aspects of A. hybridus under natural conditions. All of this contributes to an urgent need to consolidate background knowledge in order to develop an adequate management and conservation plan for this primate. It is, therefore, necessary to carry out more surveys, continuing and complementing the research started a few years ago. Here we report the population density and group structure of A. hybridus at a deforestation front in the Serranía de San Lucas. Our density estimate was also compared with the results of other surveys of the same species in different sites, with different types and levels of pressure.

METHODS

Study SiteThe Serranía de San Lucas, approximately 180 km long, is largely covered by tropical rain forest (Holdridge, 1967; IGAC, 2002), although satellite images indicate wide-spread forest clearing to the North-East, East and South-East inland from the Magdalena River. Geographically it includes a mountainous region limited to the east by the central channel of the Magdalena River, to the west by the central channel of the Cauca River, to the south by Antioquia department and to the north by the “Brazo de la Loba” of the Magdalena River. The area evaluated includes 260 ha of forest located in the northwest corner of the Serranía (8°20’N 74°07’W). The site is located in near the village of Juan Sobrino, municipality of Achí, Bolivar Department (Fig. 1). The altitude of the study area is between 14 and 800 m above sea level, the mean annual temperature is 25.7 ºC, the mean relative humidity is 80% and annual rainfall averages 3116 mm with a monthly average of 259.9 mm (Hijmans et al., 2005).

The forest has a mean height of 13.64 m (σ = 6.681) and a mean DBH of 27.4 cm (σ = 19.52 cm) and is dominated by plants of the families Urticaceae, Malvaceae, Anacardiaceae, Euphorbiaceae and Moraceae. The most abundant species are Boehmeria sp., Heliocarpus sp., Spondias mombin, Trichospermun mexicanum, Calatola costaricensis, Ficus sp. and

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Sapium sp. (Roncancio et al., in preparation). Severe fragmentation begins a few kilometers east of our study site, dominating floodplains of the Magdalena River.

Population densityThe population density of A. hybridus was estimated using the line transect distance sampling method (Peres, 1999; Buckland et al., 2001). The field work was carried out between May and September 2010. Pre-sampling was carried out before the beginning of the survey, during which reconnaissance of the terrain was undertaken, 16 line transects were cut and observers were trained. The total length of the transects was 8.5 km (mean length 532.7 m; SD ± 122.3). Transects were walked 15.7 times on average, accumulating a 133.5 km sampling effort. In the surveys only direct visual records were taken into account. Transects were walked between 7:00 and 12:00 hours and 14:00 and 18:00 hours following Peres, 1999, using 10x50 zoom binoculars. Each transect was walked by one person silently at an average speed of approximately 0.5 km/h (Estrada y Coates-Estrada, 1996; Krebs, 1999). When an individual or a group was detected, the perpendicular distance from the transect was measured and the individuals were counted, recording age class (adults, sub-adults, juveniles and infants), and the sex of adults and subadults (Defler, 1981; Peres, 1999). Observers waited at least one hour after walking a transect before returning along the same transect. The assumption was that one hour is enough time for the primates to distribute naturally in the forest. This method has no direct impact on the animals we were studying because registered data is from sightings only. There is a risk of villagers hunting along the same transects, however, the transects were very thin and the forest was quite dense. We actually had to clean some transects again because the plants grew very fast. There was no evidence of hunting while we were there.

Data analysisThe population density was estimated with DISTANCE 6.0 (Thomas et al., 2010). The analysis was run with a database containing the transects, the total sampling effort for each transect (m), the perpendicular distances (m) and the number of individuals counted during each observation of primates. The goal of distance sampling analysis is to fit a detection function to the perpendicular distances and to use this function to estimate the proportion of objects not detected during sampling. This way, real density value and object abundance in the sampling area can be obtained (Thomas et al., 2002).

In order to find the best fit detection function, the distribution of frequencies of the perpendicular distances were compared with six models:1. Half normal cosine, 2. Half normal Hermite polynomial, 3. Uniform Cosine, 4. Uniform Simple polynomial, 5. Hazard-rate Cosine and 6. Hazard-rate Simple polynomial. From the above models the model with the lowest value for the Akaike Information Criterion (AIC) was chosen. AIC is a quantitative method for the selection of the model best fitted to the data and that employs the least number of parameters (Buckland et al., 2001). The sample variance of population density was calculated empirically as the sum of the sample variances of encounter rates, estimated probability of detection and group size (Buckland et al., 2001).

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The population density of this study was compared with density values from other localities. The original data supplied by the authors were treated in the same way as the data from this study. Comparison of population densities was made graphically using confidence intervals. When confidence intervals overlapped more than 25%, we considered that there was no evidence to support significant differences in population densities with a confidence level of 95% (Cumming et al., 2007).

RESULTS

Population density and comparisons to other sitesFifty-seven records of A. hybridus were obtained during this survey. The perpendicular distance frequency distribution showed a better fit to the uniform model with cosine expansion series. The estimated population density of A. hybridus in the survey area was 32 ind/km2 (IC95%=19.3-52.9) and 10.5 groups/km2 (IC965= 6.6-16.7), with coefficients of variation of 25.26% and 22.76% respectively. The component that most contributed to the variance of the density was the encounter rate (61.1%), followed by detection probability (20%) and group size (18.9%). There were no significant differences, with a confidence level of 95%, between the population density of A. hybridus in the Serranía de San Lucas with those estimated in other surveys (Table 1, Fig. 2).

Ateles hybridus group structure The mean group size was three individuals (IC95%=2.62-4.09). The female-male ratio was 1:1.63 and the female-immature ratio 1:0.45 (Table 2).

Table 1. Comparison of A. hybridus population densities.

DISCUSSION

The population density found in this research – above 25 ind/km2 - could be considered high (Weghorst, 2007). However, density reports from Ateles species show great variability (Table 3). Most of these studies were done using line transect surveys, but without

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including the detection probability in their analysis. The probability of detecting a monkey is therefore one, regardless of the distance from the transect. Also, many of these studies ignore two basic principles of these surveys: replication and randomization. The design often comprises too few lines (sometimes just one), subjectively placed or placed along trails (Buckland et al., 2010). Because of this, it is difficult to compare the population density obtained in this study with previous data for Ateles.

Figure 2. Comparison of A. hybridus population density confidence intervals. All the confidence intervals overlap at least 25% with the confidence intervals of this study. No significant differences were found.

Table 2. Population composition.

The study area was connected to the continuous forest of the “Serranía de San Lucas”, which extends more than 180 km. Even though this is a zone of deforestation, the area is mostly mature and continuous forest. Other forests differ in several ways from the “Serranía de San Lucas” forest. The shape of the “San Juan del Carare” forest is very thin, so primates

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are exposed for most of its 65 ha extent. In the “undisturbed” forest (Aldana et al., 2008) human activities are not controlled and hunting sites were detected. On the other hand, “logged” forest (Aldana et al., 2008), “Hacienda Monterrey” forest and “El Pajuil” forest (Roncancio et al., 2010a, 2010b), hold high population densities of Ateles despite being very small and isolated fragments. The fact that they are private properties could have a positive impact on the persistence of the monkeys in these crowded fragments. But high densities in small, isolated forests might also be due to refugees from other, now destroyed forests. With so few studies of the population density of these animals, it is difficult to detect the tendencies associated with these diverse habitat features.

Table 3.Comparison of Population Densities of Ateles Genus determined by use of line-transect surveys. Sources: Weghorst (2007), Roncancio et al. (2010b).

AI = All individuals; ILI = Independently locomoting individuals.

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Population density of A. hybridus in the Serranía de San Lucas was not significantly different from other sites (Fig. 2). This result could be caused by the high values of the coefficient of variation for all sites (>10%) (Roncancio, 2009, Table 1). In this study, the component that most contributed to the variation in population density was encounter rate at 60%, i.e. the encounter rate varied among transects. Encounter rate can vary for many reasons, especially in a large area such as that evaluated here. The area has a hilly topography with many slopes and cliffs, which make it even more diverse. In addition, the vegetation is heterogeneous, so that the supply of food for the spider monkey is different throughout the area. Spider monkeys are animals with very complex behavior, their habits do not conform to easily predictable tendencies, and the conduct of the group can be diverse (Takahashi, 2008; Defler, 2010); because of this, they frequent some places more than others and sightings will be higher along certain transects. To reduce the variability in encounter rate, it would be necessary to increase the number of samples (transects) (Buckland et al., 2001; Morris y Doak, 2002; Thompson, 2002; Roncancio, 2009). On the other hand, the similarity of the density values at sites with different characteristics may reflect tolerance of this species to certain levels of disturbance, for example, by using a strategy of hoarding resources previously available for other species. In this context it has been found that other primates such as the white-footed tamarin Saguinus leucopus have lower densities at sites where they coexist with Ateles than at sites where this spider monkey is locally extinct as a result of, for example, high hunting pressure (Roncancio et al., 2011).

The sex ratio between adult male and females was 1:1.63, which is similar to ratios for A. hybridus reported in other studies (1:2.57 - Guerrero, 2007; 1:1.14 -Alfonso, 2009), but higher than the 1:0.67 found by Roncancio (2010a). However, Symington (1990) and Chapman (1990) mention that the normal sex ratio in the genus Ateles is about three females for each male, so according to these two authors, apart from Guerrero (2007), the proportions of females are very low. On the other hand, the ratio of adult females to immature (juveniles and infants) was 1:0.45. According to Heltne et al., 1976, this population would therefore not be expanding. However, only with long term studies can the direction of population growth or decline be determined because fluctuations can occur over the year due to variations in birth or survival of juveniles (Struhsaker, 2000). The mean cluster size was three individuals (IC95% = 2.4-3.7), which is similar to other records for the species (Bernstein et al., 1976; Coelho et al., 1976; Cant, 1978; Estrada et al., 2004; Green,1978; White, 1986; Gonzalez-Kirchner, 1999; Ramos-Fernández y Ayala-Orozco, 2003; Guerrero, 2007; Alfonso, 2009; Arango, 2009) and genus (Klein, 1972; Izawa, 1976). This size is consistent with the fission-fusion social organization system very typical of the genus, in which large groups form and then split into smaller groups or clusters that change constantly in size and composition (Symington, 1990).

Although, there are no formal studies for this species concerning human pressures, it is probably one of the most preserved zones in which studies of A. hybridus have been carried out in the last thirty years. Despite the variability of the data from all other studies, no differences between densities were found. Given that the sizes of the patches in the other studies were about 21 and 65 ha, that most of them were isolated, and that there has been a history of disturbance, population densities of A. hybridus in the “Serranía

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de San Lucas” would be expected to be a little lower because, according to the crowding phenomenon (Defler, 1981), these animals should be less concentrated in a location that is not very fragmented. Nonetheless, in many studies high density values in continuous forests have been found for Ateles (Table 3). The density of 32 ind/km2 in this study can be attributed to the diversity of habitats and the floral composition of the area (Wallace et al., 1998). This density value is consistent with the 33.3 ind/km2 that Green (1978) estimated for A. hybridus in the Cerro Bran, in the northern part of the Serranía de San Lucas. This value is also similar to the 32.1 ind/km2 estimated by Wallace et al., (1998) for A. paniscus (probably A. chamek) in the Noel Kempff Mercado National Park in Santa Cruz, Bolivia.

Population density is a dynamic parameter that varies in time and space (Coulson et al., 2001; Rudran y Fernández-Duque, 2003). With an evaluation made at few sites at just one point in time, we cannot be conclusive about trends in these populations (Roncancio, 2009). The density values from this study and Green’s (1978) do not allow us to make inferences for the whole Serranía de San Lucas forest. However, this region holds good proportions of native forest and has an area of more than 6000 km2. If similar densities are assumed for the entire forest, this zone probably provides habitat for the largest populations of A. hybridus throughout its range. For this reason, is necessary to carry out more studies of this kind in the Serranía de San Lucas and the rest of the species’ distribution in Colombia, to be able to assess population status in the forests and take appropriate conservation action. Currently, National Natural Parks of Colombia are managing a new protected area in this region. This information could be used to support this initiative.

Acknowledgements

This work was possible thanks to funding and logistic support of WCS Colombia, Woolly Monkey Foundation and Margot Marsh Biodiversity Foundation. We thank Sergio Solari for his comments during the process. Thanks to Ana María Aldana, Felipe Alfonso Cortés, Lina García y Amilvia Acosta, for sharing their data with us. Thanks to Jaime Cerro for allowing us the access to the Serranía de San Lucas and his family farm. Thanks to Mrs Lola, Mr. Ismael, Mrs Esperanza, Mañe and other Juan Sobrino people who constantly helped us during the fieldwork. Thanks to Rosana Londoño for her reviews and support upon finishing this field project.

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