PE65 Behavioural changes during interspecific associations. of primate groups in the Peruvian Amazon
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1 PE65 Behavioural changes during interspecific associations of primate groups in the Peruvian Amazon Living in groups has numerous benefits for individuals, including protection from predation and access to potential mates, but also has costs such as increased competition for food resources. In species which live in groups, such as primates in the Peruvian Amazon, the benefits of group living is assumed to outweigh the costs. Whether and how these costs and benefits change when a group of primates associate with another group of primates of a different species is not well understood (Stensland et al., 2003). Interspecific associations are frequently observed between the various primate species found in Pacaya-Samaria reserve, and the most frequent of these associations is between capuchin and squirrel monkeys. Across their range, capuchin monkeys (Cebus spp) and squirrel monkeys (Saimiri spp) are found in semi-permanent foraging groups (Pinheiro et al., 2011; Levi et al., 2013). This is particularly surprising as capuchins have been observed to eat other monkey species which are a similar size to squirrel monkeys (e.g. titi monkeys Callicebus, Sampaio & Ferrari, 2005), yet very few agonistic encounters have been observed between groups of squirrel and capuchin monkeys in a field study of their associations (Pinheiro et al., 2011). The Peruvian squirrel monkey, Saimiri boliviensis spp. peruviensis, are a subspecies of squirrel monkey that are found predominantly within the Peruvian Amazon. Squirrel monkeys are diurnal, frugivore insectivores with insects accounting for up to 80% of their diet (Stone, 2007b). They are one of the smaller primates found within the reserve with an average weight of 0.8 kg (Bodmer et al., 1997) and are vulnerable to a wide variety of aerial and terrestrial predators (Stone, 2007a). Previous research on squirrel monkeys has suggested that vigilance behaviour varies with the density of understory vegetation, but found little evidence for a relationship between group size and predation risk (Boinski et al., 2003). The brown capuchin monkey (Cebus apella) are one of two species of capuchin monkey found within Pacaya-Samaria reserve. They are larger, with an average weight of 3.5 kg (Bodmer et al., 1997), so are vulnerable to fewer predators. They feed on a variety of fruits and seeds, but also prey on numerous smaller vertebrates, including other primates and frogs (Izawa, 1979). Individuals appear to be less vigilant when there are more individuals of the group within 10m (Hirsch, 2002). Other studies of capuchin monkeys have suggested that increased vigilance impacts the amount of time which is available for feeding (van Schaik & van Noordwijk, 989), thus reduced time spent being vigilant may be one of the advantages of group living for capuchin monkeys. This project looks at how the vigilance and feeding behaviour of capuchin and/or squirrel monkeys changes, depending on the degree of association with individuals of the other species. The Pacaya- Samiria National Reserve is home to both squirrel and capuchin monkeys, and they are found across six major forest habitat types: riverine, liana flooded forest, open understory forest, levees, aguajale palm swamps and treefall gaps. This site therefore provides an excellent location to understand the costs and benefits of squirrel monkey and capuchin monkey associations in a variety of habitats.
2 Methods Study site The Pacaya-Samiria National Reserve is the largest protected area in Peru, spanning over 20,000 km² of tropical rainforest and is a truly exceptional wilderness area. Situated deep in the rainforest of the western Amazon basin, the Pacaya-Samiria reserve teems with aquatic and terrestrial life. The two major rivers that bound the reserve are the Ucayali and Marañon, and they join to form the River Amazon right at the point where the reserve begins. Dissertation projects running between June and August are in the middle of the low water season, during which projects will be run at Tacshcocha, but may move to the mouth of the river depending on heights (Figure 1). Figure 1. Location of survey sites Data collection Behavioural observations will be conducted daily, starting at 6:30 AM until 12 PM, and then again from 2 PM until 5 PM. A team will enter the forest each day, to collect data on squirrel monkeys (Saimiri boliviensis spp. Peruviensis) and capuchin monkeys (Cebus apella). Once a group of the target species has been found, efforts will be made to stay with the same group for the duration of the data collection period. The GPS location of the group will be recorded throughout the day in order to record information on home range and day range. Upon locating a group, the number of individuals and agesex classification of each will be recorded where possible. The presence of other primates will also be recorded, noting the species present, the number of individuals, and where possible the age sex composition of the group. Information will be collected using two-minute individual focal samples (Altmann, 1974) which note the feeding and vigilance behaviour of a single individual using an app which can be downloaded to your smartphone before starting the project. Vigilance behaviour will be recorded using a tally of the
3 number and direction (upwards, downwards, directed at human observers) of scans performed by the individual (Table 1). When feeding, the type of food (mature leaves, young leaves, fruit, flowers, seeds, insects and gums), and corresponding plant species will be recorded where known. Where plants cannot be identified in the field, photographs and samples will be taken for later identification. For each scan, the habitat type of weather conditions will be recorded, and information about the distance to the closest conspecific and closest individual of another species will be recorded at the beginning and end of each individual focal sample. The number of individuals of any species within 10m will also be recorded. After a focal sample is completed, another individual from the same group is sampled until one sample has been taken from each individual. As vigilance and feeding behaviour can be influenced by the habitat an individual is in, habitat information will also be collected. The height of the individual in the trees, and the maximum height of the canopy will be recorded at the end of each focal sample. Height will be estimated using a clinometer to record the angle of the observer from the monkey and tape measure to record the distance of the observer to the base of the tree. Using basic trigonometry these two values can be converted to the height of the monkey in the tree. During the Operation Wallacea field season, the majority of forest surveyed is seasonally flooded forest (varzea), but within this varzea forest there are many different habitat types (Table 2). The habitat type in which the individual is located will be recorded with every behavioural scan. These data may then be used to investigate habitat preferences of each species, but also to investigate variation in activity budgets in relation to habitat type. Tree density is also recorded, and the presence of fruits or flowers in a 10m diameter around the individual. Table 1: Behavioural ethogram Vigilance behaviour Behavioural state Behaviour Looks up Looks down Looks at human Looks at another item Feeding Locomotion Resting Description Focal individual looks up. This may be a movement of gaze direction only, or a movement of the head where the chin is lifted. May be a single movement, or may continue to move head (e.g. side to side) whilst maintaining an upwards gaze. Focal individual looks down. This may be a movement of gaze direction only, or a movement of the head where the chin is lowered. May be a single movement, or may continue to move head (e.g. side to side) whilst maintaining a downwards gaze. Focal individual looks at a human. May be the observer, or another human present. Focal individual looks at another item. This may be another individual, food, or any other item apart from a human. The grasping of edible material, which the focal individual moves towards their mouth to consume. The focal individual moves, whether arboreally, along the ground or by leaping. Minimal movement of focal individual while sitting, standing or laying on the ground, branch or other substrate.
4 Other behaviours Social Out of View Call Individual <5m Polyspecific An interaction between the focal individual and one or more other individuals. Interactions can be agonistic or facilitative; include grooming, playing, learning, threats, chases, strikes, bites or movement of fur of another individuals with hands or mouth. Behaviours of the focal individual cannot be recorded as obstacles lie in the visual path of the observer. The focal individual emits any call The focal individual is within 5m of a conspecific The focal individual is within 25m of an individual of a different species Table 2: Definitions of the various forms of varzea forest in Pacaya Samiria Forest Habitat Riverine Forest Liana Flooded Forest Open Understorey Flooded Forest Levees Tree Fall Gaps Palm Swamp Description Forest located immediately next to the river, with a sloping canopy. Dense vegetation changes throughout the year relative to the flood line, through ecological succession. Populated with liana vines, often very dense with a low to intermediate canopy height. No hardwood trees are found in this habitat. Sparse sunlight penetration means there is little ground flora, but large trees and dense, high canopy. Higher concentrations of tannins within the leaves also lead to a darker colour to the vegetation, particularly fallen leaves. Falling under two main categories of Restinga, which contain broader and larger trees, and Bajial, which flood more than Restinga. Levees seasonally flood, but have a greater percentage of ground flora than other habitat types due to the higher ground levels. This also means they have a characteristically lower flood line. Dense understorey vegetation is present. Fruit species such as Taschamango are good indicators of these habitats. Areas of the forest where trees have fallen, creating a unique habitat in which the canopy has been broken and sunlight can penetrate. This leads to high percentage of ground flora. Specific species of palms are found here, as well as constant visible flooding due to bad drainage of the soil. These can be in pure (only palm species) swamps or mixed (palm and other tree species) swamps. Palms are a consistent part of the canopy. References Altmann J. (1974) Observational Study of Behavior: Sampling Methods. Behaviour, 49, Bodmer R.E., Eisenberg J.F., & Redford K.H. (1997) Hunting and the Likelihood Extinction of Amazonian Mammals. Conservation Biology, 11,
5 Boinski S., Kauffman L., Westoll A., Stickler C.M., Cropp S., & Ehmkei E. (2003) Are Vigilance, Risk from Avian Predators and Group Size Consequences of Habitat Structure? A Comparison of Three Species of Squirrel Monkey (Saimiri oerstedii, S. boliviensis and S. sciureus). Behaviour, 140, Hirsch B.T. (2002) Social monitoring and vigilance behavior in brown capuchin monkeys (Cebus apella). Behavioral Ecology and Sociobiology, 52, Izawa K. (1979) Foods and Feeding Behavior of Wild Black-capped Capuchin (Cebus apella). Primates, 20, Levi T., Silvius K.M., Oliveira L.F.B., Cummings A.R., & Fragoso J.M. V (2013) Competition and Facilitation in the Capuchin Squirrel Monkey Relationship. Biotropica, 45, Pinheiro T., Ferrari S.F., & Lopes M.A. (2011) Polyspecific Associations Between Squirrel Monkeys (Saimiri sciureus) and Other Primates in Eastern Amazonia. American Journal of Primatology, 73, Sampaio D.T. & Ferrari S.F. (2005) Predation of an Infant Titi Monkey (Callicebus moloch) by a Tufted Capuchin (Cebus apella). Folia Primatologica, 76, van Schaik C.P. & van Noordwijk M.A. (989) The Special Role of Male Cebus Monkeys in Predation Avoidance and Its Effect on Group Composition. Behavioral Ecology and Sociobiology, 24, Stensland E.V.A., Angerbjörn A., & Berggren P.E.R. (2003) Mixed species groups in mammals. Mammal Review, 33, Stone A.I. (2007b) Responses of Squirrel Monkeys to Seasonal Changes in Food Availability in an Eastern Amazonian Forest. American Journal of Primatology, 69, Stone A.I. (2007a) Ecological Risk Aversion and Foraging Behaviors of Juvenile Squirrel Monkeys (Saimiri sciureus). Ethology, 113,
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