Dissertation abstract: Synecology and seed dispersal in woolly monkeys (Lagothrix lagotricha poeppigii) and spider monkeys (Ateles belzebuth belzebuth) in Parque Naçional Yasuní, Ecuador

I studied two closely-related Amazonian frugivores, Humboldt's woolly monkey (Lagothrix lagothricha poeppigii), and the white-bellied spider monkey, (Ateles belzebuth belzebuth), to compare their roles as seed dispersers. I followed focal animals of the two species over 18 months, recording feeding behaviors, identifying food plants, and measuring the seed shadows they disseminated.  I then followed the survivorship of dispersed seeds.

The study site at Yasuní, Ecuador, has possibly the highest tree species diversity known.  The majority of these trees are fleshy-fruited and these resources support a diverse assemblage of frugivores.  The two study species are large-bodied ripe-fruit specialists with high local population densities.  The contrasting socioecological strategies of these monkeys provide an interesting study in niche separation and phylogenetic differentiation.

Both species are highly effective seed dispersers. More than 72% of their diets consist of soft, ripe, fleshy fruits, and they rarely prey upon seeds.   Although the fruit taxa eaten by the two species overlapped almost entirely, spider monkeys were significantly more likely to disperse the largest of seeds, particularly those from lipid-rich fruits.  This difference appeared to result from spider monkeys' food preferences, and from their higher likelihood of swallowing fruits whole.  Woolly monkeys were more likely to strip large-seeded fruits of their flesh, or, surprisingly, to avoid them entirely.

The two monkey species dispersed large numbers of seeds over wide areas.  Mean dispersal distances for the two were similar, approximately 245m.  Differences in the grouping patterns of the two species may prove to be as ecologically important as differences in feeding or ranging patterns.  Survivorship of primate-dispersed seeds was high.  Gut-passed seeds had an average half-life on the forest floor of 21 days, and 23% of primate-dispersed seeds germinated at simulated dispersal sites.

These results indicate that for many plants the different socioecological patterns of the two primate species produce complementary seed shadows.  It is unlikely that any other mammals provide such effective and long-distance dispersal for this diverse assemblage of large-seeded plants.  The ecological importance of these primates, particularly in light of their vulnerability to hunting, should make them excellent indicators of habitat quality wherever they are found.

Abstract:  Contrasting seed shadows of two sympatric neotropical ripe fruit specialists
Past studies have erred in assuming the seed shadows produced by different primate species to be similar (e.g. Howe 1990, Levey et. al. 1994).  In order to compare the seed dispersal roles of two sympatric ripe fruit specialists, I studied the white-bellied spider monkey Ateles belzebuth and the closely-related Humboldt's woolly monkey, Lagothrix lagothricha, at a rainforest site in Ecuador for 18 months.  Both species are large-bodied and effective seed dispersers, with more than 96% of dung samples containing large (>5mm in length) seeds, an average of 3.3 intact large seeds per sample.  Gut passage times ranged from 1 hour and 13 minutes to over 25 hours and were bimodally distributed with one mode between 2 and 3 hours and a second mode at 17 hours.  Dispersal distance averaged approximately 245 meters for both species but the range of distances (54m to 505m) was larger for A. belzebuth.  Spider monkeys, however, were also significantly more likely to deposit seeds in the "hot zone" within 15 meters of fruiting crowns (Howe 1993).  Secondary dispersal was unnecessary for successful sprouting.  Roughly 30% of the primate-dispersed seeds were in place at study's end, and approximately 50% of these had sprouted. 

Disperser effectiveness depended on two principal factors: primate population density and seed size.  Because L. lagothricha at Yasuní live at much higher densities than A. belzebuth (27.2 versus 8.4 weaned individuals per km²), they disperse more seeds, about 3193 versus 2378 seeds per hectare per year.  However, the larger the seed, the less likely L. lagothricha were to disperse them.  Woolly monkeys will not swallow seeds larger than 17mm in diameter, but spider monkeys swallow and disperse seeds as large as 27mm in diameter.  Numerous canopy trees with seed diameters over 12mm including several species of Virola (Myristicacaceae), Persea (Lauraceae), Pouteria (Sapotaceae), and others are commonly dispersed by A. belzebuth but rarely dispersed by L. lagothricha.  Thirteen percent of the large seeds dispersed by A. belzebuth are larger than 4cm³, larger than any seeds dispersed by L. lagothricha.  At this site, plants with seed diameters larger than 17mm, including Ireartea deltoidea and Oenocarpus bataua (Palmae), Iryanthera jurvensis (Myristicaceae), and Guarea kunthiana (Meliaceae) therefore appear to depend on A. belzebuth exclusively among primates for endozoochorous dispersal. 

In addition to thanking those funding agencies and individuals acknowledged in History, I would like to thank Primate Conservation Incorporated.   Jay Cablk, Carrie Linder, Audrey Schlaff, Sarah Walker, and Scott Suarez assisted with data collection.

Proposal summary

Information about this research project will be provided in the near future.

• Youlatos, D. 1999. Comparative locomotion of six sympatric primates in Ecuador.  Annales des Sciences Naturelles-Zoologie et Biologie Animale. 20:161-168. 
• Youlatos, D. 1999. Positional behavior of Cebuella pygmaea in Yasuní National Park, Ecuador. Primates. 40:543-550.

Proposal summary and preliminary results
Molecular surveys constitute a valuable tool for examining evolutionary processes at several hierarchical levels of social organization: at the individual and social group levels for assessing parentage, mating systems, kin networks, and gender bias in dispersal, at the population level for characterizing the degree of and partitioning of genetic variation within and between social groups and how this variation translates into effective plans for species conservation, and at the regional level for determining the demographic, evolutionary, and biogeographic processes that shaped a species' current genetic architecture.

For my post-doctoral work, I undertook one of the first genetic studies of wild populations of ateline primates.  I first developed a set of novel microsatellite genetic markers for three species of atelines that are found in broad sympatry across much of Amazonian South America -- woolly, spider, and howler monkeys.  These are among the first microsatellite loci characterized specifically for New World primates.  I then collected a set of tissue samples to use as a source of DNA from woolly and spider monkeys found within the Proyecto Primates site and at another research site in Amazonian Ecuador.  To do this, I used a biopsy darting technique that permits the retrieval of a small plug of tissue from an animal without rendering the subject unconscious and removing it from its social group.  I supplemented this set of tissue samples with copious fecal samples collected from the same populations.

To examine parentage, breeding system, and within-group kinship patterns, I am deriving genotypes for each sampled woolly monkey individual at eight of the microsatellite loci I designed and sequencing circa 550 base pairs of the hypervariable control region of the mitochondrial genome.  I will soon finish this process for the set of around 80 woolly monkeys for whom I have samples and hope to start on the other species shortly.

This project was funded in part by a N.S.F. Research Training Grant on the Biology of Small Populations to the University of Maryland and the Smithsonian Institution.

Dissertation abstract
I investigated ranging behavior, time allocation, foraging ecology, and social organization of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a neotropical terra firme rainforest in eastern Ecuador.  My study combined behavioral observations with phenological data on resource availability to explore links between ecological factors and social organization for this species.

Results showed that day range lengths were longer and home range sizes smaller than previously reported for Lagothrix anywhere in its geographic range.  Woolly monkeys spent 37% of their day in subsistence activity -- more than any other ateline primate. Roughly half that time was spent consuming plant items and the other half foraging for animal prey.  Woolly monkeys also spent more time moving and less time resting than other atelines.

Fruits constituted 64% to 89% of the diet each month.  Monthly fruit consumption was not correlated with the availability of ripe fruits, although the use of Spondias mombin during lean months may explain the lack of a significant relationship.  Monthly ranging behavior also was not correlated with ripe fruit availability, suggesting that the intensity of intragroup feeding competition may be low.  The fact that food patch size explained little of the variance in feeding bout duration and in feeding party size supports this suggestion.  Time spent foraging for animal prey was positively related to ripe fruit abundance, perhaps suggesting that woolly monkeys lay down fat reserves when food is abundant to sustain themselves through the lean season, instead of responding to low food availability by ranging farther or altering the proportion of fruit in their diet.

Mating in Lagothrix was promiscuous, and females often harassed copulations of other females.  In contrast, males were tolerant of matings by other males.  Nearest neighbors tended to be opposite-sex individuals: adult males seemed to avoid proximity to other males, and females with juveniles appeared to avoid other adult females.

In light of their foraging ecology, traditional explanations for grouping in terms of increasing individual foraging efficiency may not apply to woolly monkeys.  Grouping by Lagothrix females may be a strategy for insuring access to mates and monitoring potential reproductive competitors.

In addition to thanking those organizations, granting agencies and individuals thanked in History, I would like to thank Nathaniel Gerhardt and Carrie Linder for assistance in the field.  An NSF Doctoral Dissertation Improvement Grant and grants from the L.S.B. Leakey Foundation and the Wenner Gren Foundation for Anthropological Research funded this project.

• Di Fiore, A. and Rodman, P.S.  (2001)  Time allocation patterns of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a neotropical terre firma forest.  International Journal of Primatology 22:449-480.

Proposal summary
Very little is known about the parameters of fruit choice or the about nutritional composition of fruits eaten by many wild South American primates.  This represents a significant gap in our knowledge of comparative Platyrrhine foraging ecology because many sympatric species of Platyrrhines show broad dietary overlap.

During the course of a twelve-month study of the foraging ecology of woolly monkeys, I collected samples of nearly 250 species of fruits and new leaves that the monkeys were observed eating.  All of these fruits have been identified to genus or species, and the trees from which all samples were taken have been measured in trunk size (DBH) and crown height.  For each of these fruits, I recorded data on fruit weight, volume, and color, and I weighed and desiccated the parts of the fruit that the monkeys consumed for future nutritional analysis which will be undertaken shortly.

Because I found in my study that insects represented a fairly large part of the woolly monkey diet, over the next few field seasons I will be collecting samples of insects eaten to determine nutrients gained from these resources.  Additionally, and as a complement to the phenology study outlined above, I will be sampling insect densities regularly throughout the year to  document seasonal changes in insect abundance and variability.

Proposal summary

Dissertation abstract (in English)
The present thesis is the result of a study about the social behavior and diet of a group of Eastern Spider Monkeys (Ateles belzebuth belzebuth) within the Ecuadorian Primates Proyect´s study area in Yasuní National Park, Amazonian Ecuador.  This is one of the first long-term studies conducted in Ecuador with a natural primate population. This species has been studied previously in Colombia and Brazil, but without acquiring an adequate understanding of  the relationship between the spatial distribution of the resources of Ateles and their social behaviour. I addressed this question and I looked for differences among natural populations of this primate.

The objetives of this research was to increase our knowledge of the natural behavior of the Eastern Spider Monkeys, their social grouping patterns, and the plants they eat. To reach these objetives, I choose, accustomed, and followed a group which lives at the Kilometer 47 of the Pompeya Sur - Iro road, inside Yasuní National Park. I collected data on activity budgets, habitat use, composition of social groups, and diet. This information was compared with results from existing studies of this and other species of Ateles. Behavioral data were correlated with climatic variation, available habitat, and fruit production. 

One of the goals was to better understand the community ecology of primate species present at the site. The group spent their time resting (30%), feeding (25%), moving (32%), and socializing (13%). Forest types were used in proportion their availability. In terms of topography, valleys and slopes were preferred, and the monkeys tended to stay about 15 to 20 m above the ground. The group consisted of 25 individuals, including infants, with a home range of about 469 ha. The group tended to break into subgroups of 1 to 13 (mean=3.24) individuals. A quarter of the group ranged singly, while the rest formed subgroups of only males, only females, or mixed groups of both sexes. Fruit, usually eaten whole and ripe, constituted 70% of their diet. Sixty per cent of their plant foods come from trees. According to monthly feeding indices, 11 species of plants were the most important to the Ateles diet.

Proposal summary
Spider monkeys are of particular interest to behaviorists because they live in a social system unusual for primates.  In this system, all of the members of a community are rarely found in the same place at the same time.  Instead, individuals are most often found in subgroups, the composition of which change up to several times a day.  This dynamic social organization is also of interest to ecologists, as it is thought to be an adaptation to the patchy and scarce distribution of fruits, the food which makes up nearly all of a spider monkey’s diet.  The social flexibility of this so-called fission-fusion social organization is likely an adaptation that allows individual community members to avoid aggressive conflict by joining or leaving a foraging party when food abundance is low.

Despite demonstrated relationships between fission-fusion social organization and overall fruit abundance in the environment, little work has been done to understand the mechanics of how and when these fissions and fusions take place.  To understand better how and when primate communities become less cohesive, we must clarify the frequency with which subgroups change composition, how long associations last, and what ecological and social variables are responsible for subgroup changes and individual associations.  A spider monkey’s understanding of the temporal and spatial variability in fruit availability should affect the trees in which it chooses to feed, and the number of individuals with which it chooses to forage.  The highly variable nature of their food sources provides the potential for aggressive conflict between individuals of the same community, particularly when fruit abundance is low.  To avoid conflicts, spider monkeys spend time in subgroups that adapt themselves to the availability of fruit resources in their environment by being flexible in size and composition. The characteristics of the fruit patches that a monkey visits determine how many animals can feed in that patch at a time.  Because prior visits to a resource and the replenishment rate of that resource largely determine the size of the fruit crop, a spider monkey’s past foraging decisions set the stage for the number of animals with which it will associate presently. By understanding how resources vary, and whether or not spider monkeys are able to track the productivity of a fruit crop, we can begin to understand the dynamics behind when and why spider monkey groups fission and fuse.

This project aims, therefore, to investigate the impact of these ecological and social factors on foraging decisions, and consequently on fissions and fusions.  This is accomplished by two-week follows of focal individuals, which allows documentation of all fissions and fusions, and documentation of all foraging choices.  Ecological data on feeding patches and fruiting rate of particular species are also collected.  Data from this project will also be applied towards computer modeling of foraging choices, in order to determine the level of the environmental understanding of spider monkeys.

Funding for this project has come from the National Science Foundation, and from the Leakey Foundation.
 

AAPA abstract (submitted):  Quantifying fission-fusion behavior and social dynamics in free-ranging spider monkeys (Ateles belzebuth belzebuth).
Increasing numbers of studies demonstrate fission-fusion or flexible social grouping patterns in primate species.  Fission-fusion social organization is described as an adaptation to foraging problems encountered by fruit specialists, particularly for Ateles ssp. and Pan ssp.  When environmental fruit abundance is low, animals are able to avoid direct competition from conspecifics by splitting away from other group members and traveling and foraging in smaller groups.  A more precise understanding of the relationship between feeding ecology, aggression, and flexibility in social structure requires a detailed examination of the factors that influence fission-fusion events in the wild, and requires quantification of group changes for more accurate comparisons between taxa.

This project investigates the dynamics of fission and fusion events in free-ranging longhaired spider monkeys at the Yasuni National Park in eastern Ecuador.  Data were collected during ten two-week follows of focal subjects from March 1999 to May 2000.  During follows, all vocalizations, feeding bouts, aggressive interactions, and changes in subgroup composition were recorded, and fission-fusion events were described in detail.

During 1279 hours of focal contact, 265 subgroup changes were detected, 236 of which were clearly observed and described.  Subgroups changed composition 0.23 times per hour, varying from 0.01 to 0.46 per hour during follows.  Only 4% of all fissions occurred within one hour of aggressive interactions.  Over 50% of fusions occurred at feeding trees or sleeping spots. An additional 36% were the result of long-calling, and 13% occurred during travel.  While a significant association was found between aggressions and fissions at the scale of an hour (P=0.0003), rates of aggression per follow were weakly related to subgroup change rate (P=0.09, n=10).  Association matrices are analyzed to assess patterns of interaction for study animals.

These data provide a foundation for comparative study of the influence of ecological and behavioral factors on social flexibility and fission-fusion social structure.

Preliminary research prior to dissertation research is being undertaken for the summr of 2001.

Proposal summary
Information about project to be included soon.

Proposal summary
Information about project to be included soon.

Proposal summary
Information about project to be included soon.

Preliminary research 
Before developing the Proyecto Primates field site, monitoring surveys were carried out in Yasuní in 1993 and 1994.  

Current research
As requested by the Ministerio del Ambiente, Proyecto Primates will direct a project monitoring primate populations in Yasuní.  The Wildlife Conservation Society (WCS), New York, has also proposed to initiate a faunal monitoring program in the Yasuní National Park and Huaorani Ethnic Reserve.  We have collaborated with WCS in the design of our monitoring programs to maximize the information to be obtained in our studies, and, if possible, WCS and Proyecto Primates personnel will jointly participate in conducting faunal cenuses on the transects of each project. 

• Proposal summary (Di Fiore and Rodman):  Ecology, behavior, and population structure of the primate community of the Ecuadorian Oriente and long-term monitoring of the population status of primates and other fauna in Yasuní National Park and the Huaorani Ethnic Reserve.

Assessment of the current state of faunal populations, and continued monitoring of these populations over the upcoming years, is thus essential to the development and implementation of management strategies for Yasuní National Park, particularly in those regions nearest to human influences.  Indeed, monitoring large-bodied primates and other faunal populations in Yasuní has recently been assigned a national priority by the Ecuadorian government in the Management Plan for Yasuní National Park, 1998.  We plan to initiate a long-term study to monitor faunal population densities throughout Yasuní National Park/Huaorani Ethnic Reserve, particularly of large-bodied primates and other large game species which are important elements in the diets of many indigenous groups and are the preferred targets of subsistence hunting.

In order to assess the impacts of human hunting pressure on faunal populations, it is essential to conduct population censuses in regions facing a range of human hunting pressures; thus our proposed monitoring compares faunal population densities at sites within Yasuní National Park/Huaorani Ethnic Reserve that are subject to varying degrees of human hunting impact.  We will use distance from human settlement areas and distance from locations of human activity, such as roads and heavily trafficked trails and rivers, as an indirect index of hunting pressure.  A total of 10 sites will be selected for faunal surveys along the Pompeya Sur - Iro petroleum road.  At each site, we will establish a 5 km straight line transect that will be marked with flagging tape every twenty five meters.  Transects  will run perpendicular to the direction of the road and start 100 m into the forest from the road margin.

Transects will be walked twice per year (beginning Summer 2000) by trained censusing teams for an initial study period of five years.  Census methodology will follow the basic techniques used to assess the impact of human subsistence hunting by Ache hunter-gatherers in the Mbaracayu Reserve, Paraguay (Hill et al. 1997).  The technique is a variant of standard line transect censusing that capitalizes on indigenous knowledge of animal sign to augment the data amount of information gained in surveys over that provided by direct animal encounters alone.  Census teams will consist of a professional biologist who will act as a data recorder and three indigenous field assistants who will act as observers.  Observers will walk in parallel through the forest along the transect line, spaced approximately 25 meters apart, at a rate of 1.5 km per hour between the hours of 0600 and 1000. 

Observers will record all encounters with all fauna (primates being a subset).  Two types of encounters will be recognized: direct (animals seen, heard, or found in their burrows) and indirect (encounters with fresh animal sign such as tracks, scat, or evidence of feeding activity).  For each direct encounter, observers will record the following data:

• Distance along the transect from the starting point at which the observer detected the animal
• Distance between the observer and the animal encountered at the moment of detection (for social species, detection distances and angles will be recorded to the nearest group member, and observers will attempt to record group size and composition and to estimate group dispersion)
• Angular direction of the encountered animal relative to the transect when detected
• Forest type around the encounter site
• Sex, age, and reproductive status of the encountered animal, if possible

• Hill, K., J. Padwe, C. Bejyvagi, A. Bepurangi, F. Jakugi, R. Tyukuarangi, and T. Tyukuarangi.  1997.  Impact of hunting on large vertebrates in the Mbaracayu Reserve, Paraguay. Conservation Biology 11: 1339-1353.

Summary based on Di Fiore's dissertation
To obtain an estimate of the density and distribution of plant resources available to primates in the Yasuní forest, we studied forest composition and phenology using a set of trees located within five 10 x 1000 meter belt transects placed randomly throughout the Proyecto Primates study area.

The mean density of trees per hectare in these transects was 586.8 individuals, with a standard deviation of 58.0, and to date, approximately 75% of the transect trees have been identified to the level of genus or species. These trees belong to at least 55 families and 173 genera.  Over 80% of transect trees were less than 25 cm in DBH and only 3.6% were larger than 50 cm.  Only 7.4% of all transect trees reached heights greater than 25 meters.

Roughly half of the trees on the transects (1492 trees in 2.5 hectares) were monitored each month between March 1995 and April 1996 to determine phenology.  Each crown was visually inspected to quantify the presence and abundance of new leaves or leaf flush, flowers, and fruits in either the crown itself or in any associated epiphytic plants.

Fruit abundance was high during March and April 1995, declined to a low in July 1995 to September 1995, then rose again starting in October 1995 before beginning to decline again in February 1996.  The availability of new leaves and flowers peaked during the period of lowest availability of ripe fruits.  Although there was no clear relationship between rainfall and the abundance of either leaves, flowers or fruits, the period of lowest ripe fruit abundance (and maximal new leaf abundance) coincided directly with the two driest and hottest months of the year.

In addition to those mentioned in History, the authors would like to thank Else Mågard, Jens-Christian Svenning and especially Robin Foster and David Neill for assistance in identification of the plants.
 

Current research
A modified version of the previous methods will be used to collect data on fruit availability during between July 2001 and Junly 2002.  Two research assistants will be helping Anthony Di Fiore with this project:  Renee Bauer and Jamille Heer.  Furthermore, data on insect availability will also be collected. 

Dissertation abstract
Following a pilot study at the Proyecto Primates field site in 1996, I conducted a two-year study of golden-mantled tamarins, Saguinus tripartitus, at the Tiputini Biodiversity Station from September 1997 to September 1999. The primary aim of this study is to provide an overview of the social behavior and ecology of golden-mantled tamarins. 

During the two-year study, I followed three habituated groups and collected data on several aspects of this species’ natural history and behavior, including the following: 1) group size and composition, 2) home range size and patterns of home range use, 3) diet and foraging behavior, and 4) patterns of social interactions, reproduction, and helping within groups. This information is important for establishing the extent to which this previously unstudied species resembles and differs from other tamarin species, including its well-studied and closely-related congener, S. fuscicollis.  Investigations of previously unstudied callitrichid species such can reveal novel combinations of traits which would provide opportunities to test hypotheses about the ultimate and proximate relationships between ecology and the distinctive features of social organization that characterize callitrichids and other cooperatively breeding vertebrates.

Note: The Tiputini Biodiversity Station, or the field site used for this study, is two hours down the Tiputini River from the Estación Científica Yasuní.  This site, unlike Proyecto Primates, is adjacent to a major river and is composed of seasonally-flooded lowland forest, palm swamps, and other wetlands.

The long-term goal of Proyecto Primates is to study the behavior and ecology of all ten species of primates that live within the field site.  Potential avenues of research currently being considered include mixed species foraging strategies by squirrel and capuchin monkeys, titi monkey genetic dispersal and genetic mating systems, squirrel monkey genetic mating system, and woolly monkey subspecific phylogeny.  One goal in the short term future is to either develop or encourage proposals of scientific projects on all species.