Wooly Monkey Behavior and Vocalizations

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Vocalizations & Displays in the Common Woolly Monkey

(Lagothrix lagothricha)

Lindsey Hughes

Abstract

Two troops of captive woolly monkeys were observed with the aid of an 8 mm video camera and a proprietary Palm Pilot program. My research up to the present will be continued, but with modifications in equipment and methods of data. The two troops differ since Troop I consists of a family group with four members; the breeding male Corey, his son Tomas and daughter Sara, and a non-breeding female named Sissi who is the Corey’s sister. The mother of Tomas and Sara died while giving birth to Sara. Troop II consists of three unrelated males, with two more unrelated males who are currently in isolation to be introduced in the near future. Troop I is one of only two captive family troops of woolly monkeys in the world; the other is located in London, England.

The video recordings were analyzed frame-by-frame using a proprietary video digitization program. The vocalizations were recorded by the video camera as well and analyzed using Sound Forge to make sound spectrographs, or sonograms. A programmed Palm Pilot was used to record the movement and behavior of both troops in order to make ethograms to display patterns of behavior and vocalization.

The following was anticipated: 1. vocalizations would be correlated with visual displays; 2. display function would be identified through context; 3 individuals would be identified through harmonics in the sonograms; 4. the behavior and vocalizations of the two troops would differ; and 5. the behavioral analysis would be useful for maintaining and breeding captive troops.

Introduction

The common woolly monkey (Lagothrix lagothricha), also known as Humboldt's woolly monkey, is found only in South America in the Amazon River Basin of Brazil, Colombia, Ecuador, Peru, and Venezuela. They range in all canopy levels of primary rainforest as well as gallery forests, and have been found in mountainous areas and cloud forests up to 3,000 meters. The classification of the common woolly monkey is as follows:

Taxon | Classification
Kingdom | Animalia
Phylum | Chordata
Class | Mammalia
Order | Primates
Suborder | Haplorrhini
Family | Cebidae
Subfamily | Atelinae
Genus | Lagothrix
Species | lagothricha

The morphology of the common woolly monkey is similar to that of other monkeys in the Atelinae subfamily. The woolly monkey is the largest monkey in South America, with the female weight averaging 11 pounds and the male weight averaging 15 pounds. They have a prehensile tail that can support their full weight and is used for feeding and locomotion. Woolly monkeys can have dark brown, pale brown, dark gray, pale gray, reddish-brown, or black fur. The limbs, tail, and head are usually darker than the back, with the face being black and the palms of the hands and feet being pink. Slight sexual dimorphism exists including the canines, body, and head in the males being longer than females. However, the female's tail is longer than the male's and the female's clitoris is longer than the males' penis, which sometimes makes it difficult to determine the sex in the wild.

Humboldt's woolly monkey is primarily frugivorous, but they also feed on leaves, seeds, flowers, and some invertebrates and small mammals. In captivity they have been known to prey upon birds that fly into their cages. The group size for woolly monkeys averages 10-12 group members, but much larger groups are known to exist. Subgroups sometimes form and travel independently from the larger group. Woolly monkeys are not territorial and allow group ranges to overlap and have been known to forage alongside each other as well as other species in their family. The woolly monkey travels through the forest quadrupedally using its tail as a fifth arm. They rarely come down to the ground and, therefore, are known to be almost totally arboreal. They even sleep 150 feet above the ground in the canopy. When on the ground, which is especially rare in the wild, they walk bipedally, using their arms and tail to balance. The tail is extremely important and is always anchored to something; it is used to pick up objects and sometimes even allows the monkeys to rest by hanging from just the tail.

The social structure of the common woolly monkey is a multi-male-multi-female group in which a hierarchy exists between the males in the group. The dominance hierarchy is determined by play-fighting and age. The species' mating system is polygamous because each receptive female mates with every male in the group, with the most dominant males receiving the most copulations. Because of this, the male that succeeds in passing on his genes is the one that releases more and better-fit sperm per session, with multiple sessions increasing the likelihood. Therefore, every male mates with every female, but only one female is copulated with at any given time. In addition to receiving the most copulations, the most dominant males also receive the most social grooming and are known to protect mothers and their infants from others in the group. In general, adult and subadult males are dominant over all other members in the group.

Male woolly monkeys are philopatric, which means that the males stay in the group in which they were born, known as their natal group, while the females leave their natal group. Female dispersion usually occurs between the ages of five and a half years to six years, the same ages that females begin to mate. Although females begin to mate between those ages, they remain sterile and do not conceive until one to three years after they leave their natal groups. The gestation period averages seven and a half months, or about 223 days, and the female gives birth to one young about every two to three years during the birthing season, which occurs between the months of August and December. After birth, the infants nurse from sixteen to twenty months, traveling independently by six months.

Little research on woolly monkeys exists, with the majority of the research focused on ecology, morphology, location, social structure, and so on. Research on the behavior and vocalizations of the common woolly monkey is almost completely nonexistent. The research on woolly monkey behavior and vocalization that has been done was performed by M. Ramirez and published through the World Wildlife Fund in 1988. His research was made into a "dictionary" that explained the behavior or reason behind each vocalization, which he spelled out using human phonetics. He also explained some of the woolly monkeys' visual communication. Although thorough in some respects, his research did not investigate sequences of behavior and vocalization or analyze each individual separately with respect to behavior and vocalization sequences.

Methods

My research on the common woolly monkey was conducted at the Louisville Zoo, one of only two places in the world that have a captive family troop. After being formally introduced to the monkeys by the head veterinarian, I was able to begin collecting data. Before starting the data collection process, I decided to spend a few weeks observing the two troops in order to become acquainted with the individuals. During the three weeks of strict observation, I took notice of each behavior and began compiling a list of the observed behaviors. This list is located in the results and discussion section. I also realized that not only could I tell the monkeys apart visually, but vocally as well. After becoming familiar with the behaviors (displays) and vocalizations of the monkeys, I began collecting data.

The data collection consisted of a variety of methods including the use of an 8 mm video camera to record behaviors, a mini disk recorder to record the vocalizations, and a proprietary Palm Pilot program to record the movement and behavior of each individual in the two troops as well as the overall behavior of each troop. At first, I videotaped the woolly monkeys individually. This method was not effective because the behavior of the other woolly monkeys could not be seen and the monkeys move extremely fast and it is difficult to follow them around the cage. I then tried to videotape sections of the cage, but that did not work well either because I could not differentiate between the monkeys because of the camera’s bad resolution. After four hours of recording over one month, I realized that I needed a much better video camera in order to continue with the research. For my future research I will have a video camera with superior resolution. The video recordings that I had were used to learn and practice the digitization process. The recordings were digitized and transferred to compact disk for later analysis. The digitized version of the video recordings could be analyzed at 1/10 of a second, with the potential advantages including the ability to record the behavior at set intervals, allowing the viewer to record the behavior of all the monkeys in view.

The mini disk recorder was used in conjunction with the video camera. I experienced multiple difficulties and problems with the mini disk recorder that eventually led me to discontinue using it in this project. This will be discussed further in the results and discussion section. Because I did not have any vocalizations recorded, I decided to use the sound from the video recordings for my vocalization analysis. Sound Forge, a computer program used for the sound analysis, enabled me to make sound spectrographs, or sonograms, on the woolly monkey vocalizations. In order to analyze just the woolly monkey vocalizations and not all of the background noise, adjustment was required. With Sound Forge, I was able to delete all of the outside and background noise that included crickets, birds, trains, human voices, and so on.

The proprietary Palm Pilot program used for recording the behaviors was called Pen Recorder and the program used to analyze the recordings was called Pen Reviewer. Below are diagrams of Pen Recorder, Pen Reviewer, and View Data.

When using Pen Recorder, I had to designate letters of the alphabet to the observed behaviors. Once I started Pen Recorder, I wrote the letter of every behavior that I observed an individual doing until they went inside or went to sleep. This method was difficult because it was impossible to keep up with the behaviors while having to remember which letter went with which behavior as well as write the letter and then keep going. The collected data was viewed in Pen Reviewer under View Data, displayed above, and then analyzed in the form of a graph, time line, and matrix, displayed below.

After using this technique for a while, I decided to change my method of recording because of the above stated reason as well as the fact that certain monkeys were more active than the others and I had to start and stop recording for the different individuals, which does not heed good results for analysis. For my further research, I will be using a new method of recording behaviors. Instead of using the proprietary Palm Pilot program, I will be using a tablet PC with a voice recognition program so I can just speak each behavior as it occurs.

Results & Discussion

The individual woolly monkeys of Troop I each have extremely different personalities, rank, age, relationships, etc. The family troop consists of four related individuals:

Name | Birth Date | Age
Corey | 11/13/91 | 11 years
Sissi | 09/29/95 | 7 years & 2 months
Tomas | 12/01/98 | 3 years & 11 months
Sara | 12/07/00 | 1 year & 11 months

Corey Sissi Sara Tomas

Corey is the dominant breeding male and is father to both Sara and Tomas. Sissi is Corey's sister and is the dominant non-breeding female. Sissi has never had any offspring and is considered sterile. The position of the second most dominant member of the troop is currently being fought over between Sissi and Tomas. Because Tomas is a subadult male and Sissi is an adult female, he and Sissi fight over everything, from food to where to sleep. Thomas and Sara are siblings and fight and play in ways similar to human siblings, but still show affection quite often, grooming each other and resting next to each other.

Tomas and his father Corey appear to have the closest relationship within the group. Tomas follows Corey around, mimicking certain behaviors. When Tomas and Sara are resting together or grooming each other, Corey generally joins them. Strange to human viewers, the family troop members are sexual with each other, especially Corey and Tomas and Corey and Sara. Sexuality between family members is surprisingly common in the primate world. According to primate research, it is quite normal for a father and son to feel on each other's genitals and have erections when around one another. These behaviors are considered greetings and are meant to establish friendly contact, usually occurring between adult males and juveniles of both sexes. During my observations, I noticed that Corey and Sissi rarely interact, while the same is true for Sara and Sissi.

The monkeys in the family troop have differing personalities, with Corey as the alpha male. He is the largest monkey, with huge canines and constant eye movement that indicates a neurological disorder, though not apparent in any other way. Corey never plays and is always pacing the cage, eating, grooming himself or others, staring at outside disturbances, or resting. Only after about a month of observation Corey appeared not to consider me an outside threat anymore, showing behaviors indicating a friendly greeting and then calming down other group members through appeasement behaviors. This meant that I could now observe their behavior undisturbed by outsiders. Tomas is more of a loner for the majority of the time; shy toward outsiders, he never makes eye contact with me, which is unlike all the others in the group. When not off by himself, Tomas is playing or play fighting with Sara, fighting with Sissi, or grooming or resting with Corey and/or Sara.

Corey staring Tomas hiding Sissi & Tomas Sissi walking Sara eating

fighting

Sissi is the most unsocial member of the group, only interacting with the others when fighting with Tomas. She is, however, active toward me, cage shaking, which is a sign that she feels threatened, and intense staring sessions at me, most likely indicating that she does not approve of my presence. When not interacting with Tomas or me, Sissi rests high up in the top of the cage, far away from everything and everyone else. Sara on the other hand is the most active and social member of the group. Sara is always doing something, whether watching me, playing with Tomas, resting with Corey and/or Tomas, eating, playing by herself with toys, or just running around bipedally on the cage floor. The youngest, most curious and loving of the group, she is the one that has tried to make contact with me the most and is the most affectionate toward others.

Below is a table listing the observed behaviors, their description, and the individuals in which the behaviors were observed.

Behavior | Description | Individuals In Which The Behavior Was Observed
Eat | Self explanatory | Corey, Sissi, Sara, Tomas
Play | Self explanatory; includes biting, running, climbing, rolling around, etc. | Sara, Tomas
Chestrub | Rub object against chest to scent mark; usually only done by males | Corey, Tomas, Sara
Swing | Self explanatory; on ropes or around the cage | Corey, Sissi, Sara, Tomas
Walk Quadrapedally | Self explanatory | Corey, Sissi, Sara, Tomas
Fight | Self explanatory | Sissi, Sara, Tomas
Groom | Each other or themselves | Corey, Sara, Tomas
Walk Bipedally | Self explanatory | Corey, Sissi, Sara, Tomas
Teeth Chatter | Dominant male moves jaws up and down rapidly, chattering his teeth; threat display or sexual arousal display | Corey
Jump | Self explanatory; on floor, up to cage or rope, etc. | Corey, Sissi, Sara, Tomas
Climb cage | Self explanatory | Corey, Sissi, Sara, Tomas
Climb Rope | Self explanatory | Corey, Sissi, Sara, Tomas
Cage Shake | Use all four limbs to shake the cage; threat display | Corey, Sissi, Sara
Rub | Use hands to rub on each other’s bodies; brings appeasement and strengthens close relationships | Corey, Sara, Tomas
Bite | Self explanatory | Sissi, Sara, Tomas
Grasp With Tail | Use “5th limb” to hold on to objects or pick up objects | Corey, Sissi, Sara, Tomas
Stare | Self explanatory | Corey, Sissi, Sara
Hump | Self explanatory | Corey, Tomas
Copulation Attempt | Attempt to copulate with another individual; practice for actual copulation; occurs between males and females and between males | Corey, Tomas, Sara
Run | Self explanatory | Sissi, Sara, Tomas
Yawn | Self explanatory | Corey, Sissi, Sara, Tomas
Lick | Themselves, each other, or various objects including the floor and the cage | Corey, Sissi, Sara, Tomas
Masturbate | Self explanatory | Corey, Tomas
Feel On Genitals | Feel on own or another individual’s genitals; display of friendship and is thought to bring appeasement | Corey, Tomas
Reach For Me | Self explanatory; reach out of cage to try to touch me | Corey, Sara
Rest | Self explanatory | Corey, Sissi, Sara, Tomas
Sneeze | Self explanatory | Corey, Sissi, Sara, Tomas
Drink | Self explanatory | Corey, Sissi, Sara, Tomas
Scratch | Self explanatory; usually themselves | Corey, Sissi, Sara, Tomas
Hang | Upside-down with tail grasping object and supporting entire body | Corey, Sissi, Sara, Tomas
Reach Out Of Cage | Self explanatory; usually to get leaves, sticks, or other food dropped outside of the cage | Corey, Sissi, Sara, Tomas
Sit | Self explanatory | Corey, Sissi, Sara, Tomas

In addition to using the video recording of the woolly monkeys for behavioral analysis, it was also used for sound analysis. I used a computer program called Sound Forge, which enabled me to make sound spectrographs, or sonograms, of the woolly monkey vocalizations. In order to analyze just the woolly monkey vocalizations and not all of the background noise, adjustment was required. Using Sound Forge enabled me to delete all of the outside and background noise including crickets, birds, trains, human voices, and so on. I was able to produce several sonograms from the data collected by listening to the sounds while watching the screen and marking where I heard common sounds of the woolly monkey. These common sounds included shrieks, squeaks, and grunts.

I then performed a spectrum analysis, an option in Sound Forge, in order to view the vocalizations in the form of a sound spectrograph. Although this analysis is not yet complete, it will be continued in the future. After more spectrographs are made and analyzed, I will be able to differentiate between individuals just by looking at their sonograms because it is my hypothesis that each individual produces different sound spectrographs although they make the same vocalizations. The human ear might not be able to differentiate between individuals when they are making the same sounds as others so this data will be useful in further vocalization research in woolly monkey populations.

The sound spectrograph below is of a squeak.

The next sound spectrograph is of a screech.

The last sound spectrograph is of a grunt.

For my further research, I will be using a new method to record behaviors. Instead of using the proprietary Palm Pilot program, I will be using a tablet PC with a voice recognition program so I can just speak each behavior as it occurs. The program is called Dragon records what I say and analyzes the data in a similar manner to that of the proprietary Palm Pilot program. I will also be using an Elura 40 digital video camcorder, which has superior resolution and sound quality combined with the ability to take digital photographs. The camera also has a steadier that eliminates most of the shakiness from holding the camera.

The observation of Troop II will begin when the two new unrelated male monkeys are introduced to Monkey Island. I will continue recording more vocalizations and perform more in depth analysis using Sound Forge. This research will be helpful in teaching zoo personnel and others interested in woolly monkeys about their behaviors and vocalizations, as well as being useful for maintaining and breeding captive troops.