Can long-tailed macaques associate color with different food items?

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1 Can long-tailed macaques associate color with different food items? Isaiah Byfield Nikitha Chintalapati Chelsea Dalgetty Aisha El-Gazzar Logan Goldsmith Asya Lobanova Daniel Rivero Joaquin Traverso Research in Ecology 2014 University of Miami

2 Abstract Long-tailed macaques live in a highly seasonal environment. The constant change in food availability is a significant challenge that these primates most overcome. One trait that might help them forage efficiently is their visual memory. For this experiment, we were trying to see if the macaques could associate the food they prefer the most with a certain color and a food they least prefer with a different color. At the end of the experiment, we found that the macaques approached to the bucket with their most preferred food (blue bucket-grapes) with the fastest time, which shows that they learned. Introduction Long-tailed macaques (Macaca fascicularis) are omnivorous, but they prefer to eat fruit (Yeager, 1994). These primates live in tropical rain forests characterized by heavy seasonal rainfall and humid, warm climate. During the dry season and the early rainy season fruit is unavailable, so they have to eat other food sources such as insects, stems, young and mature leaves, flowers, seeds, grass, mushrooms, invertebrates, bird eggs, clay and bark because they live in a seasonal environment, they constantly change what they eat (Cawthon, 2006). Foraging is an essential activity to which long-tailed macaques dedicate a high proportion of both their energy and time budgets (Gurmaya et al. 1994). Thus they should possess abilities that allow them to forage efficiently in a changing environment. Long-Tailed macaques have well developed visual memory. The macaques have been shown to remember where food was kept after a course of several months and have been proven to have the mental capacity of a three year old human child. They might be able to use this advanced memory capability to adjust to environment changes to find the food items that is available and edible at different times (Overman Jr and Doty, 1980). In this study we designed an experiment to test if long-tailed macaques can associate color with different food items. Our hypothesis was that the monkeys can associate the food they prefer the most with a certain color and a food they least prefer with a different color. Methods In the summer of 2014 we designed an experiment in order to determine if long-tailed macaques were able to associate food with a certain food item. We decided Monkey

3 Jungle in Miami Florida would be a good location because this place holds more than 140 Long-tailed macaques in semi-captive condition. We worked with the kitchen group which has about 60 monkeys. The group was composed mainly of juveniles. We chose the kitchen group because there is a fence where we can hang the buckets; the fence also provides protection to the observer. Study site and study subjects Our study site was 3.03 hectares (7.5 acres). The type of habitat in the enclosure is Hardwood Hammock of Caribbean origin. Our study subjects originated from 6 individuals imported from the island of Java in Treatments For the kitchen group of long-tailed macaques, we decided to use color coded buckets. As a team, we chose to use the colors red, blue, and yellow tape to coat our buckets. In each bucket, we put a specific food item: in the red bucket, there were coffee leaves, in the yellow bucket, we put peanuts, and in the blue buckets we put red purple grapes. These buckets were used to see if the long-tailed macaques can associate color with a certain food item. The reason that we chose primary colors (red, blue,and yellow,) was because we knew that those are easy colors for the monkeys to identify (Lucas et al., 1997). For each trial we put 20 pieces of food in each bucket. Every trial, each team was assigned a specific color to work with and fill before each trial started. In the blue bucket we put 20 grapes, in red we put 20 leaves, and in yellow we put 20 peanuts. In the beginning we put 10 pieces of food in each bucket, but then we changed to 20 because if one monkey comes and takes all of the food and another monkey comes and sees that none were remaining they would associate the colored bucket with no food inside. Before each trial we placed the buckets along the fence so it would be easy for the monkeys to eat. The buckets were placed 32 inches off the ground and 42 inches apart from each other. For each segment on the fence there was 1 bucket of each color. Trials During our thirteen trials we used three different variations of colored buckets, red, yellow, and blue. Every day we would perform two trials, one around 9:30 am and the

4 other around 11:30 am and we recorded our data. We had nine buckets, and nine observers (eight students and one teacher). Every trial, the same person would remain in the same spot, except they would receive different buckets each time out of random. Each trial was between seven and ten minutes long depending on whether there was rain or shine. For each trial to make sure the macaques would not be afraid to come to the buckets, everyone who was taking data would stand about three meters away to be safe. Behaviors Recorded During each trial we recorded a set of different behaviors. The behaviors that we recorded were these six: Grab and eat: when the monkeys came to the bucket and grabbed food from it and put it in their mouth. Grab and throw: when the monkeys came to the bucket but threw the food outside of the fence or at someone else, or anything besides putting in their mouth. Explore: when the monkeys looked inside the bucket, bit the bucket, or tried to take off the tape. Bark: when the monkeys barked, yelled or screamed at each other. Show canines: when the monkeys showed their canines or opened their mouth. Displacement: when another monkey (probably of a higher rank) moved or in other words displaced another monkey forcing it to either fight, bark, show canines, or to jump off the fence and run into the bushes. We also recorded the latency to the bucket ( When the monkey reached the bucket) and the time at which the bucket was empty. Data analysis From all the data we gathered we focused on latencies and the total visits to the bucket, which was the sum of grab and eat, grab and throw, and explore. We got the averages and medians for the grab and throw, grab and eat, and explore. After that we performed the chi square. Then we graphed the data in charts. To see if there were differences between our treatments we performed three Chisquared tests for each behavior. The first Chi-squared was performed to see if there were differences in the first half of the experiment. The second test was performed to see if there was a difference in the second half. The third test was performed to see if there was a difference in the overall experiment.

5 Results Overall we found that the long tailed macaques preferred grapes over the the peanuts and the coffee leaves (χ 2 =293.2 p<0.0001). We found some evidence that support the idea that long-tailed macaques can learn to associate food item with a certain color. Our results show that long-tailed macaques approached significantly faster to the blue bucket (χ 2 =24.23 p ), which contained their preferred food, than to the other two choices (Figure 2). However there was a lot of variation in the latencies recorded throughout the trials (Figures 3-5). For the remaining behaviors we found that the macaques visited the yellow bucket significantly less often than the other two choices, but only at the beginning of the experiment (χ 2 =3.54 p=0.03, Figure 6-8). After half of the trials the macaques visited all the choices with more or less the same frequency (χ 2 =1.12 p=0.2). Regarding the identity of the macaques that approached the buckets, most were juveniles followed by males while females were the least interested (Figure 9-11). Figure 1. Time at which the buckets were empty.

6 Figure 2: Latency to all three buckets throughout the 13 trials. Figure 3: Latency to the blue buckets throughout the 13 trials.

7 Figure 4: Latency of the Red Buckets Figure 5: Latency to Yellow Buckets (Throughout the 13 Trials)

8 Figure 6: Total behavior recorded at blue buckets throughout all 13 trials. Figure 7: Total behavior recorded at red buckets throughout all 13 trials.

9 Figure 8: Total behavior recorded at yellow bucket throughout 13 trials. Figure 9: Total number of visits at the blue bucket by juveniles, females, and males.

10 Figure 10: Total number of visits at the red bucket by juveniles, females, and males. Figure 11: Total number of visits yellow bucket by juveniles, females, and males.

11 Conclusion and Discussion In general we found that juveniles showed up more than the adults and there were more males than females. All the monkeys liked grapes the most, peanuts second, and coffee leaves the least. Even without looking at the bucket they still went for the blue buckets which support the idea that they learned. Even though they knew that there were leaves in the red bucket, they still explored it like the leaves were covering the food. Preferences in Long-tailed macaques Long-tailed macaques (Macaca fascicularis) are very picky primates. In the wild, these macaques have preferences between food items. During the Yeager experiment (1994), the macaques were given a number of different food species. There was a selection for 19 of the food species, but 13 of the food species were selected more often than expected. Long-tailed macaques appear to have very selective minds when it comes to food. When we were recording data during our trials we realized that most of the macaques were headed towards the blue bucket, which had a content of grapes. Long-tail macaques are frugivorous so most of their diet consists of ripe, fresh fruit. During dry seasons when fruit is not available, their diet would consist of mature leaves, seeds, flowers, bird eggs, insects, crabs etc. Long-tailed macaques have preference to fruit than to leaves. Aggressive behavior mostly happens when their diet is mostly fruits. This may be the reason why during our experiment (2014) the macaques preferred the blue bucket which contained grapes. Learning in Long-tailed macaques Good visual memory has also been shown in other macaque species. For example, in a related species to the long-tailed macaques, the pigtailed macaques, a study shows that the short-term memory of pigtailed macaques isn t very good. Their long-term memory (24-96 hour period) was shown to be a lot better (Overman and Doty, 2003). Variation in latencies and visits through time We found that the macaques did not differ in the number of visits to the different colored buckets. Furthermore, there was a high variation in the latencies from trial to trial. These findings could be due to two main reasons:

12 First, most of the macaques that visited our buckets were juveniles which could pay less attention to the test. From multiple studies, it has been proven that the younger juvenile Long-tailed macaques are more playful than the older individuals (Van Noordwijk, et al, 1993). From many studies of scientist it has been proven that Long-tailed macaque female juveniles play a lot with the infants and their siblings much more than other macaques. (O brien, et al, 1993). With that factor of the juveniles being more active and playful, this causes them to be more curious and less afraid of danger. This might be the reason they approached the buckets faster without worry. They would rip off the tape and lids not fearing something might happen. Once the juveniles were done investigating, proving the buckets were not a threat, the adults moved in to get their meal. That juveniles were playing and not really paying attention to the content of the buckets might also explain why the latencies to approach the buckets vary so much throughout the days. The second reason that could explain the pattern observed is that some macaques could have participated in some but not all trials. The group we worked with consists of about 60 long-tailed macaques, not all macaques came each trial. Past studies show that the rhesus monkeys ability to learn different colors and different patterns varies individually (Bartus et al, 1979). Therefore, as we couldn t identify which monkeys came to each trial, and each macaque learns differently, this could also explain the variation in the latencies found. Acknowledgements The Rhesus Pieces could not have done any of this work without the help of Monkey Jungle. We also thank our mentors Dr Krempels and Dr. Evans, and Karla Rivera and our facilitator Stephanie Baguidy. We obtained the required IACUC permit in order to conduct this research project. References Bartus, R. Dean III, R. Fleming, D Aging in the Rhesus Monkey: Effects on Visual Discrimination Learning and Reversal Learning, Journal of Gerontology, Volume 3, Issue 2, Pp Cawthon Lang KA January 6. Primate Factsheets: Long-tailed macaque (Macaca fascicularis) Taxonomy, Morphology, & Ecology. < Accessed 2014 July 14.

13 Gurmaya KJ, Adiputra IMW, Saryatiman AB, Danardono SN, Sibuea TTH A preliminary study on ecology and conservation of the Java primates in Ujung Kulon National Park, West Java, Indonesia. In: Thierry B, Anderson JR, Roeder JJ, Herrenschmidt N, editors. Current Primatology. Volume 1, Ecology and evolution. Strasbourg (France): Univ Louis Pasteur. p Lucas, P. Darvell, B. Lee, P. Yuen, T. Choong, M. Colour Cues for Leaf Food Selection by Long-Tailed Macaques (Macaca fascicularis) with a New Suggestion for the Evolution of Trichromatic Colour Vision. Folia Primatol 1998; 69: O brien, T, Robinson, J, 1993, Stability of Social Relationships in female Long- Tailed Macaques, Juvenile Primates Overman, W.H. and Doty R.W Prolonged visual memory in macaques and man Neuroscience. Volume 5, Issue 11, Pages Van Noordwijk M, Hemelrijk C, Herremans L, Sterck E, Spatial Position and Behavioral Sex Differences in Juvenile Long-Tailed Macaques, Juvenile Primates: Life History, Development and Behavior, with a New Foreword, Page Yeager,C Feeding ecology of the long-tailed macaque(macaca fascicularis) in Kalimantan Tengah, Indonesia International Journal of Primatology Volume 17, Issue 1, pp

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