Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 1 Fate of Fallen Fruit: Cebus capucinus fruit d roppings eaten by agoutis and o thers Delaney Roth Department of Evolutionary Anthropology University of California, Davis EAP Tropical Biology and Conservation Program, Fall 2016 16 October 2016 ___________________________ __________________________________________________________ A BSTRACT White faced capuchins ( Cebus capucinus ) are omnivores that forage in tree canopies eating mostly fruits. Though many previous studies have been done on the foraging behavior and diet of white faced capuchins, there is little information available on their feeding behavior in terms of fruit dro pping while eating. This study was done on a group of 13 wild white faced capuchins in Bajo del Tigre, Monteverde, Costa Rica over a two week observational period. I observed the feeding behavior of the white faced capuchins, including number of fruit piec es dropped by the capuchins during 30 second focal observations. I noted animals, such as agoutis, that were feeding on the dropped fruit to determine what animals were taking advantage of the fruit dropped by the white faced capuchins. I found that, on av erage, white faced capuchins dropped 5.2 pieces of fruit per 30 second observation period. My data demonstrates that there was a significant difference in dropping amount for different fruit types as well as significant differences in the presence of agout is feeding for different fruit species. The majority of the time white faced capuchins were feeding, other animals were feeding on the fruits the capuchins dropped, this suggests the majority of those fruits are being either dispersed further or are being fed on by other animals. Overall, my data suggest that white faced capuchins make fruits more accessible to ground foraging animals and in turn aid in second degree dispersal of those fruits. Further research would be beneficial in looking at fruit selecti vity in white faced capuchins and determining the fate of the dropped fruits that were not fed on by other animals during the time the capuchins were feeding. El destino de las frutas cadas: los monos Cebus capucinus botan frutos que luego son consumid os por guatusas y otros animales RESUMEN Los monos carablanca ( Cebus capucinus ) son omnvoros que forrajean principalmente frutos en las copas de los rboles. Aunque se han hecho varios estudios sobre su comportamiento de forrajeo y la dieta de stos monos, se tiene poca informacin disponible sobre su comportamiento en trminos de dejar caer frutos al suelo mientras se alimentan. Este estudio fue realizado sobre un grupo de 13 monos carablanca silvestres en Bajo del Tigre, Monteverde Costa Rica, duran te un periodo de dos semanas. Observ el comportamiento de los monos al comer, contando el nmero de pedazos de fruta que tiraron al suelo durante 30 segundos de observacin focal. Observ animales, como guatusas, que estuvieron comiendo las frutas cadas, para determinar qu animales aprovechan ste recurso alimenticio. Encontr que en promedio los monos tiran 5.2 pedazos de fruta en cada periodo de observacin de 30 segundos. Mis datos demuestran que hubo diferencias en la cantidad de pedazos de fruta tir ada para los diferentes tipos de fruta, as como tambin diferencias en la presencia de guatusas alimentndose segn las diferentes especies de frutas. La mayor parte del tiempo que los monos carablanca estuvieron comiendo, otros animales estuvieron comien do de las frutas que los monos tiraron, esto sugiere
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 2 que la mayora de esas frutas son o ya sea dispersadas, o alimentando a otros animales. En general mis datos sugieren que los monos carablanca hacen ms accesibles los frutos del dosel para los animales que forrajean en el suelo, los que a su vez ayudan tambin en la dispersin secundaria de las semillas de esas plantas. Sera bueno contar con ms investigacin que considere la selectividad de los frutos por los monos, y determinar el destino de los fruto s que ellos tiran y que no fueran comidos por otros animales durante el tiempo en que los monos se alimentaban. ______________________________________________________________________________ Cebus capucinus (white faced capuchins) are New World monkeys in the family Cebidae and are native to Central America and Northern South America. White faced capuchins are common primates in the Monteverde area of Costa Rica. White faced capuchins are omnivorous primates, but the majority of their diet consists of fruits Capuchins often travel and forage in the tree canopies of forests in groups of up to about 30 individuals and climb down into lower levels of the forest less often (Chapman and Fedigan 1990 Rosenberger 1992 ) There is a wide varie ty of fruit in their diet and they often eat fruits by sucking out the juice and fruit pulp then sp itting out the seeds and fibers. This suggests that they have an important role as seed dispersers in t he forests (Wainwright 2007). A study by Valenta and F edigan (2008) looked at seed dispersal by capuchins in dry forest and found that capuchins fed on over 39 different seed bearing plant species. Within those species they noted that some seeds were too big to swallow so the capuchins dropped them. In anoth er observation by Soley et al. (2016), they noted that white faced capuchins were feeding on hermit crabs, eating their abdomen and discarding the rest of the body. These observations demonstrate how capuchins are extractive foragers, often discarding food items they are unable to eat or prefer not to eat (Rosenberger 1992) Often capuchins attract other animals during their feeding bouts A feeding bout is defined by a period of time that the group is intensely feeding. Animals such as collared peccaries, agoutis, and coatis are commonly found on the nearby ground du ring a feeding bout (Wainwright 2007). Many ground foraging animals rely on plants to drop their fruits and seeds to the ground, so animals that aid in this p rocess make those foods more accessible to ground foraging animals. A study conducted by Boinski and Scott (1988) fou nd that birds t end to follow capuchins during feeding bouts so they can pick up insects and fruits that are exposed by the capuchin group. This shows the potential white faced capuchins have for attracting other foraging anima ls and making foods more accessible to them, though there is little information available about the animals that feed the white faced capuchin food droppings Even less of that information is available for the white faced capuchins in Monteverde. Thus, I addressed the following questions: ( 1 ) How many fruit pieces do white faced capuchins drop during a given feeding bout? 1a. Will the amount of fruit pieces dropped by the white faced capuchins vary for different plants? 1b. If so, what is the cause of this variatio n? And ( 2 ) What animals are eating the fruit dropped by the white faced capuchins? 2a. How often are th ose animals feeding on the fruit dropped by the white fac ed capuchins during the time the white faced capuchins are feeding? esence for different fruit types ?
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 3 METH O DS Study Site: I observed white faced capuchins ( Cebus capucinus ) in Bajo del Tigre, a part of the from 21 November to 1 December 2016 Bajo del Tigre is part of the premontane wet forest in Monteverde and is located just a couple kilometers away from the Monteverde cloud fores t Obse rvations: I began observations at 7:00am in Bajo del Tigre. I started at the main entrance and walked the trails through the area located white faced capuchins. If I was unable to locate the troo p in the morning I would search for an additional four hours beginn ing at 1:00pm. Once I located a group of white faced capuchins I recorded the time, location, number of individuals, and fruit being consumed. After, I began taking 30 second focal observa tions noting the time, f ood type, and number of food items the fo cal individual dropped (Altmann 1974). Focal animal sampling is a method of observation where the observer records the behavior of one individual for a set time period (Altmann 1974). I move d from feeding individual to feeding individual until there were no mor e individuals feeding in the grou p or the group had moved to a new location. During a focal observation or the time between focal observations I would also make notes of any additional b ehavior or potential factors influencing feeding behavior such as how the individual obtained a food item In addition, when I spotted other animals feeding on the capuchin droppings I wo uld record the time, animal name what they were feeding on, and the duration of their presence feeding. I observed Cebus capucinus with binoculars and recorded my observations using a notebook with a pen, an iPhone, and a watch to record the time. For fruit species I was unable to identify during follows I took sampl e s and pictures of the plants to be later identified at the I nstitute with help from advisors. I categorized the fruits by species morphological characteristics, abundance, and risk level I used morphological characteristics to group the fruits into four categories: 1, large and pulpy, 2, large and tough, 3, small and pulpy, and 4, small and tough. I labeled fruits with a diameter of over 3 cm as large, and those under 3 cm as small. I labeled fruits with a rough, firm, shell like consistency as tough, and those with softer or fleshy consistencies as pulpy. I categorized abundance in three categor ies by visual estimation: abundant, common, and rare I labeled p la nts that were present in over 50 percent of the Bajo del Tigre area where I searched as abundant plants that were present in over 25 percent as common plants present in 25 percent or less of the area as rare I to the ground, if the white faced capuchin would have to walk on the ground to re ach the plant, and how many fruits the individual could grab at once. RESULTS Capuchin Fruit Droppings: The white faced capuchins dropped 5.2 pieces of fruit, on average, during a 30 second focal observation The difference between a verage droppings per fruit was statistically different ( ANOVA, F 5 187 = 40.73 P = 2.21 ). Cebus capucinus dropped more oranges and guavas per
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 4 observation than Psychotria quinqueradiata Zanthoxylum fagara and Symplocos limoncillo (Fig. 1). Figure 1 Average Droppings b y Fruit Species : Average number of fruit items for each fruit type that were dropped by the white faced capuchins during a 30 second observation. Large pulpy fruits and small pulpy fruits were statistically different from large tough fruits and small tough fruits ( T test, t = 16.17 df = 88.8 ). White faced capuchins dropped more pulpy fruit items, on average, than tough items during a 30 second observation (Fig. 2). Figure 2 Average Droppings by Fruit Morphol ogy: Average number of fruit dropped by the white faced capuchins during a 30 second observation for each morphological grouping. 0 1 2 3 4 5 6 7 8 9 10 Oranges Guavas Myrcia splendens Psychotria quinqueradiata Zanthoxylum fagara Symplocos limoncillo Average number of droppings per 30 second observation Fruit Species 0 1 2 3 4 5 6 7 8 9 Large/Tough Large/Pulpy Small/Tough Small/Pulpy Average number of droppings per 30 second observation Morphology of Fruit
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 5 When comparing droppings by abundance levels, I found the difference between fruit droppings for the three abundance levels to be statistically significant ( ANOVA, F 2 190 = 15.20 P= 3.0 ), with white faced capuchins dropping more of abundant fruit items and rare fruit items than common fruit items. There was no significant trend for abundance of fruit relating to number of fruit dropped by the white faced capuchins because rare and abundant fruit were dropped more on average (Fig 3). Figure 3 Average Droppings by Abundance: Average number of fruit pieces dropped by white faced capuchins during a 30 second observation for abundant, common, and rare fruit types. There was a significant difference between the average numbers of fruit items dropped by the white faced capuchins for the different risk levels ( ANOVA, F 2, 190 = 8.07 P = 3.0 ) with high and low risk fruits being dropped mo re than medium risk fruits There was no trend for number of fruit items dropped by the white faced capuchins for fruits grouped by risk level (Fig. 4). 0 1 2 3 4 5 6 7 8 9 10 Abundant Common Rare Average number of droppigns per 30 second observation Abundance Level 0 1 2 3 4 5 6 7 8 9 10 High Risk Medium Risk Low Risk Average number of droppings per 30 second observation Risk Level
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 6 Figure 4 Average Droppings by Risk Level: Average number of fruit pieces dropped by white faced capuchins during a 30 second observation for high, medium, and low risk plants. Animals Feeding on Fallen Fruits: Agoutis were present feeding on dropped fruit pieces for all fruit species, except oranges (Fig. 5). White tipped doves were the next common animal feeding on a variety of the fruit pieces dropped by capuchins; guavas Myrcia splendens and Zanthoxylum fagara (Fig. 5). Additio nally, I observed white nosed coatis feeding on dropped fruit pieces of Myrcia splendens, Symplocos limoncillo and guavas (Fig. 5). Figure 5 Animals Feeding by Fruit Type: Number of animals observed feeding on capuchin fruit droppings for each fruit type and each animal type. Over half of the time that I observed white faced capuchins feeding and dropping fruits other animals were feeding on those fruit droppings (Fig. 6). I observed agoutis feeding on fruit dropped by the white faced capuchins more often than any other animal (Fig. 6). 0 1 2 3 4 5 6 7 Guavas Oranges Psychotria quinqueradiata Myrcia spendens Zanthoxylum fagara Symplocos limoncillo Number of Animals Feeding Fruit Type Agoutis White-nosed coatis White-tipped doves
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 7 Figure 6 Percentages of Feeding Times by Animal Type: The percentage of minutes each animal spent feeding on capuchin fruit droppings out of the total observed feeding time of capuchins (n = 232 minutes) I found agoutis feeding on dropped fruit pieces of all fru its except oranges. The majority of the time they were feeding on guavas, followed by Myrcia splendens and Zanthoxylum fagara (Fig. 7). Figure 7 Time Agoutis Spent Feeding by Fruit Species : The percent of time agoutis were feeding on each fruit species of white faced capuchin fruit droppings (n = 90 minutes) Agoutis 39% White nosed coatis 12% White tipped doves 3% No animal present 46% Guavas 43% Psychotria quinquerdiata 7% Myrcia splendens 29% Zanthoxylum fagara 14% Symplocos limoncillo 7%
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 8 Observational Results: During my observations of the white faced capuchins I noted their behavior and factors that may have influenced the amount of droppings for each fruit type. One time when the white faced capuchins were feeding on oranges, I observed them rubbing their body with the oranges before eating them. The oranges were labeled as high risk fruits because the capuchins were required to go to the g round and cross an open grass patch in order to reach the citrus tree and once there they were only able to grab at most two oranges. They would fit one in their mouth, another in their hand, and used their free hand to climb back to the feeding tree. Onc e they returned to the tree they were feeding in they broke open the orange, rubbed it all over their fur, and then began to break pieces off to eat. To eat oranges the capuchins would suck the juice out of each piece and drop the rest ; they rarely dro pp ed pieces that they had not eaten part of Three times I observed a mother with a baby on her back wait for another individual to drop some orange pieces and then collect them from the bottom of the fruit tree instead of cro ssing the open patch on ground. For guavas, I often observed the white faced capuchins just scratching the surface of a guava or only sinking their teeth in and then dropping the entire guava. These guavas were often first choices for the agoutis following below. I did not record the ripeness of these guavas, but it would be beneficial to investigate if the white faced capuchins were testing the guavas for ripeness. For large hard fruits, the white faced capuchins often dropped most or the entire fruit and these were again preferred fruit items for agoutis that were scavenging below. The Zanthoxylum fagara were small and tough and the white faced capuchins often grab bed an entire bundle of them and sat on a branch w ith the bundle to eat. The capuchins hardly eve r drop ped pieces of this fruit while they ate, instead, they would drop whatever remained on the bundle when they were done with it. When the capuchins were feeding on berries or small fruits it was uncommon for them to drop any of the fruit from their m outh. I nstead most of the droppings occurred when they were climbing around or when they were picking the fruits from the rest of the plant. Additionally, I obs erved one agouti acting very aggressively toward another agouti for several minutes one day in a narrow path chasing the agouti out of the feeding area several times This limited the number of agoutis feeding in that area to one. Other times, when the area was more open or the white faced capuchins were more spread out in the canopy, there wer e multiple agoutis feeding in one area without any aggression toward each other. D ISCUSSION I found that white faced capuchins drop on average about ten pieces of fruit per minute while feeding There was a significant difference between droppings of different fruit types, morphologies, abundance s and risk level s High abundance of fruit and low risk level were
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 9 hypothes ized to lead to a high amount of fr uit dropped by the white faced capuchins. Even so, I did not find a tre nd for abundance or risk level. However I did observe that the white faced capuchins dropped more pulpy fruit s on average than tough fruits. This suggests fruit morphology plays a role in how many fruit pieces are dropped by the capuchins. When the white faced capuchins only ate a fruit a few times I did not include that fruit in the graphs or calculations. Through my observations and data analysis I discovered that fruit mo rphology was a key factor for determining fruit droppings by the capuchins Since the white faced capuchins are looking for and eati ng different parts of each fruit grouping the fruits by morphology helps to explain that what the capuchins are attempting to get from a fruit relates to how much of the fruit they discard Another factor for determining fruit droppings could be that softer fruits are more easily detache d from the rest of the plant tha n harder fruits. So, when the capuchins are searching through the trees fruits with certain morphologies are more likely to be broken from the plant and fall to the ground. These suggestions stem from my observations that white faced capuchins would both accidentally drop fruits to the ground while foraging and would actively discard fruits while foraging. Additionally, it is possible that the fruit dropping amounts relate to monkey syndromes for those fruits. While fruit preference is typically studied for syndromes, the number of droppings for certain fruit m orphologies can relate to the fruits that are typically preferred. Monkey bird syndromes are often described as fruits that are pulpy, large, and brightly colored ( Ga utierHion et al. 1985, Julliot 1996). This aligns with my findings of pulp y fruits having more dropped pieces on average than tough fruits, though it would be necessary to determine fruit preference and accidental versus active fruit droppings by the capuchins before suggesting droppings as part of this syndrome. This also could mean the higher amount of droppi ngs in fleshy fruits was due to the white faced capuchins feeding on those fruit types more often. From my observations, I determined that risk level dictated how much of a fruit they used but not how many pieces of a fruit were dropped. Fruits that are riskier to obtain are more likely to be used completely for what the capuchins are attempting to get from those fruits Yet, there still may be much of the high risk or use those parts. For oranges, a high risk plant, the capuchins chew ed and extract ed the juice from all the pieces of the fruit but did not swallow the pulp and skin, so they ate from every piece of fruit they ended up dropping. For guavas, a low risk plant, I observed the capuchins often dropping the fruit after barely biting into it. Further research should be done looking into the fora ging behavior and selectivity for guavas by white faced c apuchins. Although guavas are low risk, and therefore droppings by the capuchins may increase, the capuchins often discard entire fruits after just scratching them or sinking their teeth in. This may be a method used by the capuchins to test for the ripene ss of a fruit or it may be due to the abundance and low risk level of the fruit. Other capuchin species are known to eat and discard fruits in relation to ripenes s (Izawa 1978), which suggests white faced capuchins could also be discarding fruits based on ripeness
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 10 Though, i n a study by Ferrari and Lopes (2002) on Cebus apella (brown tufted capuchins) they found that the capuchins discarded over one fifth of their fruit intact and of those fruits, only 4.7% were unripe Thus, ripeness may not be the only factor influencing fruit discarding. The white faced capuchins may also be feeding on larvae or insects on the guava and then dropping the rest of the fruit. To determine what causes a white faced capuchin to use or disca rd a fruit when foraging would be intriguing and beneficial to understanding their foraging behavior. Nonetheless, my observations show that white faced capuchins on average drop a high amount of fruit pieces during a feeding bout So what happens to th e fruit once it has been dropped? My data demonstrates that the majority of the time other animals are feeding on those pieces During my observations I found that agoutis coatis, and white tipped doves were present feeding on the droppings during the ti me that the capuchins were feeding. These animals may lead to different fates for the fruits. For example, for some fruits agoutis act as secondary dispersers by providing the seed with a chance to escape seed predation after the primary disperser, typically a bird or mammal, does not effectively dispers e the seed (Forget and Milleron 1991). I found there to be a significant variation in animal feeding presence during capuchin feeding for different fruit types, with guavas having the highest number of visiting animals Several factors could be responsible for this variation: the time of day, the site whe th er it was open area or closed, steep or flat, the presence of other animals, and potentially many others. For this reason, I only looked into fee ding time variation for agoutis, who were present at almost all sites all except oranges When observing agoutis, the variation in time spent feeding on capuchin droppings seemed to relate both to amount of fruits being dropped and to the site the capuchins were feeding at. With fruits that the capuchins would drop many pieces of, especially whole fruits, and where the capuchins were more spread out, there would often be more agoutis feeding. Potentially, this is because there is les s of a struggle to compete for the droppings. In those scenarios, the fruits are set up for scramble competition over contest, where the fruits are less likely to be hoarded by any individual and the competition comes from who can get to the foods more quic kly ( Belzung 1986, Isbell 1991). I observed that agoutis are feeding the most frequently on the dropped fruit; this suggests that one of the main fates of the fruits dropped by capuchins is predation or dispersal by agoutis. Slightly less than half of th e time I did not observe animals feeding o n the capuchin fruit droppings. Most likely this does not mean t hat t he fruit s were left untouched but that the fruit s were later fed on by either those same animals or other species. This shows how capuchins do not contribute to see d limitation but instead aid in dispersal (Tilman 1994). Through dropping fruits from high up in the forests t he white faced capuchins are making those fruits more accessible to ground feeding animals while aiding in the second degr ee dispersal of t he fruits they are feeding on with animals such as white nosed coatis. With my observations and data in mind, I suggest further research in determining the exact fate of the fruit not eaten during the time capuchins were feeding. This co uld lead to more information on capuchins aiding in second degree dispersal and on capuchins as potential seed dispersal limiters.
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 11 Overall, the data collected in my study suggest that white faced capuchins in the Monteverde area of Costa Rica are making fruit items more accessible to other animals by actively discarding and accidentally dropping them during their feeding bouts. This p rocess results in secondary dispersal and predation by other animals such as, agoutis, white nosed coatis, and white tipped doves. ACKNOWLEDGEMENTS I would like to extend m y gratitude to Federico Chinchilla for his guidance and advice throughout my project, to Frank Joyce for the use of his land an d for his advice, to the Estaci n Bi ol gica Monteverde, Bosque Eterno de l os Ni os, Instituto Monteverde, to Siria and Alvaro Sal azar Ugalde, and to my fellow EAP students for all their support. LITERATURE CITED Altmann, J 1974 Observational study of behavior: sampling methods. Behaviour 49.3 : 227 266. Belzung, C and J R. An derson. 1 986. Social rank and responses to feeding competition in rhesus monkeys. Behavioural processes 12 : 307 316. Boinski, S and P E. Scott. 1 98 8. Association of bi rds with monkeys in Costa Rica. Biotropica 136 143. Chapman, C A., and L M. Fedigan. 1 99 0 Dietary differences between neighboring Cebus capucinus groups: local traditions, food availability or responses to food profitability? Folia Primatologica 54: 177 186. Ferrari, S. F., and M. Aparecida Lopes. 2 00 2. Fruit rejection by tufted capuch ins ( Cebus apella : Primates, Cebidae) during the predation of Cariniana micrantha seeds: Suboptimal or just Revista de Etologia 4 : 3 9. Forget, P M and T Milleron. 1 99 1. Evidence for secondary seed dispersal by rodents in Panama. Oecologia 87.4 : 596 599. Gautier Hion, A 1985 Fruit characters as a basis of fruit choice and seed dispersal in a tropica l forest vertebrate community. Oecologia 65.3 : 324 337. Isbell, L A. 19 91 Contest and scramble competition: patterns of female aggression and ra nging behavior among primates. Behavioral Ecology 2 : 143 155. Izawa, K 1 97 9. Foods and feeding behavior of wild black c apped capuchin ( Cebus apella ). Primates 20 : 57 76. Julliot, C 1 9 96 Fruit choice by red howler monkeys ( Alouatta senicul us ) in a tropical rain fo rest. American Journal of Primatology 40 : 261 282.
Fruits Dropped by Cebus capucinus are Eaten by Agoutis Roth 12 Rosenberger, A L. 1 99 2. Evolution of feedin g niches in New World monkeys. American Journal of Physical Anthropology 88 : 525 562. Soley, F I S. Chacn, and M Soley Guardia. 2 01 6. Extraction of hermit crabs from their shells by white faced capuchin monkeys ( Cebus capucinus ). Primates 1 5. Tilman, Davis. 1994. Competition and biodiversity in spatially structured habitats. Ecology 75.1 : 2 16. Valenta, K and L M. Fedigan. 2 008 How much is a lot? Seed dispersal by white faced capuchins and implications for disperser based studies of seed dispersal systems." Primates 49 : 169 175. Wainwright, M 2 007 The mammals of Costa Rica: a natural history and field guide Comstock p.155