Communal care of offspring in the white faced capuchin monkey ( Cebus capucinus ) Kristin A. Hook College of Natural Sciences, University of Texas at Austin ABSTRACT The purpose of this study was to document whether a communal infant care system existe d in the white faced capuchin monkey, Cebus capucinus (Cebidae), in the Monteverde area. The intention was to draw comparisons in time allocation spent between infants and other individuals in the troops followed. In addition, approach and leave times in interactions involving the infant and other members of the troop as well as the sexes of those individuals involved were documented. It was found that a communal infant care system does in fact seem to exist for this species of primate. Infants spent the majority of their time on the backs of a primary female in addition to the backs of juveniles. The majority of approaches made were to engage in social interaction. The majority of approaches made by individuals other than the primary female were either solicitations or offers for rides. There was no difference in numbers of approaches initiated by female or male individuals; however, females spent more time involved with the infant during their interactions than did the males. RESUMEN El propÃ³sito d e este proyecto fue documentar un sistema de custodia comunal de las crÃas de los monos carablanca, Cebus capucinus (Cebidae), en el Ã¡rea de Monteverde. Se observaron tropas de monos con la intenciÃ³n de hacer comparaciones entre las asignaciones del tiempo compartido entre las crÃas y otros individuos. TambiÃ©n se documentaron el tiempo de los acercamientos y las despedidas en las interacciones que involucraban a las crÃas y a otros miembros de la tropa, ademÃ¡s de los sexos de los individuos que estaban invo lucrados. Se encontrÃ³ que el sistema de custodia comunal existe en esta especie de primate. Las crÃas pasaron la mayorÃa del tiempo en las espaldas de una hembra primaria, seguido por el tiempo que pasaron en las espaldas de los juveniles. La mayorÃa de l os acercamientos ejecutados fueron para entretener en las interacciones sociales. La mayorÃa de los acercamientos ejecutados por individuos que no eran la hembra primaria fueron solicitaciones u ofertas para paseos. No hubo diferencias en el nÃºmero de ac ercamientos ejecutados por las hembras o los machos; sin embargo, las hembras pasaron mÃ¡s tiempo que los machos con la crÃa durante las interacciones. INTRODUCTION Alloparenting, defined as the care of offspring by non parental individuals, has been repo rted in over 30 mammal species (Goldizen 1986). Although literature on this phenomenon is scarce for white faced capuchin monkeys, Cebus capucinus , this form of helping behavior is known to be common among the cebines, whereby adult females and juveniles of both sexes show great interest in infants from birth until about two months of Oppenheimer 1981). Alloparenting behaviors include carrying or keeping watch over infants, active or passive sharing of food, and even nursing, the latter of which exists only
2 for Cebus (Robinson 1987). This study attempts to offset the paucity of data on communal care of infants in wild capuchins, a system that probably subsists because of the ir active nature and seasonal movement to exploit fruiting trees (Robinson 1987). There have been no studies published on the time budget of infant interactions to date. A time budget is simply a measure of what an organism spends its time doing on any given primary female presumed to be its mother because the relationship with the most frequent affiliative interaction observed in all cebine species is that between a mot her and her youngest offspring (Robinson 1987). Moreover, it was theorized that females would make more infant approaches than males and that time spent by females during the interaction would be longest based on the premise that they gain a delayed benef it of experience in parental care (Goldizen 1986). Lastly, helping behavior in males was assumed to be relatively nonexistent in any given troop because of the significant loss of foraging or hunting time that would be incurred (Goldizen 1986). MET HODS This study was conducted in Monteverde, Costa Rica, from April 13 through May 5, 2005, in the latter part of the dry season. The study site was in the area of El Bajo del Tigre, which at 1300m comprises 29 hectares of protected premontane wet forest , as well as adjacent areas on and around the properties of Frank Joyce, Susie Newswanger and Bob Law (Barnert 1999). The site was chosen based on previous studies done in the area and past predicted travel patterns based on repetitive sightings of these organisms (Filipkowski 1998). Common sightings were made on the Sendero de Los MurciÃ©lagos, Sendero Arboretum, and Sendero de Los Monos (Fig. 1). A troop of capuchins was located by arriving at El Bajo del Tigre at eight in the morning, where the informa tion center employees and volunteers were questioned for news on their latest whereabouts. The majority of the search occurred on the three aforementioned trails. Continuous focal animal sampling was used due to the nature of the hypotheses that emphasize d individual behaviors. Once a troop was found, time and location. Infant was defined based on relatively tiny size and frequent presence on the back of another individ ual. Its age and sex could not be determined. Observed infant locations included the back of a primary female, free and alone, or on another budget began and conti nued until the troop was out of possible following range. Behaviors cited include approaches and leaves made by all individuals within the troop and inferred purpose of the interactions (see APPENDIX 1 for types and definitions). Approaches were defined based on close proximity judged to be less than one meter away. Leaves were defined based on leaving the one meter proximity area of the infant. The individual who initiated the approaches and leaves, either the primary female, infant, or the individual involved in the approach, were recorded as well. Finally, the number of individuals within the troop was estimated and recorded. Over time it was easier to distinguish between the two troops observed based on the composition and ratio of juveniles to adul ts. Recorded data was then broken down into percentages of how often certain behaviors occurred to get an overall picture of the
3 communal infant care system and the individual interactions between the infant, primary female, and other troop members. Adult s were identified as either male or female, and sex was disregarded in juveniles due to the small sample size. Juveniles were defined based on smaller body size, relative frequency of play they were engaged in, and a youthful appearance based on fewer face wrinkles in comparison to the adults. A Chi squared test was used to determine similarity in comparing male, female, and juvenile interactions. While observing C. capucinus for indications of a communal infant care system, notes were taken on other misc ellaneous behaviors within the two troops studied (see APPENDIX 2). RESULTS Observations were made on eleven separate contact days, all of which occurred within El Bajo del Tigre and the surrounding properties. In over 80 hours spent in the field, ap proximately thirteen hours were spent in contact. Only 183 minutes of these were actually spent observing and collecting data on the infants. The monkeys observed on the first nine days were believed to be of the same troop; however, it is highly probabl e that the last two days in the field were spent following a different troop with an overlapping range. The best estimate of the number of individuals in the first troop was sixteen, which includes the two infants followed and observed. The best estimate of the number of individuals in the second troop was eighteen, which also includes the two infants followed and observed. The sex ratio of the troops was hard to determine, due to their inconspicuous sexual organs and fast pace behind dense foliage. Rat io of juveniles to adults was nearly even for the first group, while the second group seemed to have a higher ratio of juveniles to adults (7 adults, 9 juveniles, 2 infants). This field study involved unmarked individuals and no distinctions were made a s to the identity of the individuals due to the density of foliage and constant movement of the troop. Hence, data was collected per individual infant per day, even though there were only two individual infants observed from one day to the next. Hence, t he total sample size was seventeen individual infant observations. Over the course of this study, the infants were on the backs of a primary female 54% of the time and were alone or free from another individual approximately 18% of the observed time (Fig. 2). The infants were on the backs of another individual 28% of the time (Fig. 2), with 60% of those interactions being on the backs of juveniles (Fig. 3). _______________________________________________________________________ time distribution spent with individuals within troop. Infants were observed to be either on the back of a primary female, alone and free from others, or on the back of an individual other than the primary female.________________
4 Individual males and fem ales exhibited no difference in the number of approaches made (Fig. 4), however, females interacted with the infant for a longer period of time than did the males (Fig. 5). Juveniles made appro ximately 25% of approaches that males and females did (Fig . 4) with considerably less time spent with the infant (Fig. 5). Primary females approached males and females in even numbers (Fig. 6), but interaction time was considerably longer for the males at 76% of the time (Fig. 7). Individuals other than the prim ary female initiated half of the approaches made to the infant (Fig. 8), and the majority of approaches made were to engage in a nuzzle (APPENDIX 1) with the primary female and infant (Fig. 9). ______________________________ Another interaction behavior commonly observed FIGURE 3. Chart of distribution of was when an individual approached the infant time among individuals involved in int eractions with infants. Categories of individuals were males, females, and juveniles. ___________________ in order to carry it or when the infant approached another individual in order to solicit a ride (APPENDIX 1). Leaves were in itiated by the primary female 59% of the time, the other individual 37% of the time, and the infant 4% of the time (Fig. 10). A Chi squared test was used to determine similarity in comparing male, female, and juvenile interactions with infants. ______ ________________________ The results showed there was a significant diff FIGURE 4. Number of approaches erence between varying percentages of time for made by individuals other than the individual approaches (X 2 =53, df = 2, 5. 99, primary female. Categorized by adult males, adult females, and juveniles._ P<0.05) and between varying percentages of time for approaches made by the primary female (X 2 =91.5, df = 2, 5.99, P<0.05). This signifies that approach time was not random for individuals and could in fact be dependent on sex or age of individuals approaching. It also could have been caused by many other factors that this study did not consider. FIGURE 5. Percentage of time spent interacting with the focal individual.___ _________
5 FIGURE 6. (Top Left) Approaches initiated by the primary female with infant to other individuals. Primary females did not approach juveniles. FIGURE 7. (Top Right) Percentage of time the primary female spent involved in interactions with individual adult males and adult females.____________________ FIGURE 8. (Top Left) Distribution of total approach initiations. Individuals categorized by p rimary female, individual, and infant. FIGURE 9. (Top Right) Approach types and percentage of occurrences between individuals and infants within the troops.__________________________________ _________________________________ FIGURE 10. (Left) Chart of percentage distribution of leaves initiated by either primary female, individual other than the primary female, or ____ the infant.____________________
6 DISCUSSION The purpose of this study was to determine whether a communal infant care system exists for this species of primate. Many observations of helping behaviors were recorded, and, in general, many indi viduals within the troop seemed to expend a lot of energy involved in interactions with the infants. Using approaches and interaction with the infant as an indicator of such a system, the data supports that one does in fact exist. As hypothesized, the inf ant was observed to spend the majority of time with a primary female. Although maternity of the infants was impossible to know due to lack of DNA testing, the primary female is assumed to be the mother of the focal individual, since Cebus mothers are known to have a frequent, affiliative relationship with their young (Robinson 1987). Although nursing behavior was observed several times during the nuzzle social interaction (FIG. 8), nursing is known to be a form of helping behavior in cebines and so this al one can not infer maternity of the infant (Robinson 1987). Regardless, the data supports a primary caretaker of the infant as well as many other individual interactions that may be construed as helping behaviors (APPENDIX 1). The fact that the infants sp ent the majority of their time with one caretaker demonstrates that they may be physically dependent on one primary individual to provide them with most of their biological needs. Therefore, it seems logical that female capuchins only produce singletons a t one to two year intervals because the young are so dependent until they reach five to six months of age when they achieve locomotory independence (Freese 1983). The hypothesis that females would make more approaches to infants than males was rejected because there was no difference between number of approaches made between female and male individuals. However, females do spend considerably more time involved in the interaction, as was theorized. Although female individuals lose considerable foraging t ime as well, they are presumed to spend more time involved in infant care than are males due to the increased gain of experience in parental care (Goldizen 1986). In addition, the fact that males approached infants the same number of times as females does not rule out the idea that males would have more of a time constraint due to significant loss of foraging and hunting time. In fact, this is possibly supported due to the fact that they spent considerably less time involved in the interaction with the in fant than did the females. A possible explanation for why males would invest some of their time to helping in infant care is to increase their own reproductive success by enhancing their repertoires to possibly qualify as next in line for alpha position, as alpha male is the only one to achieve substantial mating success (Robinson 1987). Further research is necessary to assess the gains for capuchin males to assist in this communal infant care system. Future studies should incorporate DNA sampling and mar ked individuals as well as marked sexes of all individuals involved to get a better idea of the conspecific interactions that occur between members within a given capuchin troop. Such testing could also be important to help assess whether or not the prima ry female is in fact the biological mother of the focal individual. It also would be interesting to study whether or not the infants exhibit a preference for those individuals involved in the infant communal care system and whether or not this is dependen t on sex. Overall, it seems possible that
7 such a system subsists in this species to lighten the strain placed on the mothers due to their active nature and seasonal foraging movements. ACKNOWLEDGEMENTS I would like to thank my advisor Javier MÃ©ndez in addition to Alan and Karen Masters, Oliver Hyman, and Matt Gasner for their support in this stubborn endeavor. My gratitude is extended to El Bosque Eterno de los Ninos, El Bajo del Tigre, Frank Joyce, Bob Law, and Susie Newswanger for letting me tromp around on their properties every morning. Thanks to El Bajo del Tigre staff Carlos AcuÃ±a, Susana Alfaro, and Rosie Fallas reviewing and editing my work. Finall y, thanks to the wild capuchins for providing me with interesting and amusing behaviors to observe. LITERATURE CITED Barnert, E.S. and C.L. Hendricks. 1999. Home range, travel paths, and energy allocation of a troop of white faced monkeys ( Cebu s capucinus ) in Monteverde. UCEAP IMV Monteverde Tropical Biology. Costa Rica: Monteverde Biological Station Library. Filipkowski, A. and E.W. Olson. 1998. Activity patterns of the white faced monkey ( Cebus capucinus ). CIEE Symposium on Tropical Ecology and Conservation. Costa Rica: Monteverde Biological Station Library. Freese, C. H. 1983. Cebus capucinus (Mono Cara Blanca, White Faced Capuchin). In: Costa Rican Natural History , D. H. Janzen, ed. The University of Chicago Press, Chicago, IL , pp. 458 460. Freese, C. H., and Oppenheimer, J. R. 1981. The capuchin monkeys, genus Cebus . In Ecology and behavior of Neotropical primates, vol. 1, ed. A. F. Coimbra Filho and R. A. Mitermeier. Rio de Janeiro: Academia Brasileira de Ciencias. As c ited in Robinson, J.G. and C.H. Janson. 1987. Capuchins, squirrel monkeys, and atelines: sociological convergence with old world primates. Cited in Smuts, B.B., et. Al. Primate Societies, (eds.) Chicago, 1987: University of Chicago Press. Goldizen, A. W. 1986. Tamarins and marmosets: communal care of offspring. Cited in Smuts, B.B., et. Al. Primate Societies, (eds.) Chicago, 1986: University of Chicago Press. Robinson, J.G. and C.H. Janson. 1987. Capuchins, squirrel monkeys, and atelines: sociol ogical convergence with old world primates. Cited in Smuts, B.B., et. Al. Primate Societies, (eds.) Chicago, 1987: University of Chicago Press. Terborgh, J. 1992. Diversity and Tropical Rainforest. New York: Scientific American Library.
8 APPENDIX 1. Interaction Types Attempted Grab the individual attempts to grab the infant from the primary female's back Carry the individual carries the infant on its own back after an approach Feed Nearby the individual feeds nearby th e infant, or the primary female with the infant feeds nearby the individual, both within one meter proximity Follow the individual follows the primary female with infant or the primary female with infant follows the individual, both within one meter proximity Groom Infant the individual is observed grooming the infant, whereby the individual comes up behind and picks at its hair Nuzzle the individual, along with the primary female and infant, lie down on a branch in a ball shape form with the infant in between them or on their backs; infant is assumed to be nursing during this time because it is attached to primary female's stomach when she gets up from position Ride the infant is on the back of an individual other than the primary female Threat Stance the individual stands in front and the primary female with infant positions directly behind this individual with teeth exposed in a threatening stance to appear bigger in size and ward off a predat or, in this instance a coati Touch the individual is observed touching with the infant 2. Miscellaneous Observations The majority of the time individuals foraged and moved along the trails. The time the troops foraged seemed to be random between 8am and 4pm. Troops seemed to partition foraging space by splitting off into smaller groups. Main activities were to rest, eat, travel, and engage in social interaction. Troops were observed eating Cecropia sp. (Cecropiaceae), Symplocos limo ncillo (Symplocaceae), and Persea Americana (Lauraceae) fruits along with random tree leaves and contents of Bromeliad tanks.
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Hook, Kristin, A.
La atencin comunitaria de la descendencia en el mono cara blanca (Cebus capucinus)
Communal care of offspring in the white-faced capuchin monkey (Cebus capucinus)
The purpose of this study was to document whether a communal infant care system existed in the whitefaced capuchin monkey, Cebus capucinus (Cebidae), in the Monteverde area. The intention was to draw comparisons in time allocation spent between infants and other individuals in the troops followed. In
addition, approach and leave times in interactions involving the infant and other members of the troop as well as the sexes of those individuals involved were documented. It was found that a communal infant care
system does in fact seem to exist for this species of primate. Infants spent the majority of their time on the backs of a primary female in addition to the backs of juveniles. The majority of approaches made were to engage in social interaction. The majority of approaches made by individuals other than the primary female were either solicitations or offers for rides. There was no difference in numbers of approaches
initiated by female or male individuals; however, females spent more time involved with the infant during their interactions than did the males.
El propsito de este proyecto fue documentar un sistema de custodia comunal de las cras de los monos carablanca, Cebus capucinus (Cebidae), en el rea de Monteverde. Se observaron tropas de monos con la intencin de hacer comparaciones entre las asignaciones del tiempo compartido entre las cras y otros individuos. Tambin se documentaron el tiempo de los acercamientos y las despedidas en las interacciones que involucraban a las cras y a otros miembros de la tropa, adems de los sexos de los individuos que estaban involucrados. Se encontr que el sistema de custodia comunal existe en esta especie de primate. Las cras pasaron la mayora del tiempo en las espaldas de una hembra primaria, seguido por el tiempo que pasaron en las espaldas de los juveniles. La mayora de los acercamientos ejecutados fueron para entretener en las interacciones sociales. La mayora de los acercamientos ejecutados por individuos que no eran la hembra primaria fueron solicitaciones u ofertas para paseos. No hubo diferencias en el nmero de acercamientos ejecutados por las hembras o los machos; sin embargo, las hembras pasaron ms tiempo que los machos con la cra durante las interacciones.
Text in English.
Parental behavior in animals
Costa Rica--Puntarenas--Monteverde Zone
Comportamiento paterno en animales
Costa Rica--Puntarenas--Zona de Monteverde
Tropical Ecology Spring 2005
Ecologa Tropical Primavera 2005
t Monteverde Institute : Tropical Ecology