Research Article |
Corresponding author: Janaína P. Back ( janainapaulajpb@gmail.com ) Academic editor: Diego Astúa
© 2019 Janaína P. Back, Adriane Suzin, Lucas M. Aguiar.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Back JP, Suzin A, Aguiar LM (2019) Activity Budget and Social Behavior of Urban Capuchin Monkeys (Sapajus sp.) (Primates, Cebidae). Zoologia 36: 1-10. https://doi.org/10.3897/zoologia.36.e30845
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Constant changes in natural environments impose challenges to wild animal populations, especially those that depend on social life. We gathered data on the activity budget and social interactions of a capuchin monkey (Sapajus sp.) group of 17 individuals confined to an urban green area receiving human food supplementation. We observed the capuchins between 7:00 am and 5:00 pm, three days a month, between January 2012 and June 2013 (total of 530 hours of direct observations). We collected 15,208 behavioral records through instantaneous scan sampling and 2,538 events of social interaction in an adapted version of the “all occurrences” method. Activity budget of capuchins was dominated by traveling (42%) and foraging (38%), followed by feeding (10%), social interactions (5%), resting (4%), and others (2%). Except for feeding, the time spent on other activities varied across sex-age classes. Social interactions of capuchins were dominated by affiliative interactions (80%), mainly social play, followed by agonistic (11%) and cooperative (10%) interactions. Sexual interactions were rare (0.4%) and often involved juveniles (45% of the events). Juveniles performed most of the social interactions, followed by the alpha male, and were the main receptors of grooming, food sharing, and agonism. On the other hand, they were the main group involved in allocarrying of infants. Grooming between females and from them to alpha male was infrequent. However, grooming of the alpha male towards the adult females was frequent. We interpreted the deviations in the activity budget and social interactions of the urban capuchins as effects of human food supplementation and restriction on dispersal, illustrating the behavioral ability of capuchin monkeys to adjust their activity in human-altered environments.
Anthropic influence, food provisioning, Neotropical primates, urban wildlife
The growth of human populations and the consequent changes suffered by natural environments have forced populations of nonhuman primates (hereafter “primates”) to adapt to the effects of habitat fragmentation. These changes include impacts on matrix permeability, quality and abundance of food resources, demography, sexual partnership, and inter-specific interactions (
Forest fragmentation and human interference tend to reduce the risk of predation by natural predators, to limit migration and to introduce high-energy aggregated food resources (
Capuchin monkeys (Cebus Erxleben, 1777 and Sapajus Kerr, 1792 – Primates: Cebidae) are omnivorous Neotropical primates with flexible social and feeding behavior (
Robust capuchins (Sapajus spp.) live in multi-male, multi-female polygynic groups (3–30 individuals), where females tend to be philopatric and males tend to migrate before reaching sexual maturity (
In the municipality of Foz do Iguaçu, southern Brazil, a group of robust capuchins survives confined to a small forest fragment in an urban area, with frequent contact with humans (
The study group lives in a 3.7 ha forest fragment (25°28’ 56.1”S; 54°33’55.9”W; DMS) within the urban matrix of the municipality of Foz do Iguaçu, state of Paraná, southern Brazil. This area is considered as a Municipal Reserve. The vegetation is classified as Seasonal Semi-deciduous Forest, within the Atlantic Forest Domain (
The study group comprised 17 individuals: one adult male, five adult females, three subadults, three juvenile, and five infants. These capuchins are confined to this forest fragment because the urban matrix impedes connectivity with other forest patches. Although Sapajus nigritus (Goldfuss, 1809) occurs naturally in this region, the coats of individuals in this group are blonder and they resemble Sapajus cay (Illiger, 1815). Therefore, they are referred here as Sapajus sp. According to local people, these capuchins have been present in the area for about 35 years, and were most likely introduced. They forage on and eat resources of the forest fragment, but also from human dwellings and crops, including human food leftovers (e.g., rice, beans, candy, and soda;
We habituated the group to the presence of human observers between September and December 2011. Posteriorly, we followed and observed the group between 07:00 am and 5:00 pm, for three days a month, between January 2012 and June 2013. We classified the individuals in sex-age classes (adult male, adult female, juvenile, subadult and infant) according to
We used an adapted version of the All Occurrences sampling method (
We estimated the activity budget (e.g., feeding, foraging, traveling, resting, and socializing) for each sex-age class (except for infants, due to their dependence on mothers) through the method of proportions (
We used a Kruskal-Wallis non-parametric ANOVA to compare the proportion of records of each category of behavior of the activity budget for the sex-age classes, as these behavioral records were not normally distributed. Dunn’s post-hoc test was used for the pairwise comparisons of the respective proportions. We analyzed the social interactions through sociometric matrices and the relationships among dyads of sex-age classes were expressed in social webs (
We assessed data normality and homoscedasticity with the Shapiro-Wilk and Levene tests, respectively. All tests were performed using the BIOESTAT 5.3 software package (
We obtained a total of 15,208 observation records (adult male: n = 1,683; adult females: n = 3,968; juveniles: n = 8,978; subadults: n = 759) in 3,180 scans and 2,538 events of social interactions during 530 hours of direct observation distributed in 53 days of sampling effort.
The activity budget was dominated by traveling (42% of records; n = 6,390) and foraging (38%; n = 5,740), followed by feeding (10%; n = 1,497), social interactions (5%; n = 730), resting (4%; n = 559), and others (2%; n = 359). Except for feeding (H = 2.7916; DF = 3; p = 0.4249; Fig.
Proportions of records (in percentage) of behavioral categories in the activity budget of sex-age classes of urban capuchin monkeys. Boxes represent the interquartile ranges; horizontal lines within the boxes represent the medians; whiskers indicate minimum and maximum values; circles indicate the proportions of records per hour of observation. Different letters indicate significant differences between sex-age classes. Kruskal-Wallis followed by Dunn’s test; p ≤ 0.05. (AF) adult females, (AM) adult male, (SUB) subadults, (JUV) juveniles.
The most frequent social interactions were affiliative interactions (80% of events; n = 2,023), followed by agonistic (11%; n = 272), cooperative (9%; n = 232), and sexual interactions (0.4%; n = 11). Juveniles were the sex-age class most involved in interactions (732 events/individual), followed by the adult male (441 events/individual), adult females (122 events/individual), infants (63 events/individual), and subadults (54 events/individual).
The most frequent affiliative interactions (4 events/h) consisted of social play (73%; 3 events/h), followed by grooming (27%; 1 event/h). Juveniles comprised the most frequent dyad composition during social play (Fig.
The most frequent agonistic interactions (0.5 events/h) were threats (89%; 0.4 events/h), followed by aggressions (11%; 0.06 events/h). Juveniles were more often involved (emitting plus receiving) in threats than expected by chance (Table
The most frequent cooperative interactions (0.4 events/h) consisted of allocarrying (83%; 0.4 events/h), followed by food sharing (17%; 0.07 events/h). Juveniles and infants participated in allocarrying more than expected by chance (Table
Sexual interactions were infrequent (n = 11; 0.02 events/h), and the adult male participated in 73% of the interactions. Among sexual interactions, we observed six copulations, four sexual displays, and one inspection of genitalia. All sexual displays preceded the observed copulations. The adult male copulated with an adult female (n = 2), with a subadult female (n = 1), and with a juvenile (n = 1). Two copulations involved one juvenile with a subadult female. Inspection of genitalia was done by the adult male towards a subadult female, whereas sexual displays were done mostly towards the adult male from subadult females (n = 2), and from a juvenile (n = 1). A juvenile performed one sexual display towards a subadult female.
Social webs expressing interactions (in percentage of the total observation records) for each sex-age dyad of urban capuchin monkeys in each social behavior: (2) social play, n = 1,476 events; (3) grooming, n = 547; (4) threat, n = 241; (5) aggression, n = 31; (6) allocarrying, n = 193; (7) food sharing, n = 39. Percentages of emissions and receptions are in decreasing order in all columns, except for social play. Line thickness is proportional to the percentages of interactions of each dyad. (AF) adult females, (JUV) juveniles, (AM) adult male, (SUB) subadults, (INF) infants.
Proportions (events/number of individuals in each sex-age class) of emissions, receptions, and participations (emissions plus receptions) observed (in bold) and expected (bottom line) for social interactions within each sex-age class of urban capuchin monkeys. AF = adult females, JUV = juveniles, AM = adult male, SUB = subadults, INF = infants, DF = degrees of freedom.
Behavior | Direction of behavior | Events/number individual of each sex-age class | Test value | |||||||
AF | AM | SUB | JUV | INF | G | DF | p | |||
Grooming | Emission | 49.4 | 177.0 | 9.0 | 31.3 | 0.4 | 70.88 | 4 | <0.0001* | |
21.9 | 109.4 | 36.5 | 36.5 | 21.9 | ||||||
Reception | 31.4 | 71.0 | 8.0 | 64.0 | 20.6 | 35.24 | 4 | <0.0001* | ||
21.9 | 109.4 | 36.5 | 36.5 | 21.9 | ||||||
Participation | 80.8 | 248.0 | 17.0 | 95.3 | 21.0 | 60.50 | 4 | <0.0001* | ||
43.8 | 218.8 | 72.9 | 72.9 | 43.8 | ||||||
Threats | Emission | 14.6 | 44.0 | 5.3 | 36.0 | 0.0 | 27.69 | 4 | <0.0001* | |
9.6 | 48.2 | 16.1 | 16.1 | 9.6 | ||||||
Reception | 11.6 | 24.0 | 15.0 | 38.0 | 0.0 | 29.55 | 4 | <0.0001* | ||
9.6 | 48.2 | 16.1 | 16.1 | 9.6 | ||||||
Participation | 26.2 | 68.0 | 20.3 | 74.0 | 0.0 | 51.87 | 4 | <0.0001* | ||
19.3 | 96.4 | 32.1 | 32.1 | 19.3 | ||||||
Aggression | Emission | 0.8 | 16.0 | 0.3 | 3.3 | 0.0 | 8.86 | 4 | 0.0645 | |
1.2 | 6.2 | 2.1 | 2.1 | 1.2 | ||||||
Reception | 0.6 | 0.0 | 0.7 | 7.0 | 1.0 | 14.61 | 4 | 0.0056* | ||
1.2 | 6.2 | 2.1 | 2.1 | 1.2 | ||||||
Participation | 1.4 | 16.0 | 1.0 | 10.3 | 1.0 | 5.36 | 4 | 0.2519 | ||
2.5 | 12.4 | 4.1 | 4.1 | 2.5 | ||||||
Allocarrying | Emission | 5.4 | 4.0 | 6.7 | 47.3 | – | 60.84 | 3 | < 0.0001* | |
9.6 | 48.2 | 16.1 | 16.1 | – | ||||||
Reception | – | – | – | 2.0 | 37.4 | 36.20 | 1 | < 0.0001* | ||
– | – | – | 32.2 | 19.3 | ||||||
Participation | 5.4 | 4.0 | 6.7 | 49.3 | 37.4 | 103.45 | 4 | < 0.0001* | ||
15.4 | 77.2 | 25.7 | 25.7 | 15.4 | ||||||
Food sharing | Emission | 3.2 | 11.0 | 0.3 | 3.7 | – | 5.40 | 3 | 0.1463 | |
1.9 | 9.7 | 3.2 | 3.2 | – | ||||||
Reception | 0.4 | 0.0 | 0.0 | 10.7 | 1.0 | 19.50 | 4 | 0.0006* | ||
1.6 | 7.8 | 2.6 | 2.6 | 1.6 | ||||||
Participation | 3.6 | 11.0 | 0.3 | 14.3 | 1.0 | 12.96 | 4 | 0.0114* | ||
3.1 | 15.6 | 5.2 | 5.2 | 3.1 | ||||||
Statistically significant differences between observed and expected proportions are indicated by asterisk (*). G-test, p ≤ 0.05. |
Overall, the observed urban capuchin monkeys spent almost 80% of time searching for food (traveling plus foraging), and only 10% of time feeding. Except for feeding, the time spent in all other activity groups (foraging, traveling, resting and socializing) varied across sex-age classes. We found that an overwhelming majority of social interactions was affiliative (almost 80% of social interactions), especially juvenile social play. Grooming interactions between females and from them to the alpha male were infrequent. However, grooming of the alpha male towards adult females was frequent. Juveniles were the main receptors of grooming, food sharing and of threats of the adult females and of aggressions of the adult male. On the other hand, the juveniles were the main emitters of the allocarrying for infants. Sexual interactions were infrequent in the group and unusually involved juveniles.
The time spent in traveling and foraging by the observed capuchin monkeys was higher when compared to populations of robust capuchins in larger fragments and continuous forest – S. nigritus (
On the other hand, the low feeding rate observed here could be explained by the high energetic content and availability of food offered by people, satisfying individual demands with less effort and a smaller amount than those provided by the forest (
The time spent in social interactions by the study group (almost 5%) is similar to those reported for wild capuchins (3% for S. cay:
Regarding sex-age classes, juveniles invested more time in foraging and less in traveling than other classes, which is similar to previous observations in gracile capuchins (
Social interactions were mostly performed by juveniles, followed by the adult male, indicating their integration in the social structure of this group. On the other hand, subadults were the least frequent participants, probably due to their subordinate status or peripheral position, usual in robust capuchins (
The frequency of grooming behavior found in our study (1 event/h) is similar to the rates observed for wild robust capuchins, with 1 events/h for Sapajus nigritus Goldfuss, 1809 (
The rates of agonism observed in our study group (0.5 events/h) was low when compared to other capuchin groups: 1 event/h for C. capucinus (
Most cooperative interactions involved juveniles, including allocarrying of infants, their probable siblings or cousins, as well as receiving food from adults, their probable parents, grandparents, or uncles. The allocarrying of infants performed by juveniles not only offers advantages in terms of energetic economy for the parents but can also enhance their own genetic fitness when they care for their kin, as they might be gathering experience to take care of their own offspring in the future (
As expected for robust capuchin breeding systems, the dominant male was the preferred partner in sexual interactions (
In conclusion, we found deviations in activity budget and social interactions of capuchins living in the studied small urban fragment, possibly influenced by the availability of anthropic food and the restrictions for dispersion imposed by the urban matrix. However, we cannot rule out the possibility that other factors have shaped the behavior of these animals. Therefore, future studies should investigate specifically the effects of dispersal restriction and food given by people on the behavior, demography and genetics of these animals. Although the disparate high population density (4.9 individuals/hectare; J.P. Back unpublished data) and the annual birth rate (0.7 births/adult/female, J.P. Back unpublished data) similar to those of wild populations in conserved habitats (
We would like to thank UNILA and Fundação Araucária for the scholarships provided to J.P. Back and A. Suzin, and the City Government of Foz do Iguaçu for the permits to conduct the study. We also thank Alexandre Vogliotti, María Celia Baldovino, Michel V. Garey, José Eduardo Silva Pereira, editors and the anonymous reviewers that provided useful comments on the manuscript.