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 (Ribeiro et al. 2009). The forest fragment includes both native and exotic fruit trees (such as Ficus sp., Syagrus romanzoffiana Cham., Jacaratia spinosa Aubli., Morus nigra L., Mangifera sp. L., Psidium sp. L., Eriobotrya japonica Thunb., Persea americana Mil.). The fragment is surrounded by houses and small corn and soy plantations. The climate is classified as humid subtropical (mean temperature 21 °C, ranging from 40 °C in the Summer to 0 °C during Winter), with annual average rainfall of 1,700 mm (Alvares et al. 2013).

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; Suzin et al. 2017). The city government has been provisioning food (fruits and meat) to the monkeys on a platform three times a week since August 2012, and human visitors frequently feed them as well (0.4 human-monkey interactions/h, in which 58% of the interactions were people feeding the monkeys, Suzin et al. 2017). The bulk of the diet (71% of feeding records) is anthropic food, mainly given by human visitors (44% of feeding records; e.g., fruit, bread, candy, and meat) and by the city government (Suzin et al. 2017). These monkeys, especially juveniles, often forage by manipulating natural (e.g., sticks, hard fruits) and anthropic objects (e.g., cans, plastic bottles; 1 events/h in the group; G.F. Silva unpublished data), including tool use (Aguiar et al. 2014). We did not observe the occurrence of natural predators, human hunting, or other human-monkey conflicts in the area during the study, and such events have not been mentioned in any interviews with local people (Suzin et al. 2017).

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 Izawa (1980). We recorded the individuals’ activity within three minutes at every 7-min interval, using the scan sampling method (Altmann 1974), taking care to not capture records from the same individual during each sampling. We distinguished the categories of the activity budget into “foraging” (including visual and/or tactile exploration, capturing and/or handling any object or food item), “traveling”, “feeding”, “resting”, “social interaction” (including only dyadic interactions: affiliative, agonistic, cooperative, and sexual), and “others” (including vigilance, drinking, defecating, urinating, urine washing, and interactions with observers; adapted from Fragaszy et al. 2004).

We used an adapted version of the All Occurrences sampling method (Altmann 1974) to collect data on social interactions, since we were not sure if all individuals of the group were within our sight at any given instant, as required by the method. We collected data for all events of social interactions of the dyads within sight during the followings of the capuchin group. We considered as affiliative interactions grooming and social play, which are associated with the development and maintenance of social bonds (Wilson 2000, Sussman et al. 2005). We considered two degrees of agonistic interactions according to physical contact (Wilson 2000): aggression (pushing, hitting, grabbing, wrestling, biting), and threats (silent or vocalized facial displays, lunging, swiping, bouncing, and chasing) (Leca et al. 2002). We considered sexual interactions as behaviors of female proceptivity, including touching and displays (eyebrow raises, head and body tilts), inspections of genitalia, and copulations (Fragaszy et al. 2004, Carosi et al. 2005, Lynch-Alfaro 2005). We considered cooperative interactions as the alloparental carrying of the young on the back and food sharing, because these behaviors initially impose costs to the initiator, but can promote mutual benefits (by kinship or reciprocity; Davies et al. 2012). We were able to discriminate between parental and alloparental carrying (hereafter “allocarrying”) because the infants’ maternal relationships were known. Finally, we considered food sharing as all events of one individual collecting or receiving food directly from the hands or the mouth of another monkey (adapted from Hattori et al. 2012).

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 (Fortes and Bicca-Marques 2005). For this estimate, we divided the number of records of each category of behavior per each hour of observation (e.g., 7:00–7:59, 8:00–8:59, ... 16:00–16:59) by the total number of behavioral records, for each sex-age class.

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 (Whitehead 2008). We calculated the frequencies of events (in percentage) for each social behavior in each dyad, considering the total number of events of dyads of the respective behavioral category. We used the G-test to test the homogeneity of emissions, receptions and participations (emissions plus receptions) among sex-age classes. For this analysis, we used the proportion (events/number of individuals in each sex-age class) of emission, reception and participation of each sex-age class. The expected frequency of the emissions, receptions, and participation for each class was calculated considering the mean of the events of each direction of behavior divided by the number of individuals in each sex-age class. The infants were excluded as emitters of allocarrying and food sharing, and the adult male, adult females, and subadults were excluded as receivers of allocarrying.

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 (Ayres et al. 2007), with a significance level of p ≤ 0.05.

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. 1), the time spent in other activities significantly varied across sex-age classes (traveling: H = 25.3850; DF = 3; P<0.0001, foraging: H = 22.8137; DF = 3; p < 0.0001; resting: H = 16.8240; DF = 3; p < 0.0080; social interaction: H = 20.2731; DF = 3; p < 0.0001; Fig. 1). Juveniles rested less than the adult male, although they foraged more than other sex-age class and socialized more than adult females and subadults (Fig. 1). Adult females traveled more than juveniles (Fig. 1).

Figure 1. 

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. 2). Participation and grooming emission by adult females and the grooming reception by juveniles were higher than expected by chance (Table 1, Fig. 3). Reciprocal grooming between adult females was rare (n = 4 events). Adult females were groomed primarily by the adult male, and groomed primarily juveniles (Fig. 3).

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 1; Fig. 4). Adult females emitted more and adult male received less threats than expected by chance (Table 1; Fig. 4). The distribution of participations in aggressions among sex-age classes did not differ from expected by chance, but juveniles received more aggressions than expected (Table 1; Fig. 5).

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 1). Juveniles emitted more, and infants received more allocarrying than expected by chance (Table 1; Fig. 6). Juveniles participated in food sharing more and received four times more shared food than expected by chance (Table 1; Fig. 7). The adult male and adult females were the most frequent sharers with juveniles, though with no statistical significance.

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.

Figures 2–7. 

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.

Table 1.Download as CSV 

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.

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 (Rímoli et al. 2008); and S. libidinosus (Sabbatini et al. 2008, Verderane et al. 2013). We believe that the high investment in traveling might be explained by the scattered distribution of food offered by people, their primary food resource, in space and time (Suzin et al. 2017). This has been previously described for long-tailed macaques – M. fascicularis (Sha and Hanya 2013). In fact, capuchin-people interactions were frequent in our site, mainly in the context of provisioning (Suzin et al. 2017). However, the high investment in foraging could also be a result of the large amount of objects discarded by humans in the fragment, resulting in a high frequency of manipulation of objects (G.F. Silva unpublished data).

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 (Jaman and Huffman 2013). Consequently, the use of the anthropic food can be associated with a decrease in time spent in feeding and increase in resting time, as observed for Papio cynocephalus Linnaeus, 1766 (Altmann and Muruthi 1988) and M. mulatta (Jaman and Huffman 2013). The capuchins in this study spent less time feeding, but they also spent less time resting, which contrasts with the pattern described above for animals with access to anthropic food. This low investment in rest could be explained by the frequent human stimulus, as also observed in captive gracile capuchins, Cebus olivaceus Schomburgk, 1848, by Tárano and López (2015). In our study site, humans frequently use the fragment as path shortcuts and often contact and feed the capuchins (Suzin et al. 2017).

The time spent in social interactions by the study group (almost 5%) is similar to those reported for wild capuchins (3% for S. cay: Pinto 2006, 4% for S. nigritus: Rímoli et al. 2008, 5% for S. libidinosus: Cutrim 2013) than those reported for provisioned capuchins (8% and 10% by S. libidinosus: Sabbatini et al. 2008, Sacramento et al. 2017, respectively). We believed that the small amount of time spent in social interactions may be explained by the scattered distribution of people-offered food, which can reflect in decreased proximity between the members of the group, which means fewer opportunities for socialization. The existence of only one adult male and the absence of neighboring groups might also be a factor lowering the amount of social interactions. The low investment in social interactions performed by adult females, when compared to juveniles, may be due to their apparent low cohesiveness (J.P. Back personal observation). This is also probably a result of the scattered distribution of local anthropic food as described above. The low investment in foraging and high investment in traveling (probably to find people with food) support this interpretation. Finally, although juveniles and subadults may have more scarce access to food (Janson and van Schaik 1993), we did not observe significant differences in time spent in feeding among sex-age classes, which could be a result of the availability of abundant and frequent anthropic food supplementation, allowing access to all individuals.

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 (Robinson 1986). Juvenile capuchins might be foraging more due to their curiosity and lower access to food (Janson and van Schaik 1993, Fragaszy et al. 2004). The high proportion of time invested in social interactions by juveniles may be associated with the high number of young individuals in the group, contributing to increased time spent on social play, as also observed in captive gracile capuchins (Tárano and López 2015).

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 (Fragaszy et al. 2004, Izar et al. 2006). The overwhelming predominance of positive interactions (90%: affiliative plus cooperative) in this study reflected high tolerance among individuals. This may also be a consequence of the anthropic food supplementation, which allows all individuals in the group to find food, relaxing within-group competition (Altmann and Muruthi 1988, Jaman and Huffman 2013). In addition, the restriction to spatial dispersion imposed by the urban matrix surrounding the forest fragment could increase kinship among these capuchins, contributing to positive interactions (Strier 2011, Davies et al. 2012). Most affiliative interactions consisted of social play, primarily performed by juveniles, as found in other studies (Resende and Ottoni 2002, Fragaszy et al. 2004). We believe the presence of several young immature individuals in the group, which are more socially active (Resende and Ottoni 2002, Fragaszy et al. 2004, Schino and Pinzaglia 2018), may have favored the occurrence of this behavior.

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 (Di Bitetti 1997) to 2 events/h for Sapajus apella Linnaeus, 1758 (Izawa 1980), although there were some apparent deviations in grooming patterns for females and the alpha male. For example, adult females groomed less among themselves and reciprocal grooming among females was rare (<0.01 events/h) in comparison to other observations in conserved habitats (O’Brien 1993, Perry 1996, Di Bitetti 1997, Tiddi et al. 2011). The grooming of the adult females to alpha male was also infrequent. Conversely, adult females were mostly groomed by the alpha male. Cases of weak interactions among robust capuchin females have been attributed to females’ spatial dispersal (Izar et al. 2012). Because female transfer is unlikely in the study area, the low frequency of interactions among adult females could be associated with the detachment produced by the scattered distribution of anthropic food. However, other factors could be operating, such as age, lack of competing groups in the fragment, and low risk of predation, which may also contribute to lower cohesiveness, restricting opportunities for social interactions among adult females and the dominant male (Janson 1984, Koenig 2002, Strier 2011, Tiddi et al. 2011, Schino and Pinzaglia 2018). On the other hand, the dominant male may still need to secure mating, which would explain the high rates of grooming towards the adult females (Janson 1984, Tiddi et al. 2011). As expected, adult females invested more time grooming the young, probably due to parental and alloparental care (Izawa 1980, Fragaszy et al. 2004). Female grooming towards juveniles could have other functions and express appeasement, due to frequent female agonism towards juveniles, or even a mechanism of reciprocity, because juveniles are the main helpers in the group (see below). Additionally, the fact that there was only one adult male in the group could be leading females to groom juveniles that might be their potential partners in the future.

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 (Phillips 1995) and for S. apella (Ferreira et al. 2008), and again could be a reflect of the daily provisioning that decreased competition for food. The heterogeneous distribution of food provided by humans may contribute to the scattered distribution of foraging individuals, resulting in fewer opportunities for agonist interactions (Janson and Vogel 2006). Threats were much more common than aggressions, probably because aggressions demand a greater amount of energy, and may cause injuries or even death (Strier 2011). As expected from their low social status (Ferreira et al. 2008, Strier 2011), juveniles were the main receivers of threats from adult females and aggression from the dominant male. The agonism among juveniles and adult females can emerge due to their physical and social proximity (Fragaszy et al. 2004), particularly when humans offer food to attract them. Aggressions emitted by the dominant male towards juveniles can emerge not only because of human provisioning but also due to the frequent participation of juveniles in sexual behaviors (Janson 1985), as observed here.

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 (Strier 2011, Davies et al. 2012). Adult capuchins shared food primarily with juveniles (almost 60%), which could also be viewed as a form of parental or alloparental care. Adult food sharing could be also interpreted here as a payoff for the allocarrying of infants performed by juveniles – a mechanism of indirect reciprocal altruism (O’Brien 1993, Davies et al. 2012).

As expected for robust capuchin breeding systems, the dominant male was the preferred partner in sexual interactions (Carosi et al. 2005, Izar et al. 2012). However, sexual interactions observed in this study were rare in comparison to other studies (e.g., Lynch-Alfaro 2005): the proceptivity of females was markedly reduced, and juveniles were frequently involved (45% of the events). It is noted that our sampling effort could disfavor observation of sexual behavior where reproduction is seasonal (e.g., S. nigritus: Di Bitetti and Janson 2001). However, because sexual seasonality often follows food resources seasonality, there is a possibility that constant human food provisioning might lead to occurrence of sex and births in our study group throughout the year, as partially supported by the births observed: two during the Winter (one in September 2011 and one in August 2012) and three in the Summer (between December 2012 and January 2013). We believe the presence of a single adult male in the group and the urban constraints to dispersion from the natal group could favor the engagement of juveniles in sexual interactions. If the supposed increased kinship could be demotivating towards courtship among relatives (Strier 2011, Davies et al. 2012), on the other hand, juveniles may take opportunities that are unlikely to occur outside the natal group.

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 (Di Bitetti and Janson 2001) suggest high-energy input for these urban capuchins, future studies should also investigate the impact of human presence and food on the health and welfare of these monkeys. These kind of studies are very important in Primate Conservation Biology, because we have an urgent demand to understand how primates adapt around human beings, as the contact between human and nonhuman primates are an inescapable aspect today.