Social Behavior Adaptations in Agroup of Black-And-Gold Howler Monkeys (Alouattta Caraya; Primates, Atelidae) Inside an Urban Forest in the Southeast of Brazil

Home , Atelinae, Black howler, Mantled howler

Current Ethology 2016, Vol.15, N°2, 1-15

Social behavior adaptations in agroup of black-and-gold howler monkeys (Alouattta caraya; Primates, Atelidae) inside an urban forest in the southeast of Brazil

RICARDO SAMPAIO1*, HUGO LOPES GOMES2, ZELINDA MARIA BRAGA-HIRANO3, JULIANA MOUTINHO PEDROSA4, AND WAGNER FERREIRA DOS SANTOS2,4,5

Primates of the Alouatta genus arefolivore - frugivore, resulting in a strategy of reduced energy expenditure, and the spatial relationships between these animals may constitutean important indication of how they establish their social organization. This study aimed to evaluatethe social behaviorof a group of black-and-gold howler monkeys (Alouata caraya) in an urban forest (3 ha) located in Ribeirão Preto (21º10’17” S and 47º48’05” W; São Paulo, Brazil). Thisgroup was organized in a harem systemthat faced instability,although during the study an age-graded system seems to have been stablished in the group. Amatrifocal subgroup was located in the center of the group and a male coalition was located in its periphery. However, this setting changed over the year. Few agonistic episodes were observed (2),and the inter-individual competition seemed reduced due to the high availability of fruit. This study providesimportant information about the plasticity in the social behavior of black-and-gold howler monkeys under the influence of anthropic actionand isolation of habitat. Keywords: Black howler monkey, urban forest, Alouatta caraya, social interaction.

Adaptações do comportamento social em um grupo de macacos bugios pretos e dourados (Alouatta caraya; Primatas, Atelidae) dentro de uma floresta urbana no sudeste do Brasil.

Os primatas do gênero Alouatta são descritos como folívoros - frugívoros, o que pode levar a uma estratégia de redução do gasto energético e o relacionamento espacial entre indivíduos pode constituir uma importante indicação de como um grupo estabelece sua organização social. Nosso estudo avaliouo comportamento social de um grupo de bugios pretos e dourados (Alouata caraya) em uma floresta urbana (3 ha) em Ribeirão Preto (21º10’17 ”S e 47º48’05” W; São Paulo, Brasil). Este grupo se organizou em um sistema de harém, enfrentando instabilidade, porém ao longo do estudo um sistema por ordem de idade parece ter sido estabelecido no grupo. Um subgrupo matrifocal estava localizado no centro do grupo e uma coalizão de machos na periferia, mas essa configuração mudou ao longo do ano. Vimos somente poucos episódios agonísticos (2) e a competição interindividual pareceu diminuída devido à alta disponibilidade de frutos. Este estudo fornece importante informações sobre a plasticidade no comportamento social de bugios vivendo sob influência da ação antrópica e isolamento do hábitat. Palavras chaves: Bugio preto, floresta urbana, Alouatta caraya, interação social.

1 Postgraduate Program in Comparative Biology (FFCLRP-USP), Ribeirão Preto, SP, Brazil 2 Postgraduate Program in Psychobiology (FFCLRP-USP), Ribeirão Preto, SP, Brazil 3 Regional University of Blumenau (FURB), Blumenau, SC, Brazil 4 Biology Department, Collegeof Philosophy, Sciences and Literature of Ribeirão Preto - University of São Paulo (FFCLRP-USP); Bar- ba-Negra Project,Ribeirão Preto, SP, Brazil 5 Behavioral Neurosciences Institute (INeC), Ribeirão Preto, São Paulo, Brazil * Corresponding author: Wagner Ferreira Dos Santos. Av. Bandeirantes, 3900. Ribeirão Preto,São Paulo, Brazil. CEP: 14040-901 Origin of the work: This workis part of the monography presented in the Biology Department, Collegeof Philosophy, Sciences and Litera- ture of Ribeirão Preto - University of São Paulo (FFCLRP-USP) as a requirement forthe obtainment of the first author’sBachelor’sDegree in Biological Sciences.

1 Ricardo Sampaio, Hugo Lopes Gomes, Zelinda Maria Braga-Hirano, Juliana Moutinho Pedrosa, and Wagner Ferreira dos Santos

INTRODUCTION Based on indirect signs expressed byinter-individual distance between all in- Howler monkeys (Alouatta) are consi- dividuals, we analyzed, during the course of dered to have a strategy to reduce energy ex- a year, the social behavior of a black-and- penditure (Crokett & Eisenberg, 1987; Mil- -goldhowler monkey group (A. caraya) li- ton, 1999, 2000; Strier, 1992).This pattern ving in an isolated urban fragmented forest behavior is probably related to a more folivo- of 25 hectares inside of thecity of Ribeirão rousthan frugivorous diet (Garber 1987, Ne- Preto(São Paulo, Brazil). We expected this ville et al., 1988, Pavelka & Knopff, 2004), groupto befacing high anthropogenic im- in which amechanism of substance detoxifi- pact living inside this isolated forest frag- cationto extract energy from leavesleads to ment, since the intra-individual competition an inactive behavior (Glander, 1975). for resources can be high, and subordinated In the social system ofhowler monke- individuals could not immigrate to other ys,inter-individual aggression israre (Alt- areas,resulting in instability in the social mann, 1959; Carpenter, 1934; Southwick, structure of the group. 1963),and theyorganize their communica- Considering this information, we have tion and social behavior by means of indi- three predictions about their social structure: rect signals (approaching and retreating), 1st) The group presentsa multi-male system with unusual episodes of bouts and vocali- with social and hierarchic structure;2nd) The- zations (Jones, 1982; Jones, 1983; Wang& re are signs of instability and of formation of Milton, 2002). Researchers believe that the- subgroups; and 3rd) The group shows a weak se signals, as well as grooming, are more pacific trend in its social behavior. related to the maintenance of a group-hie- In order to corroborate these predic- rarchic social structure than to agonistic tions, we will answer the following ques- behaviors (Jones, 1982). Therefore, the tions: 1) Do the adult males have different spatial relationship between individuals in access to the adult females?; 2) Is there a a howler monkey group can be an important formation of subgroups, and how arethey indication of how they relate and organize built?;and 3) Is there too much aggression their hierarchic social structure (Altmann, in the group, and which individuals are the 1959; Jones, 1980; Wang & Milton, 2003; most involved? Bezanzon et al., 2002 and 2008). The social groups of howler monkeys are organized in many patterns, from a typi- METHODS cal harem – where a dominant male restricts the access to females –to large groups with This study was performed at Parque several males, which shows a hierarchical Municipal Morro de São Bento (PMMSB) social structure and differentiated access to -21º10´17´´ S, 47º48´05´´ W, which is located females (Eisenberg et al., 1972; Neville et in the city of Ribeirão Preto (São Paulo, Bra- al., 1988), the latter being described for the zil). The PMMSB is a park (25 ha, Figure 1) species A. palliata,A. pigra, A. seniculus,and that features the City Zoo, as well as being a A. caraya (Crockett & Eisenberg, 1987; Ru- semi-deciduous and deciduous mesophyllous miz, 1990; Kowalewski, 2000). However, forest fragment of approximately 3 ha (Lagu- some individuals can form subgroups as na, 1997). This area contains native and exotic facultative responsesto different social and plant species and wasformally homologatedas ecological conditions (Kinzey & Cunnin- an Environmental Protection Area (Área de gham, 1994; Kappeler & van Schaik, 2002). Proteção Ambiental; APA).

2 Social behavior of black-and-gold howler monkeysin an urban forest

Figure 1. Representative map of the location of the city of Ribeirão Preto in Brazil (left), and the satellite image (Google Earth) from the Parque Municipal Morro de São Bento (PMMSB) showing the isolated urban forest fragment inside the city(right).

A four-month period (Jun-Oct, 2000) between two individuals. Inter-individual was necessary for the animals’ habituation distances greater than 3 meters were recor- with the researchers. During the same period, ded, but were not used in our analyses. the group was censured and only one group The ad libitum method (Altman, of 17 individuals was confirmed. The animals 1974), was used to analyze our predictions were grouped using age and gender catego- #1 and 3, in which any social interactions- ries, according to Calegaro-Marques and Bic- between the individuals, like conflicts, ca-Marques (1993): Adult Males (M); Adult agonistic behavior and sexual behavior Females (F); SubadultMales (SAM); Juveni- was sampled during all the study period. les (J); Infants (I). The subadult female cate- The scan sampling method was employed gory was not defined, for it was difficult to (Altman, 1974)to analyze our prediction #2, distinguish it category from juveniles. in which the spatial relationship between all All membership was separated in- the members of the group was sampled in a the following classes: M, F, SAM, J, and 20-minute intervals. I;as well as receiving codes (e.g.: M1-2, The study was divided into four social SAM1-4, F1-5). It was not possible to dis- dynamic phases (Table 1), varying in accor- tinguish individuals within the juvenile cate- dance with the composition of the group, gory, but they were included in the analysis which directly affected the social dynamics and were classified in order of appearance in and interactions between the individuals in each sampling period (J1, J2, J3...) our field of vision. The observations were made du- Theinter-individual distance data ring four days in each month,from sunrise were analyzed with multivariate analysis to sunset(betweendawn and dusk), from (Cluster Analysis). This consists in the for- Nov/2000 to Oct/2001. We used only two mation of groups of individuals according categories of inter-individual distance to to the similarities of variables displayed interpret the hierarchic social structure and bythem. The analyses included two steps: the formation of subgroups: A, two indivi- 1) establishment of similarity index (S.I.) duals in body contact; and B, 0 to 3 meters matrix, grade of similarity or association

3 Ricardo Sampaio, Hugo Lopes Gomes, Zelinda Maria Braga-Hirano, Juliana Moutinho Pedrosa, and Wagner Ferreira dos Santos between counts inter-individual distances; In the first phase, only one group li- 2) formation of groups by a linking method, ving in this areawas identified. The second and construction of dendograms based on phasewas characterized by the integration1 these indexes (Hair et al., 1995). of three individuals (F5, I3, and J6) – for In this study, the chosen S.I. was the unknown reasons – in the group, animals total number of episodes of distances A or which probably lived in the peripheral area B, which produced similarity matrices for and wentunnoticed during the first phase. each distance. These were imported to the The third phase was characterized by the PRIMER 5 software (Clarke & Warwick, birth of a howler (I4). In the fourth phase, 2001), which grouped the individuals based another howler (I5) was born. on the similarities, expressed by percentages of similarity, of all S.I., building den- First Phase dogramsvia a linking method, in which the average of the groups was used. As shown in Figure 2 (A = 0 m), two Using the dendograms, we built dia- subgroups of individuals were observed, grams that represent thelevel of association whereas the first one contained all of the between all individuals. The intensity of adult females that characterized strong af- this association is represented by arrows finities with their infants (matrifocal sub- that are proportional to the percentage of group). The male adult 1 (M1) was located similarity showed in the dendograms. close to them. The juveniles of the group established an association (0-40%) between themselves, as well aswith the adult females RESULTS (0-20%). The second subgroup showed as- sociations between subadult males and the The number of individuals in the M2 (0-40%), with little affinity towardsthe group during the study period is shownin- adult females (0-20%). Table I. The number of individuals varied When the distance considered be- from seventeen (Nov/2000) to twenty-two tween individuals increased (B= 0 to 3 m), howlers(Oct/2001), andonly two episodes as shown in Figure 3, the adult females of agonistic behavior throughout the en- still showed high association with their tire study period were recorded, whereas infants (40 – 80%),with the M1 showing both were performedonly by adult females proximity to them (40-60%). The juveni- (Sampaio, 2002). les showed greater association between

Table I – Representative characteristics of the four phases of the study with the black-and-gold howler monkeys living in the urban forest of Ribeirão Preto (SP, Brazil) PHASE PERIOD Nº OF INDIVIDUALS EVENTS 1st Nov/Dec 2000 17 Beginning of study 2nd Jan/Mar 2001 20 Immigration (3 individuals) 3rd Apr/May 2001 21 Birth of infant 4th Jun/Oct 2001 22 Birth of infant

1 We are not sure if these individuals were living isolated from the focal groups or if they had moved away from the group for a certain period of time.

4 Social behavior of black-and-gold howler monkeysin an urban forest

Figure 2. Diagram representing the similarity of inter-individual distance (0 m) in the first phase of the black- and-gold howler monkey group with 17 individuals. (M – Adult male, F - Adult Female, SAM – Subadult Male, J – Juvenile, I – Infant). Diagrams were built from dendrograms, which represent the level of association between all individuals.

Figure 3. Diagram representing the similarity of inter-individual distance (0-3 m) in the first phase of the black-and-gold howler monkey group. (M – Adult Male, F - Adult Female, SAM – Subadult Male, J – Juvenile, I – Infant). Diagrams were built from dendrograms, which represent the level of association between all individuals. themselves(40-100%)and with the adult Second Phase females (20-40%). The M2, SAM1, and SAM2 were more associated with sub- The second phase was characterized group 1, appearing in the periphery of the by the integration of three new individuals group. The SAM3 and 4 were associated in the group (F5, J6, and I3). These immi- (20-40%) together with a 5juvenile, and grants remained associated (20 – 60%) and presented little affinity in relation to the isolated from the rest of the group, as shown rest of the group (0-20%). in Figure 4 (A= 0 m).

5 Ricardo Sampaio, Hugo Lopes Gomes, Zelinda Maria Braga-Hirano, Juliana Moutinho Pedrosa, and Wagner Ferreira dos Santos

Figure 4. Diagram representing the similarity of inter-individual distance (0 m) in the second phase of the black-and-gold howler monkey group. (M – Adult Male, F - Adult Female, SAM – Subadult Male, J – Juvenile, I – Infant). Diagrams were built from dendrograms, which represent the level of association between all individuals. F5, I3 and J6 are the immigrants individuals.

In general, the level of closer proxi- center of the group, and the F3 and 4 were mity between the individuals also decrea- located far from it. The juveniles were still sed (Figure 4). The affinity among the adult associatedbetween themselves and with females (matrifocal subgroup) became less other classes.The immigrants still maintai- pronounced than in the first phase, and the ned a tight connection, and M2, SAM4, J5, F4 distanced itself from the matrifocal sub- and I2 were positioned in the periphery of group, as well as being in association with the group. the J4 (40-60%). The M1 was associated with lower affinitytowards two juveniles Third Phase (J1 and J2) and with the matrifocal sub- This phase began when the F2 gave group (0-20%). The SAM1, 2, and 3 were birth to the I4 and its previous infant (I2) associated (0-40%) and isolated from the started to show a juvenile behavior, which main group. The M2 was associated with could be noticedin thefield and is shown in the J5. Meanwhile, the SAM4 was isola- Figure 6 and 7.However, due to its smaller ted from the group. The I2, which is presu- size,it could be distinguished from the other mablyF2’s son, showed a smaller proximity juveniles andwe still decided to recognize it to F2in this phase than in the first one. as an infant. When analyzing Figure 5 (B= 0 - 3 In Figure 6 (A = 0 m), it is possible to m),it is not possible toobserve the forma- note that the adult females 1, 2, and 3 were tion of subgroups. The majority of the in- in the center of the group, and that twoju- dividuals interacted with low percentages veniles and I1 and I2 were still there, too. of affinity (20%). The M1 and SAM1 were The M1 was found near them and,with the in the center of the group, while the SAM2 exception of the interaction between F2-I4, and 3 were associated andcloser to this cen- the similarity between them was lower than terwhen compared to the previous phase, 40%. The SAM1 and 2 were weakly con- and the SAM4 and M2 were at the edge of nected between themselves, with the F4,and the group. The F1 and 2 were still in the with the matrifocal subgroup (0-20%).

6 Social behavior of black-and-gold howler monkeysin an urban forest

Figure 5. Diagram representing the similarity of inter-individual distance (0-3 m) in the second phase of the black-and-gold howler monkey group. (M – Adult Male, F - Adult Female, SAM – Subadult Male, J – Juvenile, I – Infant). Diagrams were built from dendrograms, which represent the level of association between all individuals. F5, I3 and J6 are the immigrants individuals.

Figure 6. Diagram representing the similarity of inter-individual distance (0 m) inthe third phase of the black-and- gold howler monkey group. (M – Adult Male, F - Adult Female, SAM – Subadult Male, J – Juvenile, I – Infant). Diagrams were built from dendrograms, which represent the level of association between all individuals.

The SAM3 and the M2 were asso- isolated from the whole group, while ano- ciated in the periphery of the group. Two ther one was found isolated from the group. juveniles (J3 and J4)were associated and The immigrants (F5, I3, and J6) were still

7 Ricardo Sampaio, Hugo Lopes Gomes, Zelinda Maria Braga-Hirano, Juliana Moutinho Pedrosa, and Wagner Ferreira dos Santos interacting and separated from the rest of were associated near them. The SAM2 and the group. 3 and the M2 were more peripheral, but as- In Figure 7 (B = 0 - 3 m), it is pos- sociated with of the group. sible to observe the formation of a single group that displayed a low level of associa- Fourth Phase tion between the individuals. The adult females were not in the center of this group, This phase began when the F3 gave whereas this position was occupied by three birth to the I5.Figure 8 (A = 0 m) shows the juveniles (J1, J2, and J3) accompanied by matrifocal grouping includingall adult fema- theF1, F2, F3, and F5. The M1 and SAM1 les.The M1 and two juveniles (J1 e J2) were

Figure 7. Diagram representing the similarity of inter-individual distance (0-3 m) in the third phaseof the black- and-gold howler monkey group. (M – Adult Male, F - Adult Female, SAM – Subadult Male, J – Juvenile, I – Infant). Diagrams were built from dendrograms, which represent the level of association between all individuals.

Figure 8. Diagram representing the similarity of inter-individual distance (0 m) in the fourth phase of the black- and-gold howler monkey group. (M – Adult Male, F - Adult Female, SAM – Subadult Male, J – Juvenile, I – Infant). Diagrams were built from dendrograms, which represent the level of association between all individuals.

8 Social behavior of black-and-gold howler monkeysin an urban forest found very close to them. Subadult males 1, atta genus, since the average number of in- 2, and 3 were in association between them- dividuals usually varies from 3 to 21 animals selves and at the edge of the group, while the (Carpenter, 1934; Crockett & Eisenberg, SAM4 and M2 were isolated from it. The in- 1987; Miranda & Passos, 2005;Estrada et fant I2 showed affinity with the J5 in the pe- al., 2002; Flórez& Delgado, 2011, Azkarate riphery of the group. The strongest affinities et al., 2017). These 22 individuals were con- (80-100% of similarity) were characterized fined in a 3-ha semi-deciduous forest frag- in the association between the F2 and the F3 ment (see Laguna, 1997), which comprisesa with their infants I4 and I5, respectively. highpopulation density of 100/km2, similar As showninFigure 9 (B = 0 - 3 m),in only in the number found in forests of the the center of the group, it is possible to ob- Argentina (Brown & Zunino, 1994). serve that F2, SAM1, M1, three juveniles,- Besides the isolation of this fragmen- two infants, and the other females (F1, F3, ted forest, this large number of individuals F4, and F5) were displaced from near the in- living in a small fragmented area may be dividuals – as mentioned above– to interact explained by the high percentage of fruit withSAM2, SAM3, I3, and I4. Therefore, ingested by the howler black-and-gold the matrifocal subgroup cannot be seen in monkeys when compared to other groups,as Figure 9. The M2, SAM4, and J6were fou- described by Pedrosa (2002) during the nd in the periphery of the group. same periodstudied. The area contains several exotic botanical species, including Caryota urens (Laguna, 1997 and 2000), a DISCUSSION palm tree whose fruit supply lasts the entire year (Gomes, 2004). In the period of the The number of individuals in the year in which the variety and availability group studied (17-22) was relatively higher of the fruits are lower, the howler monkeys than the average for the Alouatta caraya use the food offered to the animals of the species(Rumiz, 1990; Bicca-Marques, 1991, Zoo (Pedrosa, 2002; Gomes, 2004). Kowalewski &Zunino,1999; Dvoskinet al., The confined system this group faced 2004, Juárez et al., 2005), and for the Alou- –in whichthe migration of individuals or

Figure 9. Diagram representing the similarity of inter-individual distance (0-3 m) in the fourth phase of the black- and-gold howler monkey group. (M – Adult Male, F - Adult Female, SAM – Subadult Male, J – Juvenile, I – Infant). Diagrams were built from dendrograms, which represent the level of association between all individuals.

9 Ricardo Sampaio, Hugo Lopes Gomes, Zelinda Maria Braga-Hirano, Juliana Moutinho Pedrosa, and Wagner Ferreira dos Santos subgroups to other associated forest areas The social organization pattern of our is impossibledue to the isolation of the area study group (harem or age-graded system)is (see Figure 1)together with the great availa- not common for the Alouattacarayaspecies bility of food resulted in a high population (see Rumiz, 1990 and Kowalewski, 2000), density. This context led us to predict that and the harem systems in the Alouattaspe- the group could present: (1) a multi-male cies was organized through a matrifocal nu- system with social and hierarchic structu- cleus and a dominant adult male that had re; (2) signs of instability and formation of no need for proximity to the females, but subgroups; and (3) weak pacific trends in had access to them during the whole time their social behavior. (Neville et al., 1988). Oliveira and Ades During the entire sampling period,- (1998) investigated several groups ofA. fus- the group had two adult males, where the caspecies (= A. g. clamitans) and observed M1 was interpreted as being the first in the that adult males were frequently isolated, hierarchy, since it always located near the but that they could sometimes be grouped adult females, and M2 was always in the or associated with adult females. periphery of the group, far from the adult Concerning our second hypothesis, females, leading us to interpret that this the formation of subgroups and the occur- group was socially organized in a harem rence of isolated animals are often consid- system or in an age-graded system, thus not ered signs of instability in groups of howler confirming our first hypothesis. monkeys. Neville (1972) was the first au- The possible coalition among the thor to report the formation of subgroups in M2 and all SAMs took place in the peri- a 16-individual group of A. seniculus. phery of the group, with few interactions In our study was observed signs of with the adult females. The juveniles were instability in all sample periods, thus con- frequently associated between themsel- firming our second hypothesis and suggest- ves (mainly during playtime), with adult ing the occurrence of the formation of two females (looking for protection and social separate subgroups – one matrifocal sub- interactions, probably with their mothers or group and a coalition of subordinated males with other relatives), and with SAMs. The –, and these dynamics changed throughout only two copulations recorded by us (Sam- the sampling, wherein the first subgroup paio, 2002) were performed by the M1, and consisted in the matrifocal subgroup with we did not observe any sexual interaction an adult female and young animals. With between the other males and adult females. the exception of the adult male, all the The social organization in the genus members of another subgroup – formed by Alouatta seems to be variable. Groups of peripheral males and juveniles– showed in- theA. palliataspecies exhibits multi-male teraction with the matrifocal group. organization where the interactions betwe- Bezanson et al. (2002)stated that in- en adult males are meant to assure their dividuals of different sex-age classes in- access to the adult females, and the inter- groups of Primates may show different -individual distances between males and patterns of subgroup formation according females indicate their reproductive success to the context they belong to. This concurs (Jones, 1982).Neville (1972) showed that with what we observed in the adult and theA. seniculusspecies can organize their subadult males, adult females, and infants. groups throughanage-graded or harem sys- Nevertheless, the interactions and the so- tem. However, the behavior of the alpha cial organization within this group changed male was not well characterized. throughout the year.

10 Social behavior of black-and-gold howler monkeysin an urban forest

In the first phase, the matrifocal sub- The group structure in this phase was group was characterized by the association similar to that seen in the first phase. Howe- between all adult females and their infants, ver, the coalition among the subordinated and the M1associated with them can be un- males diminished, and the M2, SAM3, and derstood as a repelling behavior of the oth- SAM4 were still out of the center of the er males in order to avoid infanticide and group, remaining associated between them- allowaccess to copulation. This male be- selves, even though the SAM1 and SAM2 havior was only observed by Jones (1983) exhibited greater affinity with the adult fe- inregardingA. seniculus species. males F3, F4, and F5. The immigrants (F5, In the second phase, the immigrant I3, and J6) seemed to be more integrated in howler monkeys increased the instabili- the group in this phase, which could be ex- ty within the group, and the affinity of the plained by the birth of the I4. matrifocal subgroup was weaker than in the The behavior of the infants and juve- first phase. This may have happened becau- niles in this phase was more distant from se the immigrant adult female (F5) and its the main group, perhaps in search for se- infant (I3) may have had a higher interest curity, since males had interactions among on the young females of the group, having themselves in the group’s center,leading directed their “new” attention towards an to higher possibilities of conflict. Another infant, causing a lower association of the F3 possibility is that, with maturity, explorato- and a separation of the F4 from the matrifo- ry environmental behavior andpsychomo- tor-related activities lead them to be more cal group.The reason behind this may be the in the periphery of the group. possible attempt to form another subgroup. In the fourth phase, the birth of the I5 The M1 remained close to the ma- apparentlyinfluenced adult females, and all trifocal subgroup, but the SAM1 exhibi- of them (including the immigrant F5) were ted low association with the other subadult thenpresent in the matrifocal subgroup. males and with the M2,whereas it showed However, more juveniles and infants were in more association withthe adult females and the center of this association. We could see with the M1. Subadults males 2 and 3 inte- an increase in the tendency of SAMs interacted and were inserted in the group, while racting with the adult females. Therefore, the SAM4 and M2 showed more peripheral po- coalition of the males became weaker and, in sitioning within the group. the last month of sampling (Oct/2001), the In the third phase, we believe that the M2 was no longerpresent in the group. It is birth of theI4 may have contributed to the not known whether it was banishedfrom the return of F3 and F4to the subgroup of adult group, if it emigrated or if it became a satellite females (matrifocal subgroup), even though male, but this fact could be related to the poor the affinity was lower than that observed in association of the M2 with the subadult males the first phase. This finding was similar to and with the M1, or, rather, it could be due the one observed by Neville et al. (1988), to the group’s higher instability related to the who verified that the birth of an infant of increase in the number of its individuals. howler monkeys increases the affinities of Interestingly, the M2 was still part adult females among themselves, as well as of the group and did not stop interacting with their youth. We noticed that the F4 had with the subadult males, even when the greater interaction with SAM1 and SAM2. SAM1 and SAM2 – apparently the oldest However, they were still integrating inthe of the subadult males – started to associa- matrifocal subgroup. te with thematrifocal subgroup and, conse-

11 Ricardo Sampaio, Hugo Lopes Gomes, Zelinda Maria Braga-Hirano, Juliana Moutinho Pedrosa, and Wagner Ferreira dos Santos quently,with the M1. We are not sure if the This group showed a strong associa- closer proximity between these two SAMs tion among adult females (matrifocal sub- and the M1 is related to a coalition betwe- group),whereas the dominant male (M1) had en them or to competition to get access to greater proximity to them. Signs of instability females.However,no agonistic behavior be- were common throughoutthe year due to inte- tweenthese males was observed during this gration of “new” individuals, but the births of period, and, for this reason,we assume that infants strengthened the matrifocal subgroup. this behavior is more likely to be a coalition The aging of subadult males increased their among these males. association with the matrifocal subgroup and This type of male coalition was also ob- with the M1, resulting in the departure of the served by Jones (1980) in a A. palliata group. other adult male from the group. Most likely, this binding is related to the M2’s The social organization of this group departure from the group and its migration could be assumed to be a harem or age-grad- from the park to the city’s surrounding areas. ed system, which experienced signs of in- A few days after leaving, it was captured by stability, and the few agonistic episodes the Municipal Zoo anddied one week later. and inter-individual competition seemed to Despite the instability displayed by be related to the low competition for food, this group, we did not observe a more ag- since the availability of fruits was high. gressive behavior –as we expected –, thus The A. carayaspecies is globally refuting our third hypothesis; we only saw characterized as the “least concern – LC”, two displaysof agonistic behavior involving despite its declining populations (Fernan- two adult females. As mentioned before,the dez-Duque et al.,2008), butit was classi- high supply of fruits during year probably fied as a “near-threatened species” in Bra- reduced competition among the individuals, zil (Ludwig et al., 2015); in the state list and the indirect signs were enough to esta- ofSão Paulo, the species appears as “vul- blish and communicate the social hierarchy nerable” (Bressan et al., 2009). within this group. However, theaging of The “near threatened” and “vulnera- subadult males and a consequently increa- ble” statusesare very evident in our study sed competition for access to females may area, where the remaining forests in the increase the aggressiveness between males. region are highly fragmented, coveringon- ly 4% of Ribeirão Preto’s area (Henriques, 2003). Under these conditions, the geo- CONCLUSION AND FINAL CON- graphic isolation leads to high degrees of SIDERATIONS endogamy, thus resulting in unviable populations in the long term. We believe that our study provides The evaluation of the black-and- an important interpretation on the social -gold howler monkeys’group dynamics is behavior of howler monkeys (Alouatta- therefore, of great importance to establish caraya). The patterns of social interaction management plans for the conservation of observed during the samplings were effi- primates that live under this type of envi- ciently confirmed by the multivariate meth- ronmental pressure. Hence, in this study, the odology used in this research, which helped high population density of the group and the us in the identification of the social interac- resulting migration of an individual to the tion patterns, illustrating the plasticity and city area resultedin the relocation of some tendency that the social structure suffered individuals to other forest fragments (Ros- during the period of study. siand Santos, in press). In addition, the risk

12 Social behavior of black-and-gold howler monkeysin an urban forest of extinction that exists for the Primates of Bezanzon, M, Garber, P.A., Murphy, the tropical area is considerable. Thus, our J.T.,&Premo, L.S. (2008).Patterns of work can contribute to the knowledge of a Subgrouping and Spatial Affiliation in A Primate that is under high anthropic action. Community of Mantled Howling Monkeys (Alouatta palliata).American Journal of Primatology, 70, 282–293. ACKNOWLEDGEMENTS Bicca-Marques, J.C. (1991). “Ecologia e The authors are thankful to PIBIC/ comportamento de um grupo de bugios USP/CNPq and Mr. Vinicio B. Pecci, from pretos Alouatta caraya (Primates, Cebidae) the Environmental Management and Plan- em Alegrete, RS, Brasil”. Master Thesis, ning Office of Ribeirão Preto City Hall, for Universidade de Brasília, Brasília-DF, the financial support (scholarships); to Mrs. Brasil. Marisa dos Santos from Ribeirão Preto’s Bressan, P.M., Kierulff, M.C.M.,& Sugieda, City Zoo, who authorized the area of stu- A.M. (2009). Fauna Ameaçada de Extinção dy;as well as to Drs. Gelson Genaro and Mr. do Estado de São Paulo: Vertebrados. Dilmar Oliveira, who provided suggestions Fundação Parque Zoológico de São Paulo, and critical comments to improve this arti- São Paulo. Secretaria de Meio Ambiente do cle. We would like to thank to Dr. Alexandre Estado de São Paulo. 645p. A. Oliveira for the help with the statistical analysis, and to Prof. Alexandra Olimpio O. Brown, A. D.,&Zunino, G. E. (1994). Hábitat, Cunha and Prof. Abilio Borghi for their as- densidad y problemas de conservación de sistance regarding the English language. los primates de Argentina. Vida Silvestre Neotropical, 3, 131–40.

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13 Ricardo Sampaio, Hugo Lopes Gomes, Zelinda Maria Braga-Hirano, Juliana Moutinho Pedrosa, and Wagner Ferreira dos Santos

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