G Model

ARTICLE IN PRESS

BEPROC-2886; No. of Pages 9

Behavioural Processes xxx (2014) xxx–xxx

Contents lists available at ScienceDirect

Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc

Social structure of collared peccaries (Pecari tajacu): Does relatedness matter? Cibele Biondo a,b,∗ , Patrícia Izar a , Cristina Y. Miyaki b , Vera S.R. Bussab a a b

Departamento de Psicologia Experimental, Instituto de Psicologia, Universidade de São Paulo, Av. Prof. Mello Moraes 1721, São Paulo, SP 05508-030, Brazil Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, São Paulo, SP 05508-090, Brazil

a r t i c l e

i n f o

Article history: Available online xxx Keywords: Kinship Microsatellite Spatial association Tayassuidae

a b s t r a c t Relatedness is considered an important factor in shaping social structure as the association among kin might facilitate cooperation via inclusive fitness benefits. We addressed here the influence of relatedness on the social structure of a Neotropical ungulate, the collared peccary (Pecari tajacu). As peccaries are highly social and cooperative, live in stable cohesive herds and show certain degree of female philopatry and high mean relatedness within herds, we hypothesized that kin would be spatially closer and display more amicable and less agonistic interactions than non-kin. We recorded spatial association patterns and rates of interactions of two captive groups. Pairwise relatedness was calculated based on microsatellite data. As predicted, we found that kin were spatially closer than non-kin, which suggests that relatedness is a good predictor of spatial association in peccaries. However, relatedness did not predict the rates of social interactions. Although our results indirectly indicate some role of sex, age and familiarity, further studies are needed to clarify the factors that shape the rates of interactions in collared peccaries. This article is part of a Special Issue entitled: Neotropical Behaviour. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Social structure is defined as the network of inter-individual relationships established among members of a given animal group (Hinde, 1976). This network is dynamic and can change over time under the influence of many factors. Some factors represent ecological constraints such as availability of resources and predation pressure (Kappeler and van Schaik, 2002). Others are related to group composition, including kinship, familiarity, age, sex and social status (Kappeler et al., 2013). Knowledge about such factors and how they affect the establishment of relationships is necessary to fully understand the social structure of a group of animals. Kin relationships have been proposed to be important in shaping social structure (Clutton-Brock and Janson, 2012). The association among kin might facilitate cooperation, and is predicted to be favored by natural selection when the inclusive benefits of cooperation outweigh the costs of sociality (Hamilton, 1964). This could be particularly true in many mammalian societies where relatives

∗ Corresponding author. Present address: Centro de Ciências Naturais e Humanas (CCNH), Universidade Federal do ABC (UFABC), Rua São Paulo s/n◦ , São Bernardo do Campo, SP 09606-070, Brazil. Tel.: +55 11 2320 6307. E-mail addresses: [email protected], [email protected] (C. Biondo).

live together as a consequence of female philopatry (Silk, 2007). If this was the case, we could expect that mammals prefer close relatives as social partners. In fact, there is empirical evidence both for and against that hypothesis. In rhesus monkeys (Macaca mulatta), for example, maternal and paternal half-sisters are spatially closer, present higher frequency of grooming than unrelated females, and help each other during agonistic interactions with other individuals (Schülke et al., 2013; Widdig et al., 2001). In southern flying squirrels (Glaucomys volans), on the other hand, prior familiarity, but not relatedness, predicts the patterns of associations between individuals (Garroway et al., 2013), which indicates that other factors could also be important. In yellow-bellied marmot (Marmota flaviventris), in addition to kinship, age plays a significant role in social structure, with individuals of the same age class displaying more affiliative interactions among them than those of different age classes (Wey and Blumstein, 2010). Here, we studied the social structure of an ungulate species, the collared peccary, Pecari tajacu. This species is the most widespread of the Neotropical family Tayassuidae. This family together with the Old World family Suidae forms the suborder Suina (Agnarsson and May-Collado, 2008). The studies that addressed the role of relatedness in the social structure of Suina are focused in Suidae species, mainly in domestic pig and wild boars (both Sus scrofa). These studies have shown little or no influence of relatedness in the associations (Durrell et al., 2004; Iacolina et al., 2009) and rates

http://dx.doi.org/10.1016/j.beproc.2014.08.018 0376-6357/© 2014 Elsevier B.V. All rights reserved.

Please cite this article in press as: Biondo, C., et al., Social structure of collared peccaries (Pecari tajacu): Does relatedness matter? Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.08.018

G Model BEPROC-2886; No. of Pages 9

ARTICLE IN PRESS C. Biondo et al. / Behavioural Processes xxx (2014) xxx–xxx

2

of agonistic interactions of the individuals (Puppe, 1998). The social organization of S. scrofa is usually centered in one or more females and its offspring and the groups can vary temporally, with splitting and merging of subgroups (Kaminski et al., 2005). In contrast, the collared peccary is known to be highly social and cooperative, living in stable herds of five to 25 individuals with males and females of various age classes (Bissonette, 1976; Keuroghlian et al., 2004; Mayer and Brandt, 1982). This species shows male-biased dispersal, although a limited amount of female dispersal has been documented (Cooper et al., 2009, 2010), and it was suggested that individuals may disperse into non-natal groups to join a cohort of relatives (Cooper et al., 2011). Herds work as cohesive social units, in which small inter-individual distances are maintained by means of frequent amicable and few agonistic interactions (Byers and Bekoff, 1981). Cooperation is a characteristic of herds, as exemplified by situations when adults cluster around juveniles and lead them away from predators, or even when the entire herd chases predators away (Byers and Bekoff, 1981). Cooperation is also present during foraging behavior, when several individuals eat close to each other, for example, consuming the same plant (Byers and Bekoff, 1981). Byers and Bekoff (1981) suggested that these characteristics have evolved through kin selection. In support of this hypothesis, Cooper et al. (2011) demonstrated that mean genetic relatedness within herds is high, especially among females. However, the role of relatedness in rates of affiliative and agonistic interactions and spatial association between individuals of this species up to now has not been explicitly tested. In this study, we described the social structure of two captive groups of collared peccaries using Social Network Analysis (Wey et al., 2008) and evaluated whether the patterns of amicable and agonistic interactions, and spatial association between individuals were correlated to their degree of relatedness, inferred from multilocus microsatellite genotypes. As collared peccaries show stable cohesive herds (Byers and Bekoff, 1981), certain degree of female philopatry and high mean genetic relatedness within herds (Cooper et al., 2009, 2010, 2011), we hypothesized a role of genetic relatedness in their social structure, with kin in closer spatial association and showing more affiliative and less aggressive interactions than non-kin.

2. Materials and methods 2.1. Study site and animals The study was conducted at Vale Verde Farm, a private property located in the municipality of São Miguel Arcanjo, in the State of São Paulo, Brazil. This institution keeps farmed peccaries for commercial purposes since 1997. Two groups were studied: group A and B, which were created as subsets of two larger groups, group 1 and group 2, respectively. Originally, group 1 was composed by 19 individuals (16 adults and three juveniles) and group 2, by 13 individuals (all adults). All individuals were marked with radiofrequency microchips for identification. Groups A and B were formed by five possible pregnant females and one adult male each for a study about allosuckling in September 2003 (Biondo, 2006). Animals from the larger groups were captured using trap boxes with capacity for 25 kg (an animal per trap box) and were immobilized with acepromazine 1% (Acepran® , Univet, Brazil) for approximately 30 min. They were individually marked with hair cuts in different regions of the body to permit identification at distance, facilitating behavioral data collection. Blood samples were taken from each individual for subsequent genetic analyses. Each group was maintained in outdoor enclosures surrounded by 1.5 m-high net wire fences and had an area of around 900 m2

Table 1 Description of the animals analyzed. Group

Animal

Age category

Sex

Mother

A

Belly (Bel) Fore (For) Gland (Gla) Hind (Hin) Neck (Nec) Teco (Tec) Nina Nigb Nihc Pedrita (Ped)a Pipoca (Pip)a Gigi (Gig)b Nininha (Nin)c

Adult Adult Adult Adult Adult Adult Infant Infant Infant Infant Infant Infant Infant

Female Female Female Female Female Male Unknown Unknown Unknown Female Female Female Female

Unknown Unknown Unknown Unknown Unknown Unknown Neck Gland Hind Neck Neck Gland Hind

B

Dodô (Dod) Fifi (Fif) Lele (Lel) Pepa (Ppa) Pepe (Pep) Tico (Tic) Pateta (Pat)

Adult Adult Adult Adult Adult Adult Infant

Female Female Female Female Female Male Male

Unknown Unknown Unknown Unknown Unknown Unknown Lele

a

Neck’s twin litter before (Nin) and after individualization (Pedrita and Pipoca). Gland’s twin litter before (Nig) and after individualization (Gigi) and the death of one of the infants. c Hind’s twin litter before (Nih) and after individualization (Nininha) and the death of one of the infants. b

(17.0 m × 57.0 m), with a feeder of 2.0 m × 2.5 m positioned in an enclosed shelter (where food was provided for all individuals at the same time) and a water tank of 1.0 m × 1.0 m. The ground was covered with grass of the genus Brachiara and there were some trees and palms that guaranteed shade to animals. Water was provided ad libitum. The animals were fed twice a day with food manufactured at the Farm, including corn, soy, wheat and mineral salt in the formulation. In the beginning of the behavioral study, in October 2003, group A consisted of 12 individuals: one adult male, five adult females and six unsexed infants. However, in January 2004, two infants died from unknown causes. So, after these deaths, there were 10 individuals in the group, including four female infants from three different litters (Table 1). Group B had seven individuals during the entire observation period: one adult male, five adult females and one juvenile male (Table 1). Infants were captured to be marked and to have blood samples taken in February 2004, when they were approximately 3–4 months old to reduce the risk of conspecific aggression resulting from human-specific olfactory cues left by handlers. Before marking, litters of group A were distinguished by differences in size. In group B, as there was only one infant, its identification was straightforward. 2.2. Genetic analysis Because genetic estimators of relatedness are calculated using allele frequencies of the population, blood samples were also taken from all the individuals which remained in the original groups (13 individuals from group 1 and seven individuals from group 2), from which the observed groups were taken, to calculate the allele frequencies of the captive population as a whole. However, the samples of some individuals could not be satisfactorily genotyped for many loci and were discarded from subsequent analyses (two individuals from group 1 and three from group 2). In total 32 individuals were analyzed: 17 from the observed groups (10 individuals from group A and seven from group B) and 15 from the two original groups (11 individuals from group 1 and four from group 2). Blood samples were kept frozen at −20 ◦ C. DNA was extracted using standard proteinase K and phenol–chloroform protocol (Sambrook et al., 1989).

Please cite this article in press as: Biondo, C., et al., Social structure of collared peccaries (Pecari tajacu): Does relatedness matter? Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.08.018

G Model BEPROC-2886; No. of Pages 9

ARTICLE IN PRESS C. Biondo et al. / Behavioural Processes xxx (2014) xxx–xxx

Each individual was genotyped for 12 microsatellites: six specific loci (JC011, JC033, JC035, JC040, JC041, Cooper et al., 2010; and PT0226, Biondo et al., 2011), four developed for domestic pig (ACTG2, IGF1, SW444 and SW857, Rohrer et al., 1994, 1996) and two for white-lipped peccaries (Tpec10 and Tpec12, Dalla Vecchia et al., 2011). The forward primers were manufactured with a 5 -M13 tail (5 -CACGACGTTGTAAAACGAC, Boutin-Ganache et al., 2001). Polymerase chain reaction (PCR) was performed in 12 ␮l containing: 30–45 ng of DNA, 1× PCR buffer, 0.2 mM of dNTP mix, 2.5 mM of MgCl2 , 3 pmol of reverse primer, 2 pmol of fluorescent (FAM, HEX or TET, Applied Biosystems) M13 sequence primer, 1 pmol of forward primer (10 ␮M), 0.5 U of Taq polymerase (Pharmacia) and 7.2 ␮l of MilliQ water. The cycling conditions were: 5 min at 95 ◦ C, 35 cycles of 94 ◦ C for 30 s, AT (annealing temperature, JC011, JC033, JC040, JC041, ACTG2 and SW444 = 60 ◦ C; IGF1, SW857 and Tpec12 = 58 ◦ C; JC035 and PT0226 = 55 ◦ C; and Tpec10 = 52 ◦ C) for 30 s and 72 ◦ C for 30 s, followed by a final step of 72 ◦ C for 10 min. PCR products were genotyped on ABI 377 and ABI 3730 automated sequencers (Applied Biosystems) and scored with Genotyper 2.1 (Applied Biosystems) and GeneMarker (Softgenetics) software. All genotypes were characterized from at least two independent PCRs to check for genotyping errors. The majority of the cases resulted in identical genotypes. When the genotypes were different, the procedure was repeated until a consensus was obtained. MicroChecker 2.2.3 (Van Oosterhout et al., 2004) was used to estimate null allele frequencies and GenAlEx 6 (Peakall and Smouse, 2006) to calculate the number of alleles and expected and observed heterozygosities for each locus. Hardy–Weinberg and linkage equilibrium were tested based on probability tests and log-likelihood ratio G-tests, respectively, in Genepop 3.4 (Raymond and Rousset, 1995). None of the loci showed any evidence of null alleles or other genotyping errors. The mean number of alleles and the mean expected and observed heterozygosities were 6.083 ± 1.782, 0.689± 0.107 and 0.733 ± 0.142, respectively. The microsatellites were in Hardy–Weinberg equilibrium (p > 0.016 after Benjamini and Yekutieli, 2001 correction). Significant linkage disequilibrium (p < 0.010 after Benjamini and Yekutieli, 2001 correction) was observed between three pairs of loci (SW444–PT0226, SW857–JC040 and JC033–JC040), suggesting that they are not independent in this population. Although this result could be a statistic artifact due to the small sample size (N = 32) or to inbreeding, as no linkage disequilibrium was observed in larger populations (see Cooper et al., 2010 – for an example), in order to be conservative, data on JC040 (since it showed evidence of linkage with two other loci) and PT0226 (because it had only three alleles in contrast to SW444, which had six) were discarded from subsequent analyses. Therefore, pairwise relatedness (r) was calculated based on data from 10 microsatellites (JC011, JC033, JC035, JC041, ACTG2, IGF1, SW444, SW857, Tpec10, and Tpec12) using the maximum likelihood estimator of Wagner et al. (2006) implemented in the program ML-Relate (Kalinowski et al., 2006). 2.3. Behavioral data collection Observations took place from October 2003 to June 2004, with a total of 133 h (80 h for group A and 53 h for group B), after some weeks of habituation of the animals to the presence of observers, and one month after the formation of the groups, allowing animals to become well-socialized before data collection. The groups were observed daily by C. Biondo for at least one week per month in periods when the animals were more active, from 08:00 to 10:30 and from 14:30 to 17:00. On each day of observation, one group was observed in the morning and the other in the afternoon. The group that was observed in the morning in one day was observed in the afternoon in the next day and vice versa; and we tried to equalize

3

the number of observations in the morning and in the afternoon for both groups. All occurrence sampling (Altmann, 1974) was used to record the frequencies of affiliative and agonistic interactions. For simultaneous monitoring of all individuals of the group, a field assistant, trained by C. Biondo (CB) until perfect concordance, helped in data collection by warning CB about interactions whenever they occurred (but the final record was called by CB). The afilliative interactions recorded were mutual rub and olfactory investigation and contact. In mutual rub, two animals positioned side-by-side in a head-tail orientation rub their heads vertically (up and down) in the dorsal gland region of each other. Olfactory investigation and contact comprised two subcategories: olfactory investigation, when an animal touches its nose on body parts of another animal, moving the nasal disk; and social grooming, in which an animal rubs its nose up and down in regions of the body of another animal, licking and biting. Agonistic interactions observed included threat behaviors, such as snarl and tooth clack, and squabbles, when two animals raise their noses with open mouths and move back and forth, from one side to another against the other’s nose, snarling and making bite movements. For a complete description of these behavioral categories, see Byers and Bekoff (1981). In all instances, the initiators and receivers of the interactions were recorded. In order to analyze the spatial association, the pattern of subgroup formation among individuals was collected instantaneously at 10-min regular intervals (scan sampling; Altmann, 1974). To identify the subgroups, we used the relative distance criteria according to Ferraz et al. (2013): two individuals were considered in the same subgroup if the distance between them was not higher than the distance between subgroups. When the animals were walking in a single line, one behind the other, they were considered in the same subgroup. The enclosures of the two observed groups were side-by-side. This was the same configuration of the original larger groups. The behavioral recordings were made from a platform positioned at 1.50 m above the ground and in the boundary between the enclosures, where the observer and the assistant had a complete view of both groups. When the animals were far, they were identified using a binocular B-725II (SAMSUNG – 7 mm × 25 mm, Field 7.6, Seoul, South Korea). 2.4. Social interactions and spatial association analysis Agonistic and affiliative interactions were organized in n × n matrices (n = individual), where the cell entries indicated the rates (frequency/hour of observation) of interactions of each dyad. For the analysis of spatial association, the scan data were organized in matrices in which the rows corresponded to the time of the scan and the columns to the individuals. The cell entries were completed with the subgroup number. The individuals that belonged to the same subgroup received the same number and the individuals that belonged to different subgroups, different numbers. These matrices were converted into n × n dissimilarity matrices using the index of spatial association of Anderberg (1973): ID (A, B) = d/a + d, where a is the number of times that individuals A and B were in the same subgroup; d is the number of times which A was in one subgroup and B was not, or vice versa. The index value varies from zero to one, where values closer to zero indicate strong association between individuals. Because the infants in group A were individualized and marked only in February 2004, two behavior matrices were constructed for each group: one for the period previous to marking of infants (which comprises observations from October 2003 to mid February 2004, and called as first phase) and another related to the subsequent period (which comprises observations from late February to June 2004, and called as second phase).

Please cite this article in press as: Biondo, C., et al., Social structure of collared peccaries (Pecari tajacu): Does relatedness matter? Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.08.018

G Model BEPROC-2886; No. of Pages 9 4

ARTICLE IN PRESS C. Biondo et al. / Behavioural Processes xxx (2014) xxx–xxx

To verify if kin were in close association and showed more affiliative and less aggressive interactions than non-kin, correlation tests between matrices of relatedness and interaction rates and Anderberg’s indices were conducted using tau Kr test in MatrixTester v.2.2.3 (Hemelrijk, 1990a,b). Each test included 10,000 permutations. As the blood samples for genetic analysis were collected when there were only four infants in group A (second phase), the correlations of the first phase were performed using only the values of the adult dyads. This was also done with group B for comparison purposes. All the matrices were analyzed using social network analysis implemented in the software SOCPROG (Whitehead, 2009). Social networks consist of nodes, which represent the individuals, and edges, which represent the strength of the relationship between nodes. Thicker edges represent stronger relationships. In order to have a direct relationship between the thickness of the edge and the value of association between individuals, the values of Anderberg’s index were converted using the formula 1 − x, where x is the value of the index. Therefore, thicker edges represents higher values of the converted index and, consequently, stronger associations. The social networks were graphically visualized as sociograms using Netdraw (Borgatti, 2002). SOCPROG was also used to identify clusters of individuals and to calculate the value of eigenvector centrality for each individual in each group and phase. Clusters were identified by calculating the modularity (modularity-1), which is the difference between the proportion of the total association within clusters and the expected proportion, given the summed associations of the different individuals (Newman, 2004). Values of modularity above 0.3 indicate useful group divisions (Newman, 2004). The eigenvector centrality is a measure given by the first eigenvector of the matrix of association indices or interaction rates. Higher values indicate that an individual has strong associations to other individuals that, in turn, also have strong associations, and therefore, has a central position in the network. In order to verify if kinship would have a significant role in the formation of the clusters identified, correlations between cluster and kinship matrices were conducted using the Dietz’R matrix correlation test also in SOCPROG. The cluster matrices were built coding 1 to the dyads belonging to the same cluster and 0 to those of different clusters. To construct the kinship matrices, all dyads with values of relatedness (r) equal or above 0.125 (expected value

for third degree relatives) were considered to be related and were coded as 1; the dyads with r below that value were considered unrelated and were coded as 0. Cluster and kinship matrices of the first phase were constructed using just adults due to the same reasons explained above concerning tau Kr tests. 2.5. Other analyses Since the data were not in conformity with a normal distribution (Kolmogorov–Smirnov test with Lilliefors correction, p < 0.05), the medians of relatedness were compared between groups using Mann–Whitney U test computed in SPSS 13.0 (SPSS Inc.). This software was also employed to compare the medians of the affiliative and agonistic interactions rates in each group using Wilcoxon signed-rank test. 3. Results 3.1. Relatedness Coefficients of relatedness ranged from 0.00 to 0.50 (mean = 0.12 ± 0.15) in group A and 0.00 to 0.56 in group B (mean = 0.15 ± 0.21) and the medians were similar in both groups (group A = 0.05, group B = 0.06; Mann–Whitney U test, Z = −0.058, p = 0.954). However, the distribution of the coefficients (Fig. 1) showed that group A was constituted by dyads with various degrees of relatedness, while group B had many unrelated dyads and some highly related ones (with relatedness coefficients compatible with first degree relatives). 3.2. Social interactions A total of 710 interactions in 133 hr of observation (5.34 interactions per hour), 487 for group A in 80 hr (6.09 interactions per hour) and 223 for group B in 53 hr (4.21 interactions per hour), was recorded. The means and the medians of interaction rates and Anderberg’s indices are shown in Table 2. The rates of affiliative interactions (mutual rub and olfactory investigation and contact – group A: mean = 0.75 ± 1.19 and median = 0.25; group B: mean = 0.78 ± 0.83 and median = 0.50) were higher than those of agonistic interactions (Table 2) in both groups (group A: Wilcoxon signed-rank test, Z = −4.501, p = 0.000; group B: Wilcoxon

Fig. 1. Distributions of the coefficients of relatedness. (a) Group A and (b) group B.

Please cite this article in press as: Biondo, C., et al., Social structure of collared peccaries (Pecari tajacu): Does relatedness matter? Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.08.018

G Model

ARTICLE IN PRESS

BEPROC-2886; No. of Pages 9

C. Biondo et al. / Behavioural Processes xxx (2014) xxx–xxx Table 2 Means (M), standard deviations (SD), and medians (Md) of rates of agonistic interactions (AI), mutual rub (MB), and olfactory investigation and contact (OIC), and Aderberg’s index of spatial association (SA) registered in each group for the total period of observation (just for interactions) and for each phase separately. Behavior

Phase

Group A

Table 3 Values of eigenvector centrality observed for each individual in each phase. AI, agonistic interaction; MR, mutual rub; OIC, olfactory investigation and contact. Group

Individual

Md

M ± SD

Md

AI

Total First Second

0.27 ± 0.51 0.12 ± 0.18 0.39 ± 0.65

0.00 0.00 0.20

0.15 ± 0.22 0.06 ± 0.11 0.24 ± 0.27

0.00 0.00 0.20

MR

Total First Second

0.29 ± 0.54 0.26 ± 0.57 0.32 ± 0.51

0.00 0.00 0.00

0.32 ± 0.41 0.10 ± 0.23 0.54 ± 0.43

0.20 0.00 0.40

OIC

Total First Second

0.46 ± 0.82 0.23 ± 0.30 0.65 ± 1.03

0.25 0.10 0.25

0.46 ± 0.57 0.12 ± 0.19 0.80 ± 0.63

0.25 0.00 0.60

SA

First Second

0.30 ± 0.15 0.46 ± 0.14

0.28 0.47

0.37 ± 0.20 0.52 ± 0.11

0.27 0.56

signed-rank test, Z = −4.723, p = 0.000). Both groups showed strong spatial association between individuals with mean Anderberg’s indices lower than 0.58 (Table 2). 3.2.1. Agonistic interactions In contrast to it was predicted, no correlation was found between rates of agonistic interactions and coefficients of relatedness between dyads in both groups (first phase: group A, tau Kr = −0.173, pl = 0.2875; group B, tau Kr = −0.219; pl = 0.171; second phase: all individuals – group A, tau Kr = −0.110, pl = 0.184; group B, tau Kr = 0.056; pr = 0.389; only adults – group A, tau Kr = −0.043, pl = 0.429; group B, tau Kr = −0.137; pl = 0.287). In the first phase, Hind’s infants (Table 1) did not participate in the sociogram of group A and Dodo, in the sociogram of group B. In both groups, all the individuals participated in the social structure based on agonistic interactions in the second phase. Both groups were divided into two clusters in the first phase (group A: maximum modularity = 0.393 Fig. 2a; group B: maximum

AI

MR

OIC

Phase 1

Phase 2

Phase 1

Phase 2

Phase 1

Phase 2

A

Belly Fore Gland Hind Neck Teco Nn Ng Nh Pedrita Pipoca Gigi Nininha

0.42 0.23 0.25 0.62 0.39 0.27 0.29 0.11 0.00 – – – –

0.28 0.47 0.19 0.26 0.19 0.66 – – – 0.33 0.13 0.04 0.06

0.11 0.36 0.59 0.34 0.27 0.57 0.00 0.00 0.00 – – – –

0.34 0.34 0.41 0.35 0.41 0.55 – – – 0.00 0.00 0.00 0.00

0.38 0.36 0.39 0.35 0.11 0.59 0.19 0.15 0.21 – – – –

0.43 0.39 0.25 0.06 0.47 0.59 – – – 0.07 0.13 0.12 0.02

B

Dodô Fifi Lele Pepa Pepe Tico Pateta

0.00 0.32 0.20 0.32 0.60 0.37 0.51

0.25 0.41 0.21 0.31 0.33 0.64 0.33

0.65 0.71 0.16 0.04 0.16 0.17 0.00

0.41 0.46 0.28 0.41 0.34 0.50 0.10

0.34 0.00 0.47 0.00 0.41 0.59 0.39

0.49 0.22 0.37 0.44 0.21 0.52 0.25

Group B

M ± SD

5

modularity = 0.500, Fig. 2c) but not in the second (group A: maximum modularity = 0.265, Fig. 2b; group B: maximum modularity = 0.261, Fig. 2d). However, kinship had no influence in clusters composition of the first phase (Dietz’R tests, group A: r = 0.289, p = 0.501; group B: r = −0.185, p = 1.000). In the first phase, in both groups, one female was the most central individual with the highest eigenvector centrality: Hind in group A and Pepe in group B (Table 3). In the second phase, males were the most central individuals in both groups (Table 3). 3.2.2. Affiliative interactions As observed for agonistic interactions, the rates of mutual rub did not correlate with the pairwise relatedness in both groups (first

Fig. 2. Sociograms of agonistic interactions. (a and b) Group A, first and second phase, respectively; (c and d) group B, first and second phase, respectively. Nodes represent individuals and line widths, rates of interaction. Circle = female; rectangle = male; triangle = juvenile.

Please cite this article in press as: Biondo, C., et al., Social structure of collared peccaries (Pecari tajacu): Does relatedness matter? Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.08.018

G Model BEPROC-2886; No. of Pages 9

ARTICLE IN PRESS C. Biondo et al. / Behavioural Processes xxx (2014) xxx–xxx

6

phase: group A, tau Kr = 0.045, pr = 0.406; group B, tau Kr = −0.134, pl = 0.322; second phase: all individuals – group A, tau Kr = −0.004, pl = 0.480; group B, tau Kr = −0.038, pl = 0.416; only adults – group A, tau Kr = 0.085, pr = 0.358; group B, tau Kr = −0.104, pl = 0.307). The rates of olfactory investigation and contact also did not correlate with relatedness, with the exception of the first phase in group B, which showed a negative correlation, with kin displaying lower rates of this behavior than non-kin, contrasting to it was predicted (first phase: group A, tau Kr = −0.185, pl = 0.252; group B, tau Kr = −0.712, pl = 0.030; second phase: all individuals – group A, tau Kr = 0.038, pr = 0.372; group B, tau Kr = −0.012, pl = 0.466; only adults – group A, tau Kr = 0.167, pr = 0.260; group B, tau Kr = −0.072, pl = 0.394). In the first phase, in both groups, the mutual rub sociograms indicated that infants did not integrate the social structure (Fig. 3a and c). Both groups were divided into clusters (group A: two clusters, maximum modularity = 0.356, Fig. 3a; group B: three clusters, maximum modularity = 0.461, Fig. 3c), however these clusters were not defined by kinship (Dietz’R tests, group A: r = 0.055, p = 0.661; group B: r = 0.040, p = 0.595). In the second phase, in group A, infants participated of the structure but as a separated cluster from adults (maximum modularity = 0.313, Fig. 3b). Again, these two clusters were not predicted by kinship (Dietz’R tests, r = −0.036, p = 0.729). In group B, no clusters were formed (maximum modularity = 0.178) and the unique infant, Pateta, participated in the structure interacting with three adult females: Lele (his mother), Dodo and Pepa (Fig. 3d). Males were the most central individuals in both groups, showing high values of eigenvector centralities (in both phases in group A and in the second phase in group B, Table 3). In contrast to mutual rub, infants integrated the sociograms of olfactory investigation and contact since the first phase (Fig. 4). In both groups, clusters were identified in the first phase (group A: four clusters, maximum modularity = 0.329, Fig. 4a; group B: three clusters, maximum modularity = 0.370, Fig. 4c) but not in the second (group A: maximum modularity = 0.180, Fig. 4b; group B: maximum modularity = 0.192, Fig. 4d). Two adult females (Pepa and Fifi) were not included in the structure in the first phase in group B (Fig. 4c). Kinship did not predict the clusters formed in the first phase in both groups (Dietz’R tests, group A: r = −0.068, p = 0.749; group B: r = −0.364, p = 1.000). As observed for mutual rub, males had central positions with high values of eigenvector centralities in both phases and groups (Table 3). 3.3. Spatial association As predicted, the coefficients of relatedness were negatively correlated with the Anderberg’s indices, meaning that related individuals were closer in the spatial structure, with exception only of the second phase in group A (first phase: group A, tau Kr = −0.493, pl = 0.019; group B, tau Kr = −0.463, pl = 0.043; second phase: group A – all individuals: tau Kr = −0.029, pl = 0.390; only adults: tau Kr = 0.021, pr = 0.447; group B – all individuals: tau Kr = −0.443, pl = 0.016; only adults: tau Kr = −0.509, pl = 0.024). The sociograms showed that all individuals were connected in the network and there was no formation of clusters in both groups in both phases (group A: first phase – maximum modularity = 0.085, second phase – maximum modularity = 0.102; group B: first phase – maximum modularity = 0.148, second phase – maximum modularity = 0.144; Fig. 5). In both groups, except in the first phase in group B, infants were the individuals with the highest values of eigenvector centrality and the males with the lowest (Table 4). 4. Discussion We tested here two hypotheses concerning the role of relatedness in the social structure of collared peccaries: (1) individuals

Table 4 Values of eigenvector centrality observed for each individual in each phase for spatial association. Group

Individuals

Phase 1

Phase 2

A

Belly Fore Gland Hind Neck Teco Nna Nnb Nga Ngb Nha Nhb Pedrita Pipoca Gigi Nininha

0.28 0.27 0.29 0.28 0.29 0.17 0.31 0.31 0.31 0.31 0.30 0.30 – – – –

0.29 0.27 0.35 0.34 0.28 0.23 – – – – – – 0.36 0.37 0.36 0.28

B

Dodo Fifi Lele Pepa Pepe Tico Pateta

0.41 0.40 0.37 0.42 0.41 0.22 0.37

0.36 0.37 0.42 0.40 0.36 0.31 0.42

with high degree of relatedness would be closely associated and (2) show more affiliative and less aggressive interactions than unrelated individuals. In agreement to our first hypothesis, Anderberg’s indices were negatively correlated with relatedness in group A in the first phase and in group B in both phases, indicating that close relatives were closer in the spatial structure and evidencing the role of relatedness as a factor which promotes cohesion. Proximity between relatives could facilitate the emergence of cooperative behaviors observed in this species, such as food sharing and predator defense (Byers and Bekoff, 1981) due to benefits associated to inclusive fitness (Hamilton, 1964). Our results, associated to high degree of relatedness among individuals in natural herds (Cooper et al., 2011), support the hypothesis that kin selection could have an important role in the evolution of social behavior in collared peccaries, as proposed by Byers and Bekoff (1981). Evidence that relatedness is correlated with association patterns between pairs of individuals are observed in a variety of mammalian species, for example, African elephants (Loxodonta africana, Archie et al., 2006), Atlantic spotted dolphins (Stenella frontalis, Welsh and Herzing, 2008), and mandrills (Mandrillus sphinx, Bret et al., 2013). Our observations in captivity support the idea from field data that collared peccaries herds are highly cohesive and coordinated units (Byers & Bekoff, 1981). The means and medians of Anderberg’s indices were lower than 0.58 in both groups, indicating strong spatial associations. In addition, social networks analysis revealed that groups were cohesive with no clustering divisions with all individuals connected. Patterns of spatial association were marked by infants occupying a central position and males being more peripheral in both studied groups. The centrality of the infants in the network may be linked to high adult tolerance, as exemplified by published events of food removal or attacks by juveniles without aggressive responses by adults (Byers and Bekoff, 1981). The tolerance to infants has been observed in many mammalian species. In yellow-bellied marmots (M. flaviventris) for example, infants are important for the maintenance of social cohesion, receiving more affiliattive interactions than older individuals (Wey and Blumstein, 2010). In the same way, juveniles of European free-tailed bats (Tadarida teniotis) are less

Please cite this article in press as: Biondo, C., et al., Social structure of collared peccaries (Pecari tajacu): Does relatedness matter? Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.08.018

G Model BEPROC-2886; No. of Pages 9

ARTICLE IN PRESS C. Biondo et al. / Behavioural Processes xxx (2014) xxx–xxx

7

Fig. 3. Sociograms of mutual rub interactions. (a and b) Group A, first and second phase, respectively; (c and d) group B, first and second phase, respectively. Nodes represent individuals and line widths, rates of interaction. Circle = female; rectangle = male; triangle = juvenile.

frequently targeted by adult aggressions (Ancillotto and Russo, 2014). Our second hypothesis, that kin would show more affiliative and less aggressive interactions than non-kin, was not supported by the results presented here, as the rates of agonistic and affiliative interactions did not correlate with the degree of relatedness

in the most cases. In addition, the social network analyses did not support a role of kinship in the formation of the clusters observed in the sociograms. These results could suggest that other factors such as sex, age and familiarity would be important in collared peccary social structure, as observed for other mammals. Sex and age affect the pattern of interactions of ring-tailed coatis (Nasua nasua):

Fig. 4. Sociograms of olfactory investigation and contact. (a and b) Group A, first and second phase, respectively; (c and d) group B, first and second phase, respectively. Nodes represent individuals and line widths, rates of interaction. Circle = female; rectangle = male; triangle = juvenile.

Please cite this article in press as: Biondo, C., et al., Social structure of collared peccaries (Pecari tajacu): Does relatedness matter? Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.08.018

G Model BEPROC-2886; No. of Pages 9 8

ARTICLE IN PRESS C. Biondo et al. / Behavioural Processes xxx (2014) xxx–xxx

Fig. 5. Sociograms of spatial association. (a and b) Group A, first and second phase, respectively; (c and d) group B, first and second phase, respectively. Nodes represent individuals and line widths, the corrected values of Anderberg’s index. Circle = female; rectangle = male; triangle = juvenile.

adult females groom each other more frequently than other members of the group; in contrast, juveniles and subadults rarely groom individuals of the same age (Hirsch et al., 2012). Prior familiarity predicts the proportion of time southern flying squirrels (G. volans) nest together in the winter, but not kinship (Garroway et al., 2013). Although we did not specifically evaluate the influence of sex, age and familiarity, some of our findings could suggest a role of these factors in the peccary social structure. We observed that males were central in mutual rub and olfactory investigation and contact networks in both phases and in agonistic interactions network in the second phase, with very strong relationships with some adult females. It could be explained by the fact that adult males and females rubbed each other more frequently than adult females did (Díaz, 1978). In addition, both mutual rub and olfactory investigation contact are involved in reproductive behavior: before display behavioral patterns exclusively associated to courtship and copulation, male and female frequently sniff, nuzzle and rubbed each other (Sowls, 1984). In addition, mutual rub data indicated that infants do not rub adults in the first phase and in the second phase, in group A, infants formed a cluster and performed this behavior exclusively among them. This result could be explained by a physical factor: infants cannot reach the gland of an adult individual to rub, and their effort to do this is clear. Therefore, it would be possible to hypothesize that rubbing individuals of similar ages could be more comfortable since they are similar in height. However, despite their similar heights in the first phase, infants did not rub each other. A possible explanation is that rubbing starts at a very specific time of the individual’s development, possibly due to delayed gland maturity, as infant gland do not seem to produce fluids until they are 40 days old (Hannon et al., 1991). Puppe (1998) did not find a role of relatedness in the rates of agonistic interactions between the individuals in another Suina species, the domestic pig (S. scrofa). However, unfamiliar dyads showed significantly more agonistic interactions than familiar (Puppe, 1998). Interestingly, the peccaries studied here were all familiar with each other in both groups, because they had already been together before this study, and showed lower rates of agonistic interactions compared to the rates of affiliative interactions.

As we found that relatedness affects spatial proximity but not the rates of affiliative and agonistic interactions, we cannot discard the importance of other factors. Thus, additional studies are needed to clarify which intrinsic factors are important in the patterns of interactions of collared peccary social structure. 5. Conclusions This study contributes toward our understanding of social structure of Suina species, since we addressed for the first time the importance of relatedness in the social interactions and spatial association of a species of the Neotropical family Tayassuidae. In agreement with our hypothesis that kin were in close proximity in the social structure, we found a correlation between the degree of relatedness and the spatial association in group B in both phases and in group A in the first phase, which suggests some importance of kinship as a factor that promotes cohesion in peccary social groups. However, contrary to our hypotheses, we found no evidence that kin show more affiliative and less aggressive interaction than non-kin in both groups. It suggests that relatedness does not predict the rates of interactions. The motivations to interact could be influenced by other variables, such as sex, age, and familiarity and other studies needs to be done to explain which factors influences the rates of interactions and the social structures of collared peccaries. Acknowledgements We would like to thank Dr. Jerry Hogan for the invitation to write this manuscript. Manuel Carrano for permitting us to conduct this research in his farm; Valdir, Nivaldo and Alfio Biondo for valuable support with the management of the animals; Vanilda A. M. Biondo for helping in the behavioral observations; Sérgio L. G. Nogueira-Filho and Guilherme Carrano for the assistance in the feed formulation; Érika S. Tavares, Tania E. Matsumoto and Flávia T. Presti for aiding in the genetic analyses; Fábio S. R. do Amaral and two anonymous reviewers for helpful comments and suggestions

Please cite this article in press as: Biondo, C., et al., Social structure of collared peccaries (Pecari tajacu): Does relatedness matter? Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.08.018

G Model BEPROC-2886; No. of Pages 9

ARTICLE IN PRESS C. Biondo et al. / Behavioural Processes xxx (2014) xxx–xxx

on an earlier version of the manuscript. Funding was provided by FAPESP (02/04356-0) and CNPq (140083/2002-2). This work was developed in the Research Center on Biodiversity and Computing (BioComp) of the Universidade de São Paulo (USP), supported by the USP Provost’s Office for Research. This study was conducted according to the Brazilian laws.

References Agnarsson, I., May-Collado, L.J., 2008. The phylogeny of Cetartiodactyla: the importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies. Mol. Phylogenet. Evol. 48, 964–985. Altmann, J., 1974. Observational study of behavior – sampling methods. Behaviour 49, 227–267. Ancillotto, L., Russo, D., 2014. Selective aggressiveness in European free-tailed bats (Tadarida teniotis): influence of familiarity, age and sex. Naturwissenschaften 101, 221–228. Anderberg, M.R., 1973. Cluster Analysis for Applications. Academic Press, New York. Archie, E.A., Moss, C.J., Alberts, S.C., 2006. The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proc. R. Soc. B: Biol. Sci. 273, 513–522. Benjamini, Y., Yekutieli, D., 2001. The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165–1188. Biondo, C., (PhD thesis) 2006. Estrutura social e alo-amamentac¸ão de catetos (Tayassu tajacu) em cativeiro. Universidade de São Paulo, São Paulo. Biondo, C., Keuroghlian, A., Gongora, J., Miyaki, C.Y., 2011. Population genetic structure and dispersal in white-lipped peccaries (Tayassu pecari) from the Brazilian Pantanal. J. Mammal. 92, 267–274. Bissonette, J.A., (PhD thesis) 1976. Relationship of social organization in collared peccaries to resource utilization. University of Michigan, Ann Arbor. Borgatti, S.P., 2002. NetDraw Software for Network Visualization. Analytic Technologies, Lexington, KY. Boutin-Ganache, I., Raposo, M., Raymond, M., Deschepper, C.F., 2001. M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. Biotechniques 13, 24–27. Bret, C., Sueur, C., Ngoubangoye, B., Verrier, D., Deneubourg, J.L., Petit, O., 2013. Social structure of a semi-free ranging group of mandrills (Mandrillus sphinx): a social network analysis. PLOS ONE 8, e83015. Byers, J.A., Bekoff, M., 1981. Social, spacing, and cooperative behavior of the collared peccary, Tayassu-tajacu. J. Mammal. 62, 767–785. Clutton-Brock, T., Janson, C., 2012. Primate socioecology at the crossroads: past, present, and future. Evol. Anthropol. 21, 136–150. Cooper, J., Vitalis, R., Waser, P., Gopurenko, D., Hellgren, E., Gabor, T., DeWoody, J., 2009. Quantifying male-biased dispersal among social groups in the collared peccary (Pecari tajacu) using analyses based on mtDNA variation. Heredity 104, 79–87. Cooper, J., Waser, P., Gopurenko, D., Hellgren, E., Gabor, T., DeWoody, J., 2010. Measuring sex-biased dispersal in social mammals: comparisons of nuclear and mitochondrial genes in collared peccaries. J. Mammal. 91, 1413–1424. Cooper, J.D., Waser, P.M., Hellgren, E.C., Gabor, T.M., DeWoody, J.A., 2011. Is sexual monomorphism a predictor of polygynandry? Evidence from a social mammal, the collared peccary. Behav. Ecol. Sociobiol. 65, 775–785. Dalla Vecchia, A.C., Biondo, C., Sanches, A., Keuroghlian, A., Miyaki, C.Y., Galetti, M., Galetti Jr., P.M., 2011. Isolation and characterization of microsatellite loci for white-lipped peccaries (Tayassu pecari) and cross-amplification in collared peccaries (Pecari tajacu). Conserv. Genet. Resour. 3, 151–154. Díaz, G.A.C., 1978. Social behavior of collared peccary (Tayassu tajacu) in captivity. CIEBA 22, 73–126. Durrell, J., Sneddon, I., O’connell, N., Whitehead, H., 2004. Do pigs form preferential associations? Appl. Anim. Behav. Sci. 89, 41–52. Ferraz, K.M.B., Izar, P., Sato, T., Nishida, S., 2013. Social and spatial relationships of capybaras in a semi-confined production system. In: Moreira, J.R., Ferraz, K.M.P.M.B., Herrera, E.A., Macdonald, D.W. (Eds.), Capybara. Springer, New York.

9

Garroway, C.J., Bowman, J., Wilson, P.J., 2013. Complex social structure of southern flying squirrels is related to spatial proximity but not kinship. Behav. Ecol. Sociobiol. 67, 113–122. Hamilton, W.D., 1964. The genetical evolution of social behaviour. J. Theor. Biol. 7, 1–52. Hannon, P.G., Dowdell, D.M., Lochmiller, R.L., Grant, W.E., 1991. Dorsal-gland activity in peccaries at various physiological states. J. Mammal. 72, 825–827. Hemelrijk, C.K., 1990a. A matrix partial correlation test used in investigations of reciprocity and other social-interaction patterns at group level. J. Theor. Biol. 143, 405–420. Hemelrijk, C.K., 1990b. Models of, and tests for, reciprocity, unidirectionality and other social-interaction patterns at a group level. Anim. Behav. 39, 1013–1029. Hinde, R.A., 1976. Interactions, relationships and social-structure. Man 11, 1–17. Hirsch, B.T., Stanton, M.A., Maldonado, J.E., 2012. Kinship shapes affiliative social networks but not aggression in ring-tailed coatis. PLoS ONE 7. Iacolina, L., Scandura, M., Bongi, P., Apollonio, M., 2009. Nonkin associations in wild boar social units. J. Mammal. 90, 666–674. Kalinowski, S.T., Wagner, A.P., Taper, M.L., 2006. ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol. Ecol. Notes 6, 576–579. Kaminski, G., Brandt, S., Baubet, E., Baudoin, C., 2005. Life-history patterns in female wild boars (Sus scrofa): mother–daughter postweaning associations. Can. J. Zool. 83, 474–480. Kappeler, P.M., Barrett, L., Blumstein, D.T., Clutton-Brock, T.H., 2013. Constraints and flexibility in mammalian social behaviour: introduction and synthesis. Philos. Trans. R. Soc. B: Biol. Sci. 368. Kappeler, P.M., van Schaik, C.P., 2002. Evolution of primate social systems. Int. J. Primatol. 23, 707–740. Keuroghlian, A., Eaton, D.P., Longland, W.S., 2004. Area use by white-lipped and collared peccaries (Tayassu pecari and Tayassu tajacu) in a tropical forest fragment. Biol. Conserv. 120, 411–425. Mayer, J.J., Brandt, P.N., 1982. Identity, distribution, and natural history of the peccaries, Tayassuidae. In: Mares, M.A., Genoways, H.H. (Eds.), Mammalian Biology in South America. Pymatuning Laboratory of Ecology, University of Pittsburgh, Linesville. Newman, M.E.J., 2004. Analysis of weighted networks. Phys. Rev. E 70. Peakall, R., Smouse, P.E., 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295. Puppe, B., 1998. Effects of familiarity and relatedness on agonistic pair relationships in newly mixed domestic pigs. Appl. Anim. Behav. Sci. 58, 233–239. Raymond, M., Rousset, F., 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249. Rohrer, G.A., Alexander, L.J., Hu, Z., Smith, T., Keele, J.W., Beattie, C.W., 1996. A comprehensive map of the porcine genome. Genome Res. 6, 371. Rohrer, G.A., Alexander, L.J., Keele, J.W., Smith, T.P., Beattie, C.W., 1994. A microsatellite linkage map of the porcine genome. Genetics 136, 231. Sambrook, J., Fritsch, E.F., Maniatis, T., 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory. Schülke, O., Wenzel, S., Ostner, J., 2013. Paternal relatedness predicts the strength of social bonds among female rhesus macaques. PLOS ONE 8. Silk, J.B., 2007. The adaptive value of sociality in mammalian groups. Philos. Trans. R. Soc. B: Biol. Sci. 362, 539–559. Sowls, L.K., 1984. The Peccaries. The University of Arizona Press, Tucson, AZ. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538. Wagner, A., Creel, S., Kalinowski, S., 2006. Estimating relatedness and relationships using microsatellite loci with null alleles. Heredity 97, 336–345. Welsh, L.S., Herzing, D.L., 2008. Preferential association among kin exhibited in a population of Atlantic spotted dolphins (Stenella frontalis). Int. J. Comp. Psychol. 21, 1–11. Wey, T., Blumstein, D.T., Shen, W., Jordán, F., 2008. Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim. Behav. 75, 333–344. Wey, T.W., Blumstein, D.T., 2010. Social cohesion in yellow-bellied marmots is established through age and kin structuring. Anim. Behav. 79, 1343–1352. Whitehead, H., 2009. SOCPROG programs: analysing animal social structures. Behav. Ecol. Sociobiol. 63, 765–778. Widdig, A., Nürnberg, P., Krawczak, M., Streich, W.J., Bercovitch, F.B., 2001. Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. Proc. Natl. Acad. Sci. U. S. A. 98, 13769.

Please cite this article in press as: Biondo, C., et al., Social structure of collared peccaries (Pecari tajacu): Does relatedness matter? Behav. Process. (2014), http://dx.doi.org/10.1016/j.beproc.2014.08.018