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. Author manuscript; available in PMC: 2021 Jul 28.
Published in final edited form as: Folia Primatol (Basel). 2020 Jul 28;91(6):610–621. doi: 10.1159/000508761

Variation in adult male-juvenile affiliative behavior in Japanese macaques (Macaca fuscata)

Kylen N Gartland 1, Colin M Brand 1, Lawrence R Ulibarri 1, Frances J White 1
PMCID: PMC7704533  NIHMSID: NIHMS1600606  PMID: 32721965

Abstract

Adult males of some primate species are known to positively interact with juveniles. In cases where paternal certainty is high, these behaviors have been largely attributed to the paternal investment hypothesis. Males have also been observed to interact with non-kin juveniles, which has often been explained in terms of mating effort. Here, we examined variation in adult male-juvenile affiliation in semi-free ranging Japanese macaques (Macaca fuscata) at the Oregon National Primate Research Center against possible influencing factors such as age, dominance rank, and female affiliation and tested for fitness benefits. We conducted 154 hours of focal observations on 14 adult males from June to September 2018. Males differed significantly in their rate of juvenile-directed affiliation, but not in their fitness in terms of number of offspring. There was a significant positive correlation between rank and age in the group, indicating that in this group rank does not conform to the classic inverted-U pattern observed elsewhere in this species. Although there was a significant positive correlation between rank and juvenile-directed affiliation, the highest-ranking male had few offspring and exhibited little juvenile-directed affiliation. These results suggest little to no preliminary support for either the paternal investment or mating effort hypotheses as explanations for juvenile-directed affiliation. This study suggests that there are multiple behavioral strategies for older males that may influence reproductive success.

Keywords: Japanese macaque, juvenile, affiliation, adaptive hypotheses, adult male

Introduction

In mammals, direct care of young by adult males occurs in approximately 5–10% of species [Clutton-Brock, 1991; Woodroffe & Vincent, 1994]. However, care by males is more common in primates than other mammals as this set of behaviors has been observed in 30–40% of primate genera [Clutton-Brock, 1991; and references therein]. Male care of immatures may be obligate or facultative, and has been explained under a number of evolutionary models including the paternal investment hypothesis and the mating effort hypothesis [Busse and Hamilton, 1981; Wright, 1990; Clutton-Brock, 1991; Smuts and Gubernick, 1992; Paul et al., 1996; van Schaik and Paul, 1996; Mitani and Watts, 1997; Silk, 1999; Boose et al., 2018].

The paternal investment hypothesis predicts that males should 1) preferentially interact with related infants and that 2) these male-infant relationships should increase the infant’s chances of survival and future reproductive success. It has been suggested that paternal investment can be positively associated with the degree of paternal certainty [Garber and Leigh, 1997; Fernandez-Duque et al., 2009], however, the paternity certainty hypothesis has not been an adequate explanation for the evolution of male care of young in all nonhuman primate species [Smuts and Gubernick, 1992].

The mating effort hypothesis proposes that there is a mutually advantageous and reciprocal relationship between males and females in which male care of immatures occurs under the following conditions: 1) infants can benefit from male care, 2) females (or infants) can control and offer important benefits to males, and/or 3) females have opportunities to compare the behavior of different males and distribute mating benefits based on this comparison [Smuts and Gubernick, 1992]. For example, studies have reported that male vervet monkeys (Chlorocebus pygerythrus) were observed to be more affiliative with infants when that infant’s mother was in visual contact [van Schaik & Paul, 1996]. Another study of Assamese macaques (Macaca assamensis) found that females demonstrated preference, as measured through selective affiliation, for two particular male traits: dominance or access to resources and prior affiliation with immatures (Haunhorst, Fürtbauer, Schülke, & Ostner, 2019). Male care of infants has been observed to increase male reproductive success in a number of species [Clutton-Brock, 1991; van Schaik and Paul, 1996; Silk, 1999; Rosenbaum et al., 2018]. According to this hypothesis, males that provide care to immatures should be more likely to sire the female’s subsequent offspring or have a generalized increase in reproductive success.

These two hypotheses offer adaptive, but not mutually exclusive, explanations for this set of behaviors. It is important to note that, for example, a male could affiliate with their own biological offspring both as a form of paternal investment and as a strategy to gain reproductive access to the offspring’s mother. In order to make inferences about support for these adaptive hypotheses, studies often evaluate individual factors (such as dominance rank, age, female affiliation, etc.) which may be highly correlated with male-juvenile affiliation. The age of the adult male has been observed to be highly correlated with frequency of male care in multiple species of macaques with older males more likely to affiliate with infants or immatures than younger males [Alexander, 1970; Langos et al., 2013]. Older males past their physical peak who may experience reduced likelihood of future reproductive opportunities may look to enhance their own fitness by investing more in their own immatures or by using juvenile-directed affiliation as an alternative mating strategy to gain social contact with the mother [Langos et al., 2013].

There is also evidence that both the sex and the age of the immature are important in male affiliative attention. Males have been observed to preferentially direct attention towards male immatures rather than females [Langos et al., 2013]. A sex-preference towards females, if found, could lend support to the mating effort hypothesis. Furthermore, while literature on the paternal investment hypothesis and mating effort hypothesis have focused primarily on mother-dependent immatures, adult male primates have also been known to form long-term affiliative relationships with independent juvenile individuals, either kin or non-kin [Alexander, 1970; Horrocks and Hunte, 1993; Buchan et al., 2003; Moscovice et al., 2009; Rosenbaum et al., 2016]. For example, there is evidence in mountain gorillas (Gorilla beringei beringei) for long-term affiliative relationships between adult males and unrelated maturing group members [Rosenbaum et al., 2015, 2016]. In these cases, relationships between juveniles and adult male gorillas were found to be based on the adult male’s rank rather than paternity and were demonstrated to persist across both developmental classes and social upheaval (ibid.). As such, it is important to consider male rank as a potential correlate to juvenile-directed affiliation and as a possible factor to incorporate into hypothetical models. Furthermore, there may be additional unexplored benefits of juvenile-directed affiliation for the adult males. For example, the preferential focus on older male juveniles may serve to lay the foundation for future alliances or a preferential focus on maturing female juveniles may allow males to begin cultivating future mating opportunities.

It has been suggested that the expression of paternal behavior may be group-dependent rather than species-specific, and that seasonal variation may play a role in the degree to which these behaviors occur [Itani, 1959; Berghänel et al., 2011]. Paternal behavior has largely been observed to take the form of grooming, playing, and carrying, with increases in the rate of these behaviors during the birthing season [Itani, 1959; Alexander, 1970]. Male affiliative bonds with juveniles have been reported repeatedly in a number of macaque species, which may be a function of their high gregariousness and adaptability [Alexander, 1970; Berghänel, Ostner, Schröder, & Schülke, 2011; Itani, 1959; Maestripieri & Carroll, 1998; Minge, Berghänel, Schülke, & Ostner, 2016; Mitchell, 1969]. As such, macaques present a uniquely well-suited model genus for examining juvenile-directed affiliative behavior. A study of male-immature relationships in Assamese macaques (Macaca assamensis) suggested that these relationships extended beyond infancy and were primarily maintained by the immature [Minge et al., 2016]. However, it was unclear whether these male-immature relationships represented true paternal care [ibid]. It is also important to note that while there are reports of these behaviors across the Macaca genus, the frequency and intensity of juvenile-directed affiliation varies across both populations and species. However, these behaviors have been particularly reported in Japanese macaques (Macaca fuscata).

Japanese macaques live in large multi-male multi-female social groups characterized by matrilineal hierarchies and male dominance (Itani, Tokuda, Furuya, Kano, & Shin, 1963; Watanabe, 1979). Male parental behavior has been repeatedly observed in this species. A study on seasonality of parental behavior in adult male Japanese macaques found that there was a significant increase in these behaviors during the birthing season [Alexander, 1970]. Alexander (1970) concluded that over 75% of sexually mature males exhibited an increase in affiliative behavior with juveniles (classified as 1 to 4-year-old individuals) during the birthing season. Furthermore, this seasonal shift was consistent across all ages and ranks of adult males, and younger males (aged 5 to 7) were more likely to engage in play behaviors with juveniles across seasons. It was also observed that some high-ranking males invested in specific juveniles [Alexander, 1970]. Some studies have suggested that this behavioral trend is a response by the adult males to distress of juveniles abandoned by their mothers with the birth of a newborn [Itani et al., 1963]. Another study, which observed that dominant males maintained relationships with newborns, young juveniles, and their mothers following the birthing season, suggested instead that dominant males may play a role in the socialization of the immatures [Alexander, 1970]. It is possible that this early socialization contributes to establishing and maintaining the authority of the dominant males among the next generation of troop members and may offer an evolutionary explanation of the ability of male Japanese macaques to maintain authority after their physical peak [Imanishi, 1965; Yamada, 1966].

Based on the propensity for male Japanese macaques to form affiliative bonds with juveniles, this study used the Japanese macaque population at the Oregon National Primate Research Center to investigate 1) whether there is variation between adult males in juvenile-directed affiliative behaviors, 2) whether age and/or dominance rank influence variation in juvenile-directed affiliation, and 3) if there is any significant relationship between reproductive success and variation in juvenile-directed affiliation. We tested the correlation between rates of juvenile-directed affiliation, affiliation received from females, fitness, age, and dominance rank. This group included both natal and non-natal juveniles. Non-natal individuals were introduced to the group as weaned yearlings. We also investigated the variation in direction of affiliative behavior towards natal or non-natal juveniles where possible to assess potential kin-bias. The presence of non-natal juveniles offered an opportunity to preliminarily exclude paternity as a sole explanation for this behavior. These two lines of inquiry allowed us to explore whether this behavior is a potential expression of either the paternal investment hypothesis or the mating effort hypothesis.

We would expect that if adult males who have higher rates of juvenile-directed affiliation also have higher rates of received affiliative behavior from adult females and higher fitness, then this would be consistent with a female preference for males that affiliate with juveniles. This would support male affiliation with juveniles as a potential mechanism of mating effort. In addition, we would expect that if adult males preferentially affiliated with natal juveniles who are more likely to be their own offspring or a genetic relative, this would be consistent with affiliation with juveniles as a form of paternal investment.

Materials and Methods

Housing

The study group was located at the Oregon National Primate Research Center and housed in a one-acre outdoor enclosure with steel walls and open access to an indoor feeding room measuring approximately 3 meters by 12 meters. The corral included a number of platforms and other structures for play and enrichment. The group was fed a diet of commercial monkey chow provided twice daily as well as supplementary fruits, vegetables, and grains. Water was available ad libitum. The housing area also included two observation towers outside but overlooking the corral from which observations were conducted. As part of general animal husbandry practices of the ONPRC, animals were given unique markings on their backs, allowing for individual identification of all members of the group from the observation tower.

Study Subjects and Age Classifications

These data were collected on the semi-free ranging group of Japanese macaques at the Oregon National Primate Research Center (ONPRC) in Beaverton, Oregon, USA. At the outset of the study, the focal group included 134 females and 87 males aged between 0–25 years (Table 1).

Table 1:

Japanese Macaque Focal Group Demographics as of June 2018

Infant Juvenile Subadult Adult Aged Total
Females 4 70 12 31 17 134
Males 1 62 8 11 5 87
Total 5 132 20 42 22 221
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Each individual in the troop was given unique dye markings on their backs to allow for identification. Age classifications were provided by the ONPRC [K. Coleman, pers. comm.]. The provided age classifications were assigned as follows: infants (<1 year), juveniles (>1 year to 4 years), subadults (>4 to 7 years), adults (>7 to 15 years) and aged (>15 years).

Juveniles were easily visually distinguished from infants by their given markings, as well as by their decreased nursing and increased independence at 1–2 years of age [Coleman, Robertson, and Bethea 2011; personal observations]. Additionally, there were juveniles of approximately 1 year of age born in extra-troop harem groups, that had been introduced into the group. These juveniles may have had distant biological relatives within the larger group, but they had not been raised with these genetic relatives nor integrated into the maternal hierarchies. There was a total of six of these juveniles at the beginning of the study, five males and one female, ranging from 11–17 months old. These individuals were easily identified by black dye on their heads. While these juveniles were successfully accepted into the existing group, they were non-natal and thus had no genetic parents or strong kin alliance system within the group.

For this study, 14 males classified as either aged or adult individuals were the subjects of focal follows. Table 2 lists male, age class, age, fitness, and rank. Rank was classified according to three classes (high, middle, low) based upon priority-of-access to enrichment food observations. For the study subjects, the average age of a male classified as “aged” was 20.25 (± 3.02) and the average age of a male classified as “adult” was 8.44 (± 0.78) years.

Table 2:

Individual Subject Identification, Age Class, Age, Rank, Fitness and Number of Mothers

ID Age Class Age (Years) Rank Fitness Number of Mothers
M1 Aged 25 High 4 4
M2 Aged 21 High 3 3
M3 Aged 20 High 2 2
M4 Aged 18 High 6 6
M5 Aged 17 High 5 5
M6 Adult 9 Low 4 4
M7 Adult 10 Middle 6 6
M8 Adult 8 Middle 11 11
M9 Adult 8 Middle 5 4
M10 Adult 8 Low 4 4
M11 Adult 8 Low 2 2
M12 Adult 9 Low 10 10
M13 Adult 8 Low 2 2
M14 Adult 7 Low 2 2
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Behavioral Observations

Observations were conducted between June and September 2018 on Monday through Friday from 0830 to 1600 h. The data collection period largely overlapped with birth season, which ranges from May-August in Japanese macaques at the ONPRC with the largest number of births usually occurring in June and July, and is the aforementioned peak for male-juvenile affiliative behavior [Alexander, 1970; Coleman et al., 2011]. We collected 154 hrs of data with equal effort (11 hours) per male. The subjects are frequently observed by staff and public visitors and so were behaviorally acclimated to human presence.

Fifteen minute focal follows of single subjects were conducted using 30-second instantaneous scans [Altmann, 1974]. Approximately 20 focal follows were conducted per day with breaks in observation between follows (1–2 follows per subject per day). The order of subjects for focal follows was randomly selected such that each individual was the subject of at least 1 follow per day. The lead author collected all data.

We recorded social and solitary behaviors (Table 3). All social behaviors included partner classification where possible. It was not always possible to reliably identify individuals aside from the fourteen study subjects. Thus, unless the social partner was another adult male study subject, potential partners were coded according to classes rather than individual identifiers. These classes included adult female, sub-adult individual, juvenile individual, infant, or unknown individual. Where possible, we recorded whether a male was interacting with a natal or non-natal juvenile. Directionality (recipient versus instigator) was recorded for social behaviors when possible.

Table 3:

Ethogram of Recorded Behaviors and Modifiers

Behavioral Class Behavior Definition
Other Social (SOC) Groom (GM) Manipulation of the hair of another individual (s) with hand and/or mouth
Play (PL) Social interactions that are characterized by apparent low tension; may be accompanied by a “play face” (facial gesture in which mouth is open and facial features are relaxed). May include any of the following: grunting, wrestling, sham-biting, jumping on, jumping over, chasing, fleeing, hiding.
Tolerant Contact (TO) Ventral Social (VS) Other (OT) Subject is in physical contact with another individual(s).
Huddling and/or close stationary contact other than grooming, with another individual(s).
Subject is engaged in behavior not listed in Ethogram; describe in comments section of observation sheet
Aggressive (AGG) Chase (CH) Behavior that involves pursuit past the location the recipient maintained at the start of the interaction.
Threat (TH) Expression containing facial, vocal, or physical components (may include head thrusting, open-mouth threat, scream, raised eyebrow, ground beating, lunge).
Bite (BI) During which the skin/limb of another animal is grasped with the teeth; may be accompanied by head shaking.
Contact (CO) May include nipping, grabbing, kicking, pulling, pushing, poking, slapping, pulling hair, butting, shoving.
Other (OT) Subject is engaged in other form of aggressive behavior not covered by the above categorizations.
Socio-Sexual (SOS) Mount Subject mounts another individual.
Grab (GR) Subject physically grabs another individual (usually female) in sexual approach. Scored as receptive if individual is female.
Copulate (CO) Subject engages in copulation with another individual.
Proceptive Approach (PA) Subject receives sexual approach, sexual grab, or display of genitalia/sexual swelling from a female individual.
Solitary (SOL) Abnormal (AB) Subject is engaged in atypical behavior; may include any of the following: stereotype, self-bite, copraphagy, floating limb.
Eat (EA) Subject is ingesting liquid (drinking) or solid food material (common usage).
Explore (EX) Subject inspects or manipulates object other than food.
Forage (FO) Subject is searching through grass or other substrate material, presumably for food.
Locomotion (LO) Subject engages in movement from one location to another while using its entire body.
Self-Groom (SG) Picking through and/or slowly brushing aside own hair with hands and/or mouth.
Self-Play (SP) Subject engages in independent play with active movement; may include swinging, running, or spinning on objects.
Sleep (SL) Subject appears to be sleeping; is stationary with eyes closed.
Stationary (ST) Subject is inactive without motile movement; may still involve head or arm movement.
Other (OT) Subject is engaged in behavior not listed in Ethogram; describe in comments section of observation sheet.
Out of View (OV) Individual is out of observer view. Do not record partner.
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Data Analyses

We calculated hourly rates of juvenile affiliation per adult male based on the number of affiliative events observed divided by the number of observation hours. We calculated rates based exclusively on juvenile-directed affiliation. Affiliative events were all events in which an adult male was observed engaged in grooming, play, tolerant contact, ventro-social contact, or other social behaviors (such as carrying) in which the social partner was a juvenile (Table 3). The study period encompassed four equal observation time blocks resulting in four affiliation rates per focal male (N=56).

The original intention was to create a dominance hierarchy based on aggressive interactions between the adult males. However, the resulting matrix was largely empty, with many males never having been observed interacting with each other. As a result, we were unable to create a reliable linear dominance hierarchy for use in statistical analyses. Therefore, we opted to categorize individuals as having either high, middle, or low rank. These rank categorizations were based on opportunistic observations including priority-of-access to enrichment food and frequency with which individuals became involved in settling aggressive encounters within the group.

We ran a one-way ANOVA of the rate of juvenile-directed affiliation, again using individual identification as a random factor, to ascertain whether males differ significantly in their rate of affiliative behavior towards juveniles. We then ran non-parametric Spearman’s correlations with 0.05 level of significance for the following pairs of variables: (1) dominance rank and age, (2) dominance rank and the rate of juvenile-directed affiliation, and (3) the rate of affiliative behavior received from adult females and the rate of juvenile-directed affiliation.

We used a G-test of goodness-of-fit to equal fitness to examine whether males differed in their observed number of offspring (Sokal & Rohlf, 2012). Fitness was measured as the total number of offspring per male. Number of offspring ranged from 2-11 from an average of four mothers (Table 2). We reported the number of different females the males sired offspring with for each male (Table 2). The number of sired offspring was determined from genetic data for each male provided by the ONPRC. The oldest identified offspring was approximately 17 years old and the youngest was approximately 1 year old. The youngest age of male reproduction in this study sample was five years of age and the oldest male in this study is 25. As such, this data is presumably a reasonable estimate of fitness for this group. Variation in access to females was not included as a tested variation as the number of females in the group has remained consistent over time. Finally, in order to see whether fitness was determined by age, we ran a linear regression of fitness on age. All analyses were conducted using SAS©, version 9.4 (Cary, NC, USA).

Results

We observed 1,342 male-juvenile affiliative interactions by the 14 study subjects. Males displayed significant variation in the rate of affiliation directed at juveniles (F = 10.81; df = 1, 54; p<0.01). On average, males engaged in approximately 9 (mean=8.64 ±1.89) affiliation events with juvenile partners per hour. 36% (N=483) of the interactions were confirmed to be with non-natal juveniles. Two particular males (M2 and M4) exhibited 86% of the total non-kin interactions. These males interacted exclusively with non-natal juveniles and comprised 31% (N=154) and 55% (N=267) of these interactions, respectively. The remaining 14% non-natal interactions were by six other males. We could not identify the remaining 64% of interactions (N=859) as either natal or non-natal.

We did find that dominance rank was significantly correlated with age (r = 0.803; N = 14; p < 0.001). We found a significant positive correlation between rank and rate of juvenile-directed affiliation (r = 0.594; N = 14; p < 0.05). There was no significant correlation between affiliation received from adult females and rate of juvenile-directed affiliation (r=0.178; N =14; p=0.543), nor between fitness and rate of juvenile-directed affiliation (r=0.237; N=14; r=0.414). However, males did not differ significantly in fitness (G=19.53; p=0.108, n.s.) and we found no significant relationship between age and fitness (F=0.43; p=0.522, n.s.) (Figure 1).

Figure 1:

Figure 1:

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Linear regression of fitness and age

Discussion

In this study, we found a dominance structure in which rank was significantly positively correlated with age. Takahashi (2002) reported an age-rank relationship in dominance tenure in Japanese macaques such that both younger and aged males were either lower ranked or held high ranks for shorter-terms. However, long-term higher rank acquisition was also impacted by the continued tenure of previously dominant males, with incoming males experiencing a dominance plateau if current dominant individuals did not emigrate or disappear from the troop [Takahashi, 2002]. However, this study group also represents a departure from the inverted-U dominance structure [Cowlishaw, 1991; Takahashi, 2002].

Contrary to the traditional model in which dominant males have the greatest reproductive success, this has not been consistently observed in Japanese macaques [Eaton, 1974; Inoue et al., 1993; Takahata et al., 1999]. The lack of a significant correlation between age, rank, and fitness match what has been previously observed. Both genetic data and personal communications with ONPRC staff demonstrated that young males (aged approximately 8–10 years) have the highest fitness. While rank appears to translate to priority of access to food within this group, as is typical, it does not appear to translate into priority of access to females. This implies that female choice may be over-riding the male priority-of-access model and allowing females to preferentially mate with younger males.

We did not find any significant correlation between affiliation received from females and age or dominance rank. This would appear to suggest that females in this group do not have a statistically demonstrable preference for more dominant, or older, males. Similarly, the lack of significantly correlation between juvenile-directed affiliation and affiliation received from adult females suggests that females do not prefer more highly affiliative males. These results are in direct contrast to observed female preference for both dominance and affiliation with immatures demonstrated in Assamese macaques (Haunhorst et al., 2019), which may indicate species-level variation within the larger genus Macaca. We conclude that while there may be some degree of female preference operating within this group, it is not consistently a preference for high-ranking males. This is consistent with previously discussed Japanese macaque studies.

Many studies have related the variation in affiliation with juveniles by adult males to potential fitness benefits. The only significant correlation we found was between rate of juvenile-directed affiliation and rank. However, there was no significant correlation between rate of juvenile-directed affiliation and fitness. The lack of a significant correlation between rank (or age) and fitness is surprising, as the reproductive access conferred upon individuals by attaining high dominance rank has been well-recorded in previous literature [Alberts, Watts, & Altmann, 2003; Bulger, 1993; Cowlishaw, 1991; de Ruiter, 1993; Majolo, Lehmann, de Bortoli Vizioli, & Schino, 2012; Sukmak, Wajjwalku, Ostner, & Schülke, 2014; Watts, 2010]. This evidence suggests a complex relationship between fitness, age, rank, and juvenile-directed affiliation.

Animal care technicians and behavioral staff consistently identified M3 as the most dominant male. It is interesting to note that the top-ranking male (M3) had both a low rate of affiliation events with juveniles and a low reproductive success in comparison with the other older males. This reaffirms similar findings from studies of males in enclosed and semi-free ranging groups in which dominance was not correlated with number of offspring, or in which reproductive activity followed predictions based on the priority of access model but was interrupted by elements of female preference for lower ranking males [Inoue et al., 1993; Takahata et al., 1999]. However, as this current study was heavily influenced by the behavior of two specific males, it will be important to examine behavioral changes as male age increases and whether these results remain consistent for other individuals.

Similar to Alexander (1970), we observed that more dominant adult males affiliated most with juveniles and that two of these adult males each intensely invested in one particular juvenile. This suggests that these relationships are differentiated bonds and not a pattern of generally directed behavior. We observed that two males engaged in the highest rates of juvenile-directed affiliation (M2 & M4) and were observed interacting exclusively with non-natal juveniles. As these juveniles were born to parents not in the group and introduced at approximately one year of age, they can be eliminated as offspring of the affiliating males. This would suggest that paternal investment is not a strong evolutionary driver of this behavior in this population. While this behavior has clear benefits for the juvenile partner such as protection and access to better resources, the lack of genetic relationship between the juveniles and adult males makes identifying functional benefits for the adult males not immediately obvious. It is also possible, following previously established theory for infant-directed behavior in females (Silk, 1999), that the general low cost of juvenile-directed affiliation by males is outweighed by potential benefits despite the probability of the male having either sired the immature or gaining future mating opportunities. The benefits of these behaviors may have been diluted by low paternal certainty, however the behaviors themselves could still be functionally selected for as a byproduct of past selection for paternal or mating strategies. This should be a focus of further studies.

Reports by animal care technicians at the ONPRC and at other national primate research centers have confirmed that these juvenile-directed behaviors are not unique to the ONPRC Japanese macaque troop. There have been multiple observations of similar carrying and affiliative behaviors in rhesus macaque groups resident at the ONPRC and other institutions. While these observations have yet to be confirmed, the reported prevalence of these behaviors is of great interest from an evolutionary perspective. A long-term study would enable an examination of the longevity male-immature affiliative bonds and a seasonal comparison. Furthermore, the inclusion of multiple species would allow for an investigation of variation in behavioral patterns between species.

Acknowledgements

We are very grateful to the Behavioral Science Unit and the animal care technicians at the Oregon National Primate Research for their insight and contributions to this project. We would especially like to thank Dr. Kristine Coleman for her continued support and assistance in coordinating this project.

Funding Sources

The ONPRC receives funding from the National Institute of Health (NIH P51 OD011092).

Footnotes

Statement of Ethics

This study was approved by the Oregon National Primate Research Center (ONPRC) Institutional Animal Care and Use Committee (IACUC) (IP00001766) and followed the guidelines outlined in both the Animal Welfare Act (AWA, 1966–2002) and the Guide for the Care and Use of Laboratory Animals (NRC, 1996). The ONPRC is accredited by the Association for the Assessment and Accreditation of Laboratory Animal Care, International (AAALAC, International).

Disclosure Statement

The authors have no conflicts of interest to declare.

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