American Journal of Primatology 76:989–998 (2014)
RESEARCH ARTICLE The Function of Greetings in Male Tonkean Macaques ARIANNA DE MARCO1,2,3*, ANDREA SANNA1, ROBERTO COZZOLINO1, AND BERNARD THIERRY4,5 1 Fondazione Ethoikos, Radicondoli, Italy 2 Parco Faunistico di Piano dell’Abatino, Poggio San Lorenzo, Italy 3 Istituto di Scienze e Tecnologie della Cognizione, Consiglio Nazionale delle Ricerche, Rome, Italy 4 Centre National de la Recherche Scientifique, Département Ecologie, Physiologie et Ethologie, Strasbourg, France 5 Université de Strasbourg, Institut Pluridisciplinaire Hubert Curien, Strasbourg, France
Males living in multi‐male groups are both strong rivals and potential allies. In several primate species they regularly interact through ritualized exchanges known as greetings. We studied five captive groups of Tonkean macaques (Macaca tonkeana) to test five hypotheses regarding the social function of greetings. We found that greetings were mostly reciprocal interactions, and that they often involved physical contact and facial displays. Although they were mostly initiated by the higher‐ranking individual in each dyad, subordinates could initiate approximately one‐third of greetings, which indicates that greetings do not serve as a formal acknowledgement of dominance relationships. Although greeting frequencies were negatively correlated to the frequency of supplantations and conflicts, they were not significantly influenced by age and dominance status, showing that greetings are not used to appease partners or decrease tension between males. Males most frequently greeted partners with whom they spent more time in proximity and body contact, and this is consistent with the hypothesis that greetings play a role in reinforcing social relationships. Lastly, greetings increased in frequency between individuals involved in challenges for rank, lending support to the hypothesis that males assess the state of their social relationships through greetings. Am. J. Primatol. 76:989–998, 2014. © 2014 Wiley Periodicals, Inc. Key words:
greeting; affiliation; dominance; ritualization; Macaca tonkeana
INTRODUCTION Group living is a quite demanding adaptive strategy because it creates an environment in which conspecifics have to compete and cooperate with the same partners. This is especially true for adult males residing in multi‐male social systems; although they are rivals regarding reproductive access, they are also potentially powerful allies for each other. Sexual selection has armed primate males with a competitive drive and dangerous canines [Plavcan, 2004; van Hooff, 2000], and the antagonistic character of their social relationships has been emphasized by observers, with male–male interactions described mostly as neutral or hostile, especially in monkey species displaying male dispersal [Caldecott, 1986; Smuts, 1987; Strier, 2000]. On the other hand, a fair number of non‐agonistic interactions do occur between males, and we have learned that resident males can negotiate cooperation, reconcile, and appease one another [Aureli & de Waal, 2000; van Hooff & van Schaik, 1994]. In several primate species, ritualized exchanges of communicative signals occur between males, and they are usually known as greetings. However, researchers have used a variety of labels to designate similar or different motivations and
© 2014 Wiley Periodicals, Inc.
adaptive functions for these interactions, and it is currently difficult to accurately delineate the range of behaviors and contexts included. In baboons (Papio spp.) a male typically greets another male by approaching him while producing affiliative facial expressions and gestures. Baboon greetings take place in several contexts and fulfill different functions that are not necessarily mutually exclusive. In some baboon species, they tend to occur more often between individuals that have good quality relationships with each other, meaning that they frequently interact using non‐agonistic behaviors [Whitham & Maestripieri, 2003]. Previous studies suggest that the risky behavior of exposing a vulnerable area such as the genitals during
Correspondance to: Arianna De Marco, Parco Faunistico di Piano dell’Abatino, via Capofarfa 50, 02030 Poggio san Lorenzo (Ri), Italy. E‐mail: [email protected] Received 1 September 2013; revised 7 March 2014; revision accepted 9 March 2014 DOI: 10.1002/ajp.22288 Published online 9 April 2014 in Wiley Online Library (wileyonlinelibrary.com).
990 / De Marco et al.
greetings makes this behavior a reliable interaction allowing males to test and/or reinforce social relationships [Colmenares, 1990, 1991; Fraser & Plowman, 2007; Smuts, 2002; Smuts & Watanabe, 1990; Whitham & Maestripieri, 2003]. It was also hypothesized that greetings reduce social tension and help resolve conflicts [Abegglen, 1984; Colmenares et al., 2000; Smuts & Watanabe, 1990]. In most baboons, greetings are generally initiated by the lower‐ranking individual in a dyad, so they may convey submission [Colmenares, 1990; Fraser & Plowman, 2007; Hausfater & Takacs, 1987; Smuts & Watanabe, 1990]. In Guinea baboons (Papio papio), however, there does not seem to be any link between greeting and dominance rank [Whitham & Maestripieri, 2003], and in hamadryas baboons (P. hamadryas), males use an additional form of greeting whereby one male approaches another, presents his hindquarters, and leaves to notify travel direction [Abegglen, 1984; Kummer, 1968]. Ritualized affiliative behaviors have also been described in macaques (Macaca spp.). In Barbary and Tibetan macaques (Macaca sylvanus and Macaca thibetana), males use infants in triadic interactions to approach each other and initiate affiliative interactions, which may strengthen their social relationships [Deag, 1980; Henkel et al., 2011; Ogawa, 1995; Paul et al., 1996]. Similar behaviors have also been reported in bonnet macaques (Macaca radiata) [Silk & Samuels, 1984]. It is worth adding that in these three species, males can also contact each other at the dyadic level using embraces, mounts or genital grips [Ogawa, 1995; Preuschoft, 1995; Silk, 1994; Sugiyama, 1971]. In long‐tailed macaques (Macaca fascicularis), males occasionally grasp another individual’s hindquarters, and they may grasp each other face to face [Thierry, 1985]. Lastly, penis grabbing and mounting have been reported as greetings in crested macaques (Macaca nigra), one of the seven species originating from the Sulawesi island [Reed et al., 1997]. Since greeting interactions are generally observed outside the context of aggression in macaques, they should not have an appeasement function, but rather serve to regulate social relationships between males. However, except for triadic interactions in Barbary macaques, the function of greetings has not been systematically examined in macaques to date. Our study addresses greetings between males in a species from Sulawesi, the Tonkean macaque (Macaca tonkeana). This species is characterized by relaxed dominance relationships and a high level of social tolerance compared to other macaques [Thierry, 2007, 2010]. Affiliative contacts and appeasement signals are especially frequent between Tonkean macaques [De Marco et al., 2011; Demaria & Thierry, 2001; Thierry, 1984]. They also show a high propensity to prevent the escalation of conflicts; third parties can stop aggression by addressing appeasement
Am. J. Primatol.
signals to adversaries [Petit & Thierry, 1994], while group‐mates uninvolved in a conflict are more likely to affiliate with one another after witnessing such appeasement [De Marco et al., 2010]. We took the main five hypotheses that emerge from previous studies regarding the function of greetings, and tested them in Tonkean macaques. They are not necessarily mutually exclusive, and we can formulate them as follows: 1. Social relationship reinforcement hypothesis [Fraser & Plowman, 2007; Smuts & Watanabe, 1990]: if greetings are used to reinforce social relationships, individuals should primarily greet their preferred partners, that is, individuals they are frequently seen to be close to. 2. Appeasement hypothesis [Hausfater & Takacs, 1987; Kummer et al., 1974]: if greetings are used to stop conflicts, they should occur immediately after aggression, and in each dyad the lower‐ ranking partner should initiate them more often that the higher‐ranking one. 3. Formal dominance hypothesis [Fraser & Plowman, 2007; Hausfater & Takacs, 1987; Whitham & Maestripieri, 2003]: if greetings are an acknowledgement of dominance relationships between males, they should be strictly unidirectional within each dyad. 4. Social relationship testing hypothesis [Colmenares, 1990; Smuts & Watanabe, 1990; Whitham & Maestripieri, 2003]: if greetings are used by males to test the state of their social relationships, they should greet the partners with whom their social relationships are least secure more often, that is, those with whom they have more frequent agonistic interactions, or with whom dominance relationships are unstable; patterns of greetings should also be dependent on the direction of dominance relationships. 5. Tension reduction hypothesis [Abegglen, 1984; Colmenares, 1990; Hausfater & Takacs, 1987; Smuts & Watanabe, 1990]: if greetings are used to decrease tension between partners, their frequencies should vary consistently with individual dominance status, rates of agonistic interactions and signs of anxiety, and they should increase in periods of social disturbance.
METHODS Subjects We studied five captive groups of Tonkean macaques (Table I), which belong to a population originating from a stock imported to France in 1972 [Herrenschmidt, 1977; Thierry et al., 1994]. The males studied in groups A and B were born in these groups. The males studied in groups C, D, and E originated from groups A and B (Table I). Group A
Greetings in Tonkean Macaques / 991
TABLE I. Information About Groups and Subjects
Groups A B C D E
Origin of groups
Composition of groups
Division of original stock into groups A and B in 1972 Division of original stock into groups A and B in 1972 Founded in 2005 from individuals removed from group B Founded in 2007 from individuals removed from group A Founded in 2007 from individuals removed from group B
4 adult males, 3 adult females, 6 juveniles, 1 infanta 8 adult males, 11 adult females, 11 juveniles, 5 infants 3 adult males, 3 adult females, 4 juveniles 5 adult males, 5 adult females, 3 juveniles, 1 infant 4 adult males, 3 adult females, 2 juveniles, 2 infants
Name of focal males (age in years at the time of study) Mic (15), Gui (9), Gas (7), Meg (7) Nem (24), Bul (12), Vor (8), Vac (8), Bem (6), Vir (6), Mil (6), Jan (6) Nab (12), Pla (10), Pal (6) Gre (17), Ach (11), Cha (9), Don (8), Gra (5) Rim (9), Sho (8), Sim (8), Utt (6)b
a
Infants: under 1‐year old; juveniles: 1–4 years; adults: at least 5‐year old. Ages in 2011.
b
was housed in an enclosure 120 m2 and 4 m high at the Orangerie Zoo of Strasbourg, France. Group B lived in a wooded park of 2 acres, but at the time of this study it was maintained in an enclosure 40 m2 and 2.3 m high located within the same park at the Primatology Center of Strasbourg, France. The other three groups were kept in enclosures approximately 500 m2 and 5 m high at the Parco Faunistico di Piano dell’Abatino Rescue Centre in Rieti, Italy. Enclosures were furnished with wooden structures, perches, and ropes. Monkeys were fed with commercial monkey diet pellets, and fresh fruit and vegetables. Water was available ad libitum. We adhere to the American Society of Primatologists principles for the ethical treatment of primates, and research complied with national laws. Observational Methods Observations focused on males at least 5 years old outside the context of food distribution. They took place in the morning from 10.00 to 13.00 in July– September 1998 for group A, April–May 2000 for group B, May–September 2011 for groups C and D, and May–July 2012 for group E. Some mating periods occurred during the course of the study, but no observations were carried out during days when a male was in consort with an estrous female. Six different observers were involved in the study (A. De Marco, A. Sanna, S. Bernard, N. Coulange, C. Fullgrabe, E. Vero). As the different study groups were sampled at different periods of time, we could not measure the inter‐observer reliability between all observers. However, they recorded the same behavior units, and we verified from a sample of 69 observation hours that the two observers involved in the study of groups C, D and E achieved an inter‐ reliability score of 0.77 [kappa coefficient, Cohen, 1960]. In groups A, C, D, and E, we observed each male continuously for 3 hours, totaling 24 hours per individual. In group B, focal samples lasted 5 minutes per
hour, for a total of 260 minutes per focal individual, and an additional observation period of 39 hours was devoted to all‐occurrence sampling. We recorded supplantations (an individual approaches another who leaves immediately) and behaviors indicating anxiety (scratching, yawning) using focal sampling methods [Altmann, 1974]. We measured affinities between males using instantaneous sampling at 10‐min intervals to record spatial proximity (i.e.,
RESEARCH ARTICLE The Function of Greetings in Male Tonkean Macaques ARIANNA DE MARCO1,2,3*, ANDREA SANNA1, ROBERTO COZZOLINO1, AND BERNARD THIERRY4,5 1 Fondazione Ethoikos, Radicondoli, Italy 2 Parco Faunistico di Piano dell’Abatino, Poggio San Lorenzo, Italy 3 Istituto di Scienze e Tecnologie della Cognizione, Consiglio Nazionale delle Ricerche, Rome, Italy 4 Centre National de la Recherche Scientifique, Département Ecologie, Physiologie et Ethologie, Strasbourg, France 5 Université de Strasbourg, Institut Pluridisciplinaire Hubert Curien, Strasbourg, France
Males living in multi‐male groups are both strong rivals and potential allies. In several primate species they regularly interact through ritualized exchanges known as greetings. We studied five captive groups of Tonkean macaques (Macaca tonkeana) to test five hypotheses regarding the social function of greetings. We found that greetings were mostly reciprocal interactions, and that they often involved physical contact and facial displays. Although they were mostly initiated by the higher‐ranking individual in each dyad, subordinates could initiate approximately one‐third of greetings, which indicates that greetings do not serve as a formal acknowledgement of dominance relationships. Although greeting frequencies were negatively correlated to the frequency of supplantations and conflicts, they were not significantly influenced by age and dominance status, showing that greetings are not used to appease partners or decrease tension between males. Males most frequently greeted partners with whom they spent more time in proximity and body contact, and this is consistent with the hypothesis that greetings play a role in reinforcing social relationships. Lastly, greetings increased in frequency between individuals involved in challenges for rank, lending support to the hypothesis that males assess the state of their social relationships through greetings. Am. J. Primatol. 76:989–998, 2014. © 2014 Wiley Periodicals, Inc. Key words:
greeting; affiliation; dominance; ritualization; Macaca tonkeana
INTRODUCTION Group living is a quite demanding adaptive strategy because it creates an environment in which conspecifics have to compete and cooperate with the same partners. This is especially true for adult males residing in multi‐male social systems; although they are rivals regarding reproductive access, they are also potentially powerful allies for each other. Sexual selection has armed primate males with a competitive drive and dangerous canines [Plavcan, 2004; van Hooff, 2000], and the antagonistic character of their social relationships has been emphasized by observers, with male–male interactions described mostly as neutral or hostile, especially in monkey species displaying male dispersal [Caldecott, 1986; Smuts, 1987; Strier, 2000]. On the other hand, a fair number of non‐agonistic interactions do occur between males, and we have learned that resident males can negotiate cooperation, reconcile, and appease one another [Aureli & de Waal, 2000; van Hooff & van Schaik, 1994]. In several primate species, ritualized exchanges of communicative signals occur between males, and they are usually known as greetings. However, researchers have used a variety of labels to designate similar or different motivations and
© 2014 Wiley Periodicals, Inc.
adaptive functions for these interactions, and it is currently difficult to accurately delineate the range of behaviors and contexts included. In baboons (Papio spp.) a male typically greets another male by approaching him while producing affiliative facial expressions and gestures. Baboon greetings take place in several contexts and fulfill different functions that are not necessarily mutually exclusive. In some baboon species, they tend to occur more often between individuals that have good quality relationships with each other, meaning that they frequently interact using non‐agonistic behaviors [Whitham & Maestripieri, 2003]. Previous studies suggest that the risky behavior of exposing a vulnerable area such as the genitals during
Correspondance to: Arianna De Marco, Parco Faunistico di Piano dell’Abatino, via Capofarfa 50, 02030 Poggio san Lorenzo (Ri), Italy. E‐mail: [email protected] Received 1 September 2013; revised 7 March 2014; revision accepted 9 March 2014 DOI: 10.1002/ajp.22288 Published online 9 April 2014 in Wiley Online Library (wileyonlinelibrary.com).
990 / De Marco et al.
greetings makes this behavior a reliable interaction allowing males to test and/or reinforce social relationships [Colmenares, 1990, 1991; Fraser & Plowman, 2007; Smuts, 2002; Smuts & Watanabe, 1990; Whitham & Maestripieri, 2003]. It was also hypothesized that greetings reduce social tension and help resolve conflicts [Abegglen, 1984; Colmenares et al., 2000; Smuts & Watanabe, 1990]. In most baboons, greetings are generally initiated by the lower‐ranking individual in a dyad, so they may convey submission [Colmenares, 1990; Fraser & Plowman, 2007; Hausfater & Takacs, 1987; Smuts & Watanabe, 1990]. In Guinea baboons (Papio papio), however, there does not seem to be any link between greeting and dominance rank [Whitham & Maestripieri, 2003], and in hamadryas baboons (P. hamadryas), males use an additional form of greeting whereby one male approaches another, presents his hindquarters, and leaves to notify travel direction [Abegglen, 1984; Kummer, 1968]. Ritualized affiliative behaviors have also been described in macaques (Macaca spp.). In Barbary and Tibetan macaques (Macaca sylvanus and Macaca thibetana), males use infants in triadic interactions to approach each other and initiate affiliative interactions, which may strengthen their social relationships [Deag, 1980; Henkel et al., 2011; Ogawa, 1995; Paul et al., 1996]. Similar behaviors have also been reported in bonnet macaques (Macaca radiata) [Silk & Samuels, 1984]. It is worth adding that in these three species, males can also contact each other at the dyadic level using embraces, mounts or genital grips [Ogawa, 1995; Preuschoft, 1995; Silk, 1994; Sugiyama, 1971]. In long‐tailed macaques (Macaca fascicularis), males occasionally grasp another individual’s hindquarters, and they may grasp each other face to face [Thierry, 1985]. Lastly, penis grabbing and mounting have been reported as greetings in crested macaques (Macaca nigra), one of the seven species originating from the Sulawesi island [Reed et al., 1997]. Since greeting interactions are generally observed outside the context of aggression in macaques, they should not have an appeasement function, but rather serve to regulate social relationships between males. However, except for triadic interactions in Barbary macaques, the function of greetings has not been systematically examined in macaques to date. Our study addresses greetings between males in a species from Sulawesi, the Tonkean macaque (Macaca tonkeana). This species is characterized by relaxed dominance relationships and a high level of social tolerance compared to other macaques [Thierry, 2007, 2010]. Affiliative contacts and appeasement signals are especially frequent between Tonkean macaques [De Marco et al., 2011; Demaria & Thierry, 2001; Thierry, 1984]. They also show a high propensity to prevent the escalation of conflicts; third parties can stop aggression by addressing appeasement
Am. J. Primatol.
signals to adversaries [Petit & Thierry, 1994], while group‐mates uninvolved in a conflict are more likely to affiliate with one another after witnessing such appeasement [De Marco et al., 2010]. We took the main five hypotheses that emerge from previous studies regarding the function of greetings, and tested them in Tonkean macaques. They are not necessarily mutually exclusive, and we can formulate them as follows: 1. Social relationship reinforcement hypothesis [Fraser & Plowman, 2007; Smuts & Watanabe, 1990]: if greetings are used to reinforce social relationships, individuals should primarily greet their preferred partners, that is, individuals they are frequently seen to be close to. 2. Appeasement hypothesis [Hausfater & Takacs, 1987; Kummer et al., 1974]: if greetings are used to stop conflicts, they should occur immediately after aggression, and in each dyad the lower‐ ranking partner should initiate them more often that the higher‐ranking one. 3. Formal dominance hypothesis [Fraser & Plowman, 2007; Hausfater & Takacs, 1987; Whitham & Maestripieri, 2003]: if greetings are an acknowledgement of dominance relationships between males, they should be strictly unidirectional within each dyad. 4. Social relationship testing hypothesis [Colmenares, 1990; Smuts & Watanabe, 1990; Whitham & Maestripieri, 2003]: if greetings are used by males to test the state of their social relationships, they should greet the partners with whom their social relationships are least secure more often, that is, those with whom they have more frequent agonistic interactions, or with whom dominance relationships are unstable; patterns of greetings should also be dependent on the direction of dominance relationships. 5. Tension reduction hypothesis [Abegglen, 1984; Colmenares, 1990; Hausfater & Takacs, 1987; Smuts & Watanabe, 1990]: if greetings are used to decrease tension between partners, their frequencies should vary consistently with individual dominance status, rates of agonistic interactions and signs of anxiety, and they should increase in periods of social disturbance.
METHODS Subjects We studied five captive groups of Tonkean macaques (Table I), which belong to a population originating from a stock imported to France in 1972 [Herrenschmidt, 1977; Thierry et al., 1994]. The males studied in groups A and B were born in these groups. The males studied in groups C, D, and E originated from groups A and B (Table I). Group A
Greetings in Tonkean Macaques / 991
TABLE I. Information About Groups and Subjects
Groups A B C D E
Origin of groups
Composition of groups
Division of original stock into groups A and B in 1972 Division of original stock into groups A and B in 1972 Founded in 2005 from individuals removed from group B Founded in 2007 from individuals removed from group A Founded in 2007 from individuals removed from group B
4 adult males, 3 adult females, 6 juveniles, 1 infanta 8 adult males, 11 adult females, 11 juveniles, 5 infants 3 adult males, 3 adult females, 4 juveniles 5 adult males, 5 adult females, 3 juveniles, 1 infant 4 adult males, 3 adult females, 2 juveniles, 2 infants
Name of focal males (age in years at the time of study) Mic (15), Gui (9), Gas (7), Meg (7) Nem (24), Bul (12), Vor (8), Vac (8), Bem (6), Vir (6), Mil (6), Jan (6) Nab (12), Pla (10), Pal (6) Gre (17), Ach (11), Cha (9), Don (8), Gra (5) Rim (9), Sho (8), Sim (8), Utt (6)b
a
Infants: under 1‐year old; juveniles: 1–4 years; adults: at least 5‐year old. Ages in 2011.
b
was housed in an enclosure 120 m2 and 4 m high at the Orangerie Zoo of Strasbourg, France. Group B lived in a wooded park of 2 acres, but at the time of this study it was maintained in an enclosure 40 m2 and 2.3 m high located within the same park at the Primatology Center of Strasbourg, France. The other three groups were kept in enclosures approximately 500 m2 and 5 m high at the Parco Faunistico di Piano dell’Abatino Rescue Centre in Rieti, Italy. Enclosures were furnished with wooden structures, perches, and ropes. Monkeys were fed with commercial monkey diet pellets, and fresh fruit and vegetables. Water was available ad libitum. We adhere to the American Society of Primatologists principles for the ethical treatment of primates, and research complied with national laws. Observational Methods Observations focused on males at least 5 years old outside the context of food distribution. They took place in the morning from 10.00 to 13.00 in July– September 1998 for group A, April–May 2000 for group B, May–September 2011 for groups C and D, and May–July 2012 for group E. Some mating periods occurred during the course of the study, but no observations were carried out during days when a male was in consort with an estrous female. Six different observers were involved in the study (A. De Marco, A. Sanna, S. Bernard, N. Coulange, C. Fullgrabe, E. Vero). As the different study groups were sampled at different periods of time, we could not measure the inter‐observer reliability between all observers. However, they recorded the same behavior units, and we verified from a sample of 69 observation hours that the two observers involved in the study of groups C, D and E achieved an inter‐ reliability score of 0.77 [kappa coefficient, Cohen, 1960]. In groups A, C, D, and E, we observed each male continuously for 3 hours, totaling 24 hours per individual. In group B, focal samples lasted 5 minutes per
hour, for a total of 260 minutes per focal individual, and an additional observation period of 39 hours was devoted to all‐occurrence sampling. We recorded supplantations (an individual approaches another who leaves immediately) and behaviors indicating anxiety (scratching, yawning) using focal sampling methods [Altmann, 1974]. We measured affinities between males using instantaneous sampling at 10‐min intervals to record spatial proximity (i.e.,
