American Journal of Primatology 77:222–228 (2015)

RESEARCH ARTICLE Exchanging Grooming, But not Tolerance and Aggression in Common Marmosets (Callithrix jacchus) MARCO CAMPENNÌ1,2, ARIANNA MANCIOCCO1,3, AUGUSTO VITALE1, AND GABRIELE SCHINO3* 1 Reparto di Neuroscienze Comportamentali, Dipartimento di Biologia Cellulare e Neuroscienze, Istituto Superiore di Sanità, Rome, Italy 2 Stockholm Resilience Centre, Stockholms Universitet, Stockholm, Sweden 3 Istituto di Scienze e Tecnologie della Cognizione, C.N.R., Rome, Italy

In this study, we investigated the reciprocal exchanges of grooming, tolerance and reduced aggression in common marmosets (Callithrix jacchus), a cooperatively breeding primate whose groups are typically characterized by uniformly high genetic relatedness and high interdependency between group members. Both partner control and partner choice processes played a role in the reciprocal exchanges of grooming. In contrast, we did not find any evidence of reciprocity between grooming and tolerance over a preferred food source or between grooming and reduced aggression. Thus, reciprocity seems to play a variable role in the exchange of cooperative behaviors in marmosets. Am. J. Primatol. 77:222–228, 2015. © 2014 Wiley Periodicals, Inc. Key words:

grooming; tolerance; aggression; reciprocity; cooperative breeding; Callithrix jaccus

INTRODUCTION Cooperative behaviors are a common feature of animal societies, and reciprocity is one of the possible mechanisms supporting their evolution [West et al., 2007]. Among primates, a vast literature supports a role for reciprocity in explaining the exchange of cooperative interactions [Cheney, 2011; Schino & Aureli, 2009; see Clutton‐Brock, 2009 for a different view]. Although reciprocity is extensively investigated, two aspects of the reciprocal exchange of cooperative behaviors still need to be clarified: the relations between two different decision‐making processes that can underlie reciprocation, and the relations between kinship and reciprocity. Bull and Rice [1991] were probably the first to note that reciprocal exchanges of benefits can be based on two different processes, partner fidelity [later called partner control by Noë, 2006] and partner choice. Partner control models conceive dyads of individuals as conceptually isolated, and test reciprocity on the basis of short‐term temporal relations between cooperative events [this correspond to classical reciprocal altruism; Axelrod & Hamilton, 1981; Trivers, 1971]. Partner choice models, in contrast, emphasize that decision‐ making can be based on a comparison of the benefits to be obtained from the different partners and can be tested by assessing how animals distribute their cooperative behavior among group mates in relation to the amount of cooperation received [Campennì & Schino, 2014; Noë, 2001]. The debate about the role of reciprocity in the evolution of cooperation has been

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affected negatively by a failure to distinguish between these different processes [e.g. Schino, 2007]. In fact, evidence that animals direct their cooperative behavior preferentially to those individuals that cooperate most (i.e. partner choice) is abundant [reviewed in Schino & Aureli, 2009] while demonstrating that recent cooperation received increases cooperativeness (i.e. partner control) has proved more difficult [reviewed in Tiddi et al., 2011]. Thus, conflating the two processes was a cause of confusion. A few recent studies, however, have tried to separate the effects of the two different processes and have measured their independent effects in the same species and setting, often concluding that partner choice seems to be the prevalent process [e.g. Fruteau et al., 2011; Schino et al., 2009; Tiddi et al., 2011]. While reciprocity has always been controversial, the role of kinship in promoting the evolution of cooperation has rarely been questioned [see Nowak et al., 2010, for an exception]. How these two evolutionary processes can interact during the



Correspondence to: G. Schino, Istituto di Scienze e Tecnologie della Cognizione, C.N.R., Via Ulisse Aldrovandi 16b, Rome 00197, Italy. E‐mail: [email protected] Received 25 March 2014; revised 17 July 2014; revision accepted 30 July 2014 DOI: 10.1002/ajp.22324 Published online 17 September 2014 in Wiley Online Library (wileyonlinelibrary.com).

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evolution of cooperation is however unclear. In fact, an unspoken assumption of studies of cooperation has often been that, if cooperation occurs between relatives, then it is to be explained entirely by kin selection [Chapais, 2001; Chapais & Berman, 2004]. Recently, however, Schino and Aureli [2010] have shown that, when the relative roles of kinship and reciprocity are assessed simultaneously, the latter seems to play a larger role in explaining the distribution of cooperative behaviors among group members. Also, it is not entirely clear how animals make their choices among group members that are equally related, and in particular what is the role of reciprocity in those animal societies in which members of a group are typically all closely related. Cornwallis et al. [2009] have shown that in cooperatively breeding vertebrates kin discrimination (the differential allocation of helping to more closely related individuals) is lower when kinship is uniformly high. Under these conditions indiscriminate helping seems to be favored. In cooperative breeders, indiscriminate helping may also be due to the high interdependency between the group members. In fact, cooperative breeding has been proposed to favor the evolution of prosocially motivated nearly indiscriminate helping [Burkart et al., 2007]. Common marmosets (Callithrix jacchus) are cooperative breeders that live in extended family groups where all individuals are often closely related and where the successful raising of offspring requires the contribution of all group members [Digby et al., 2007]. Under these conditions two contrasting hypotheses can be formulated about the role of reciprocity in regulating the exchange of cooperative behaviors. First, it is possible that, given the uniformly high genetic relatedness and high interdependency, marmosets are indiscriminate in their social choices and distribute their cooperative behaviors uniformly among group mates. Second, it is possible that, given the impossibility to discriminate according to differential relatedness, reciprocity plays a more relevant role in guiding social choices. In this study we aimed at assessing reciprocal exchanges of grooming, tolerance and (reduced) aggression in marmosets. We took particular care in trying to evaluate both partner control and partner choice processes.

METHODS Subjects and Housing Subjects of this study were the members of two captive groups of common marmosets housed at the Section of Behavioural Neuroscience of the Istituto Superiore di Sanità in Rome, Italy. The two groups were formed by seven and four individuals, respectively. The larger group included two mature males, three mature females, and two juvenile females; the smaller group included two mature males and two

mature females. The original pairs had been formed 3–4 years before data collection, and no animal had been added to the groups thereafter except by birth. One of our groups included a reproductive pair of unrelated adults and their offspring. In the other, the father of the offspring had died and its position as dominant male had been taken by one of his sons. Summarizing, all of the dyads in our study groups had a coefficient of relatedness r ¼ 0.5, except for a single dyad (the reproductive adults of one of the groups). Kinship was therefore uniformly high. We relied on David’s scores to arrange monkeys in a linear dominance hierarchy based on the direction of agonistic interactions [de Vries et al., 2006]. Each group lived in a 220  150  80 cm indoor cage enriched with ropes, branches, and nest boxes. The entire colony (5 family‐groups at the time of observations) is housed in a room in which animals are in constant olfactory and auditory contact with each other, while visual contact is partially prevented by curtains and partitions between cages. Temperature is kept at 21  1°C, with a relative humidity of about 50%. A light/dark cycle of 12 hr (including UV‐ B lights) is maintained. Each home cage is connected through a tunnel to two interconnected experimental cages (each sized similarly to the home cages) situated in an adjacent room. Observations were conducted while the animals were in one of these experimental cages. They are visited daily by the different groups independently of experimental sessions and are therefore familiar to all marmosets. The experimental cages included two suspended platforms (20  30 cm), each equipped with a round bowl (diameter 10 cm) in which a preferred food was provided midway through the daily observation session (see below for details). Procedure Data were collected by M.C. between May and August 2011. Observations were conducted daily on both groups alternating the order of observation. A total of 81 hr of observation was made. Each observation session consisted of three consecutive phases: a pre‐feeding phase (40 min), a feeding phase, and a post‐feeding phase (40 min). The feeding phase began with the provision of a preferred and shareable food (strawberry yoghurt) and ended when feeding finished. Food was put in two bowls located on the two platforms described above. On average, feeding phases lasted 3.7 min. During the pre‐feeding and post‐feeding phases the observer recorded the timing and the identities of the individuals involved in all occurrences of grooming and aggression (ear‐tuft retraction, ehr‐ehr vocalizations, chases, and physical assaults). For an ethogram see Stevenson and Poole [1976] and available online at: www.marmosetcare.com. During the feeding phase the observer also recorded (using

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the instantaneous sampling method with a sampling interval of 15 s) the identity of any individual present on the two feeding platforms. The simultaneous presence on a platform during the feeding phase was used as a measure of tolerance [see Tiddi et al., 2011]. Data Analysis

Calculation of dyadic scores Dyadic scores of grooming were the total time each monkey spent grooming each other monkey, divided by total observation time. Similarly, dyadic scores of aggression were the number of times each monkey was aggressive to each other monkey, divided by total observation time. Calculation of dyadic scores for tolerance during feeding required a different procedure in order to control for the differences in the occasions for being tolerant. First, we obtained the total number of sampling intervals in which each monkey had been recorded as being on the same feeding platform with any other lower‐ranking monkey. Then, for each monkey, we divided its raw dyadic scores by the total number of sampling intervals in which it was present on the platforms, so as to control for variation in the presence on the platforms. Temporal relations between events A survival analysis [Cleves et al., 2008] was used to obtain an estimate of the rate (“hazard”, in survival analysis jargon) at which marmosets reciprocated grooming in relation to the time elapsed from the end of the received grooming. This estimate of grooming rate (and its 95% confidence intervals) was compared to the baseline rate of grooming in order to determine the time window following the receipt of grooming during which the rate of reciprocation was significantly higher than the baseline rate of grooming. In this way, we both tested for an effect of the receipt of grooming on the probability of immediate reciprocation and identified “immediately reciprocated” grooming episodes (i.e. those episodes that occurred during the above determined time window). The baseline was calculated by averaging grooming rates of all dyads in the group; each dyadic datum was weighed according to the dyad’s contribution to the sample of grooming episodes used in the survival analysis. This weighing procedure was necessary to insure that the baseline used was comparable to the data included into the survival analysis. Analyses of temporal relations between grooming and tolerance or aggression tested: (i) whether grooming given prior to the feeding phase increased tolerance or reduced aggression received during the subsequent feeding phase; (ii) whether tolerance or aggression received during the feeding phase increased or decreased (respectively) grooming given after the feeding phase. Temporal relations between grooming and tolerance or aggression were tested

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using within‐dyad regressions, that is, regressions in which the identities of both the actor and the receiver were entered as fixed effect independent variables into the analysis. Linear (with robust standard error) or Poisson (with bootstrap standard error) regressions were used depending on the type of dependent variable (proportion of time spent together on the platform or count of episodes of grooming or aggression, respectively). The relevant independent variable was the presence of grooming, aggression, or tolerance in the previous observation phase.

Partner choice based on benefits received Tests of whether marmosets directed more of their grooming or tolerance or less of their aggression preferentially to those individuals that groomed or tolerated them more or aggressed them less (and vice versa) were based on within‐subject linear regressions with robust standard errors. As the analysis of temporal relations between grooming events showed that grooming received caused a short‐term increase in grooming given (see the results), the within‐subject regression was also repeated excluding all cases of immediate reciprocation (identified as explained above). In this way, partner choice was evaluated excluding any effect of partner control. Dyadic scores for tolerance and aggression were calculated only for dominant‐subordinate dyads, as subordinates cannot grant tolerance to dominants and are also severely constrained in their aggression. Thus, within‐subject regressions testing the exchanges of grooming for tolerance and reduced aggression included only half of the dyads. All analyses were run using Stata 11.2 [StataCorp, 2009]. All probabilities are two‐tailed. Statement of Research Ethics The research described in this paper complied with protocols approved by the Italian Ministry of Health (permit number DM 275/12–C, 26.11.2012) and with the legal requirements of Italy. It adhered to the American Society of Primatologists (ASP) principles for the ethical treatment of nonhuman primates. RESULTS Frequency of Cooperative and Aggressive Behaviors A total of 646 episodes of grooming (totaling 395 min of grooming) were observed. Marmosets groomed their average group mate for 12  2 s per hour of observation (mean  standard error based on 54 dyadic data points). During the feeding phase of observations, marmosets were recorded sharing the feeding platforms with a group mate 1070 times. Dominant marmosets tolerated the close presence of subordinates on the

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feeding platforms for 13  2% of the time they spent on the platforms (mean  standard error based on 26 dyadic data points). During the feeding phase, a total of 186 aggressions were observed. Dominant marmosets were aggressive to their average subordinate group mate 4.03  1.2 times per hour of observation (mean  standard error based on 26 dyadic data points). Outside of the feeding phase aggression rates were much lower (0.025  0.007 episodes/hour). Temporal Relations Between Events Receiving grooming increased the probability of returning grooming. Figure 1 shows the time course of the probability of returning grooming in relation to the time elapsed after the end of the received grooming. It shows that the probability of returning grooming was higher than the baseline probability of grooming for about two minutes (126 s) after the end of the received grooming. Thus, receiving grooming did increase the returning of grooming, although the effect was rather short‐lived. In contrast, no temporal relations between grooming and tolerance were evident. Receiving grooming prior to the feeding phase did not increase tolerance towards the former groomer during subsequent feeding (coeff. ¼ .0.055, df ¼ 9, t ¼ .1.41, P ¼ 0.192, and N ¼ 510). Similarly, being tolerated on the feeding platforms during the feeding phase did not increase subsequent grooming (coeff. ¼ .0.282, z ¼ .0.94, P ¼ 0.346, and N ¼ 522). Also, no temporal relations between grooming and reduced aggression were evident. Receiving grooming prior to the feeding phase did not decrease aggression directed to the former groomer during subsequent feeding (coeff. ¼ .0.049, z ¼ .0.17, P ¼

Fig. 1. Rate of grooming reciprocation (hazard) in relation to the time elapsed from the end of the received grooming. The figure shows the smoothed hazard estimate, its 95% confidence intervals, and the baseline rate of grooming. See the Methods for details of the analyses.

TABLE I. Grooming Given in Relation to Grooming Received and Other Control Variables Independent variable

Coefficient

t‐value

All grooming Grooming received 0.351 5.52 Rank of recipient 0.238 0.08 Age of recipient 0.113 0.44 Sex of recipient 0.934 4.04 Intercept 3.533 4.28 Excluding immediately reciprocated grooming Grooming received 0.284 4.85 Rank of recipient 0.240 3.18 Age of recipient 0.156 0.65 Sex of recipient 1.017 5.20 Intercept 3.788 4.87

P‐value

Exchanging grooming, but not tolerance and aggression in common marmosets (Callithrix jacchus).

In this study, we investigated the reciprocal exchanges of grooming, tolerance and reduced aggression in common marmosets (Callithrix jacchus), a coop...
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