Available online 19 April 2011. MS. number: 10-00471R .... (Altmann 1974) to collect data on grooming sessions occurring
Animal Behaviour 81 (2011) 1223e1230
Contents lists available at ScienceDirect
Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav
When females trade grooming for grooming: testing partner control and partner choice models of cooperation in two primate species Cécile Fruteau a, *, Sylvain Lemoine b,1, Eléonore Hellard c, 2, Eric van Damme a, Ronald Noë d, 3 a
CentER, Tilburg University CERCOPAN (Centre for Education, Research and Conservation of Primates and Nature) c Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, CNRS, Université Lyon1 d Ethologie Evolutive, DEPE, IPHR, UMR 7178, CNRS-UdS b
a r t i c l e i n f o Article history: Received 6 July 2010 Initial acceptance 11 August 2010 Final acceptance 2 March 2011 Available online 19 April 2011 MS. number: 10-00471R Keywords: biological market Cercocebus atys Chlorocebus aethiops grooming hierarchy parcelling raising the stakes time matching
We tested predictions following from the biological market paradigm using reciprocated grooming sessions among the adult females in a sooty mangabey, Cercocebus atys, group with 35 females (Ivory Coast) and in two groups of vervet monkeys, Chlorocebus aethiops (South Africa) with four and seven females, respectively. Closely ranked females often groomed frequently. The exchanges within such dyads were generally characterized by time matching, but the subordinates groomed for longer than their dominant partners. The reciprocal nature of over 90% of the grooming sessions allowed us to investigate ‘partner control’ strategies such as ‘parcelling’ and ‘raising the stakes’. Females of both species neither parcelled nor gradually invested more grooming in the course of sessions. Rather, the longer bouts of a grooming session were usually at the beginning of the session and the length of the first bout reliably predicted the length of the whole session for frequently grooming partners. Furthermore, we compared potential trust-building behaviour (or ‘strategies’) in frequent and infrequent grooming partners. We found that infrequent groomers of both species showed no signs of trust building and that the first bout they invested in a grooming session did not predict the session length. We conclude that each female has a good knowledge of her value as a grooming partner within each dyad and knows how much she has to invest to receive a satisfactory amount of grooming within the same session. Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
In biology, behaviours are called ‘altruistic’ if they result in a momentary decrease in fitness of the actor and increase in fitness of the recipient. Altruism has long been considered as paradoxical in evolutionary terms until Hamilton (1964) and Trivers (1971) proposed explanations for their occurrence in related (kin selection theory) and unrelated (reciprocal altruism theory) individuals, respectively. The iterated Prisoners’ Dilemma (IPD) has been the game-theoretical paradigm of choice for reciprocal altruism (RA) in spite of some crucial differences between the two concepts (Noë 1990). The essence is the same, however: both RA- and IPD-based models predict contingent strategies with relatively short memories, that is, the animals are expected to base their choice of action * Correspondence: C. Fruteau, CentER, Tilburg University, PO Box 90153, 5000 LE Tilburg, The Netherlands. E-mail address:
[email protected] (C. Fruteau). 1 S. Lemoine is at CERCOPAN, 4 Ishie Lane, HEPO Box 826, Calabar, Cross River State, Nigeria. 2 E. Hellard is at the Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, CNRS, Université Lyon1, 43 Bd du 11 Novembre 1918, 69622 Villeurbanne cedex, France. 3 R. Noë is at Ethologie Evolutive, DEPE, IPHC, UMR 7178, CNRS-UdS, 23 rue Becquerel, 67087 Strasbourg cedex 2, France.
on the behaviour shown by their partner during their last few interactions. It has proved difficult to demonstrate such contingent strategies in nature, however (e.g. Roberts 1998; Hammerstein 2003; Bshary & Bronstein 2004; Sachs et al. 2004; Bergmüller et al. 2007; Silk 2007; West et al. 2007a, b; but see Bshary et al. 2008 for a rare exception), while the results of experiments with captive primates have been mixed (e.g. Melis et al. 2008; Brosnan et al. 2009; Dufour et al. 2009). With the introduction of biological market theory (Noë & Hammerstein 1994, 1995) the emphasis switched from partner control to partner choice. According to this theory, the exchange rate of goods and services (‘commodities’), traded between partners to their mutual benefit, is determined by the law of supply and demand. The driving force is partner choice, which induces outbidding competition among the group of individuals from which the partner(s) are chosen. While many studies of mutualistic systems (reviewed in Bshary & Noë 2003; Sachs et al. 2004; Leimar & Hammerstein 2010) and intraspecific cooperation (reviewed in Kutsukake & Clutton-Brock 2008, 2010) have shown the importance of the biological market theory in predicting how cooperation operates, there is still some disagreement among primatologists (reviewed in Barrett & Henzi 2006; Schino & Aureli 2010).
0003-3472/$38.00 Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2011.03.008
1224
C. Fruteau et al. / Animal Behaviour 81 (2011) 1223e1230
In primates, allogrooming (grooming, hereafter) has long been considered as an indicator of the long-term bonds between individuals (Hinde 1976; Schino et al. 2007; Dunbar 2010). More recently and in the framework of biological market theory, grooming has been considered as a low-cost currency in the sense that it can be used to compensate for imbalances in the trading of other commodities (Barrett et al. 1999, 2000). Hence, grooming is either reciprocated in kind by the partner (Barrett et al. 1999, 2000; Manson et al. 2004) or exchanged for another commodity, such as tolerance at food sources (Barrett et al. 1999, 2002), agonistic support (Hemelrijk & Ek 1991; Schino 2007), food (de Waal 1997), access to newborns (Henzi & Barrett 2002; Gumert 2007a; Fruteau et al. 2011) and mate compliance (Gumert 2007b). We investigated grooming sessions (hereafter called neutral sessions) during which grooming was not obviously and immediately exchanged for commodities such as food, infant and mate access in two free-ranging primate species, sooty mangabeys, Cercocebus atys, and vervet monkeys, Chlorocebus aethiops. While both species are mainly terrestrial and seasonal breeders they show substantial differences. Mangabeys range in the rainforest and form large groups. Females display exaggerated sexual swellings during their sexual cycles and few conflicts characterize their relationships outside the mating season. In contrast, vervets form small units of about 10 individuals and range in open areas such as savannah. Females have concealed ovulations and conflicts are frequent between group members. We defined a grooming session as a sequence of bouts exchanged between two partners. We used biological market theory (Noë & Hammerstein 1994, 1995) to predict how grooming bouts would be traded among females. We first checked whether supply/demand ratios or power asymmetries between partners influenced grooming bout lengths. The original function of grooming was undoubtedly the removal of ectoparasites and treatment of the fur (Hutchins & Barash 1976; Zamma 2002), but primates groom much more than seems necessary for these basic functions (e.g. Dunbar 2010). We therefore conjecture that the mechanisms that originally ensured that the animals liked to be groomed (e.g. the release of beta-endorphin, Keverne et al. 1989) became themselves rewarding in the course of evolution. Whatever the precise present-day function, we can safely assume that grooming has diminishing returns: ectoparasites are at some point removed and hormone titres at some point reach their maximum. In other words, in long grooming bouts the first minute of a bout is worth more than the last minute. However, we assume that grooming bouts of equal length given by a certain donor would be of equivalent value to a specific receiver. Power asymmetries such as rank distance between females should influence the grooming lengths, because dominants have additional commodities, such as tolerance at food patches, restraint in dyadic conflicts with the subordinate and agonistic support in conflicts, to trade that subordinates cannot offer. We therefore predicted that the subordinate of a dyad would generally groom more than the dominant, but that females of neighbouring rank would time-match their investments in term of grooming duration more than those of distant rank (Henzi et al. 2003). We expected to find a strong effect of the number of potential grooming partners for females. We therefore thought that this effect would be stronger in mangabeys than in vervets because of their larger groups. Biological market theory is not an alternative to partner control models and therefore does not exclude the use of ‘partner control’ strategies once cooperating dyads have formed. One partner control mechanism that would apply to grooming is parcelling (Connor 1995). Connor (1995) assumed that cooperating individuals are initially caught in an iterated Prisoner’s Dilemma. By delivering their goods and services in small packages they de facto change the payoff
matrix of each round of the game in such a way, however, that it is no longer a Prisoner’s Dilemma, and thus they reduce the risk of exploitation. The model applies especially well to grooming, since this service can be delivered in packages of almost any size. The model would thus predict that grooming bouts remain short within grooming sessions. We cannot predict, however, how short a bout should be to fulfil the requirements of the payoff matrix. We therefore simply predicted that grooming partners should take turns within grooming sessions and that the grooming bouts should be roughly equal in length within and between partners. Roberts & Sherratt (1998) developed the parcelling model further and proposed the ‘raising-the-stakes’ (RTS) strategy according to which animals can limit the risk of being exploited by starting with delivering small packages, but then increasing the portion delivered in each round, as long as the partner continues matching the investment. The dyadic structure of grooming sessions makes them likely interactions in which RTS could be used (Keller & Reeve 1998). RTS applies notably to the start of new cooperative relationships, but would also apply if the trust in partners goes back to (almost) zero between interactions during a series of repeated interactions. Barrett et al. (2000), after attempting to compare investments between grooming sessions chronologically dispersed over time in baboons, Papio ursinus, concluded that one has little chance of recording the real starting point of a relationship. We looked, therefore, for the use of RTS within grooming sessions but not between sessions. If RTS is used, we expected that partners would invest little at the beginning of the session and would gradually increase their investment if their partner at least matched the last bout of grooming given, but only in dyads in which trust needed to be built up during each grooming session. We therefore made a distinction between dyads grooming frequently and those grooming infrequently, assuming that trust building would still be necessary only in the grooming sessions of the latter. We predicted that frequent grooming partners would groom for longer at the start of the session than infrequent groomers. Finally, the first bout of a session may have the quality of a first bid and reflect the willingness of the individual to invest in this particular grooming session. Thus, we predicted that the first grooming bout within a session should reliably predict the total length of the session as long as grooming is not interrupted by external events. METHODS Research Areas, Subjects and Data Collection Sooty mangabeys We conducted the study in the Taï National Park, Ivory Coast between 1 November 2001 and 20 August 2002. The park is one of the last remaining blocks of West African primary forest and covers about 454 000 ha. The forest is classified as ‘tropical moist forest’ (Whitmore 1990), with a mean annual rainfall of 1875 mm, a mean annual temperature of 24 C (Taï Monkey Project data, 1991e1999) and a distinct dry season from December to March. Our group of mangabeys was well habituated to human observers before the study and we recognized all adult, subadult and infant members by facial features. Its home range covered about 7 km2 near the western border of the park. The group was not provisioned. During the study we observed 7e14 adult males, 35 adult females and about 70 juveniles and subadults. Seven infants were born between 10 December 2001 and 10 March 2002. One died on 2 February 2002. We focused the data collection on adult females. We used unidirectional ‘approach/retreat’ and ‘threat/retreat’ interactions to determine the female dominance hierarchy. It remained stable throughout the study period (linearity of the female rank order:
C. Fruteau et al. / Animal Behaviour 81 (2011) 1223e1230
MatMan test: c241 ¼ 447:89, P < 0.0001, h ¼ 0.97, K ¼ 0.97). We used both ad libitum and focal sampling observation techniques (Altmann 1974) to collect data on grooming sessions occurring between all females. Grooming bouts were timed to the nearest 30 s. A bout was considered to have ended when either the direction of grooming changed or when there was a break of more than 30 s. We used 15 min focal sampling with at least 60 min between consecutive samples of the same individual and 3 min between samples of different individuals. However, for the analyses we also used the focal samples that were at least 9 min long (89 of 2272 samples) if they were truncated because the subject moved out of the observer’s sight. For each focal animal, we recorded each minute (instantaneous sampling, Altmann 1974) the presence/ absence of the female’s infant, the distance from its mother and the nearest adult female and adult male within 5 m. Social interactions were recorded continuously (detailed ethogram in Range & Noë 2002). Owing to limited visibility in the early evening, we opted for a sampling schedule from 0700 to 1600 hours. We collected a total of 568 h of focal samples for all of the 35 adult females (range 63e65 per female). All females were followed at least once every 3 days and we randomized each female’s sampling to account for the time of day. Ad libitum data were recorded all day long (even while doing focal sampling on a subject) as soon as a social interaction (aggression, grooming, mount, etc.) between two identified individuals was observed. Vervet monkeys We conducted the study in the Loskop Dam Nature Reserve, Mpumalanga province, South Africa. The Loskop reserve is characterized by a ‘bushveld’ (tall grasses, thick acacia bushes) type of habitat. The reserve covers approximately 25 000 ha, on average 1000 m above sea level. The area has dry and cold winters (temperatures below 5 C at night and 25 C during the day) from May to October and hot and humid summers (rainfalls of about 500 mm; temperatures 25e40 C) from November to April. Both study groups had home ranges of approximately 3 km2 each that were about 3 km apart. The home range of the Donga group followed narrow dry riverbeds and mainly contained tall trees, such as fig trees, while the home range of the Picnic group was situated in a plain essentially composed of tall grasses and acacia bushes. Two artificial lakes, the Loskop Dam and the Picnic Dam, respectively, provided water to the Donga and Picnic groups the whole year round. The Donga group did not have contact with tourists and was not provisioned outside the context of experiments (see Fruteau et al. 2009). The Picnic group was provisioned by tourists, almost exclusively on Sundays, and regularly ate from the dustbins of the picnic site. The group also obtained food rewards during experiments (see Fruteau et al. 2009). The Donga group was habituated to the presence of human observers at the beginning of the study (from May to mid-October 2004) and the Picnic group was habituated before the second field session (from February to July 2005). The Donga group had three to five adult males, seven adult females, one to two subadult males and one to two infants at a time. The female dominance hierarchy changed between the first and the second field period after the death of the beta female (linearity of the female rank order: MatMan test: first period: c223 ¼ 48, P ¼ 0.002, h ¼ 1, K ¼ 1; second and third periods: c220 ¼ 60:67, P < 0.0001, h ¼ 1, K ¼ 1). The Picnic group had two to three adult males, four adult females, one juvenile male and two to six infants at a time. The female hierarchy remained stable throughout the two field periods (linearity of the female rank order: MatMan test: c2undef ¼ undefined, P ¼ 0.373, h ¼ 1, K ¼ 1). The genetic relatedness between most members of the groups was known as a result of work done during a follow-up study (J. Hula, R. Pansini, R. Noë & M. Kruetzen, unpublished data), in which material for the genetic analysis was
1225
extracted from faecal samples of each individual. Kin coefficients were calculated based on 13 loci (D10S1483, D1S518, D11S928, D1S207, D3S3591, D1S244, D8S1106, D5S1466, D7S2446, D11S1902, D18S42, D15S108, D2S144) and using the pairwise relationship coefficients from Queller & Goodnight (1989) and the pairwise relationship coefficient r from Wang (2002), which gave similar results. Two individuals were considered unrelated when their coefficient of similarity was
