Functional Implications of Allogrooming in Cercocebus torquatus

International Journal of Primatology, Vol. 21, No. 2, 2000

Functional Implications of Allogrooming inCercocebus torquatus

Ana Perez1 and Joaquim J. Vea1

Received May 13, 1998; revision October 8, 1999; accepted November 2, 1999

We examined the hygienic functional hypothesis of allogrooming in twocaptive groups (N � 9 and N � 8) of white-crowned mangabeys (Cercocebustorquatus lunulatus) by analyzing the corporeal distribution of allogroomingsolicitations according to the variable degree of accessibility of the variousbody sites. We used focal-animal sampling and continuous recording andnonparametric statistics (sing test and � 2). The fact that in both groups moreallogrooming was solicited to sites associated with accessibility problems isconsistent with the hygienic functional hypothesis of allogrooming. In anycase, there are two facts that suggest that this hypothesis cannot account forall the characteristics of such behavior: 1) the strong distributional selectivityshown by allogrooming solicitations—they concentrated primarily on dorsaland caudal regions instead of those difficult to reach or inaccessible on thewhole—and 2) the significant role played by sex in the intragroup distributionof anogenital solicitations. Supporting the multifunctional nature of allo-grooming, we find very appealing the ritualization hypothesis, according towhich the allogrooming performed on certain body sites would have acquireda sociocommunicative meaning.

KEY WORDS: allogrooming; primates; function; hygiene; Cercocebus.

INTRODUCTION

Grooming behavior embraces all types of care and attention of thebody surface—fur, skin or feathers—performed by the individual itself—

1Departamento de Psiquiatrıa y Psicobiologıa Clınica, Universidad de Barcelona, Pg. de laVall d’ Hebron 171, E-08035 Barcelona, Spain; E-mail: [email protected] & [email protected].

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0164-0291/00/0400-0255$18.00/0 2000 Plenum Publishing Corporation

256 Perez and Vea

autogrooming—or by conspecifics: allogrooming. In the Mammalia, it usu-ally implies the exploration—tactile, visual or both—of one or more sitesof the body surface, the separation of the fur and the extraction of debrisand ectoparasites. Primates, endowed with highly developed manipulativeabilities as well as complex and flexible social systems, devote a considerablepercentage of time to grooming in general and to allogrooming in particular.We exclusively analyzed allogrooming and, specifically, its functional impli-cations.

Broadly speaking, there are three basic functional hypotheses of allo-grooming in primates: 1) hygienic (see below), 2) distensive (Terry, 1970;Boccia et al., 1989; Schino et al., 1990), and 3) affiliative (Yerkes, 1933;Smuts, 1985; Dunbar, 1991; Chiarello, 1995). Regarding the social implica-tions of allogrooming Seyfarth (1977), Seyfarth and Cheney (1984), andHemelrijk and Ek (1991) proposed models that relate allogrooming net-works to the structure of dominance relationships and identified patternsof association and exchange between it and other social behaviors (Seyfarth,1977; Seyfarth & Cheney 1984; Hemelrijk and Ek 1991).

Many authors have supported the hygienic functional hypothesis ofallogrooming, pointing out aspects such as cleansing of the fur, the extrac-tion of ectoparasites and the prevention of infections. The main evidenceprovided by the different authors is the highest concentration of allogroom-ing on bodily sites inaccessible to autogrooming, that is, areas that cannotbe seen and/or comfortably groomed by the subject itself (Furuya, 1957;Sparks, 1967; Goodall, 1968; Poirier, 1970; Hutchins and Barash, 1976;Barton, 1983, 1985; Ghiglieri, 1984; Borries, 1992; Reichard and Soomer,1994).

We tested the compensation hypothesis for the inaccessibility to autog-rooming (Perez and Vea 1999), according to which 1) in those sites thatare inaccessible or difficult to reach, the percentage of solicitations shouldbe higher than the percentage of body surface occupied; and 2) in thosesites easily accessible, the percentage of solicitations should be lower thanthe percentage of the body surface occupied. Having confirmed that allo-grooming exchanged within two groups of Cercocebus torquatus lunulatuswas concentrated primarily on bodily sites that are inaccessible and difficultto reach rather than on ones easy to reach (Perez and Vea, 1999), we soughtwhether groomees are prone to solicit more allogrooming to the bodilysites involving accessibility problems, per Boccia’s work (1983, p. 401).

In addition, because the pattern of anogenital presenting has got spe-cific social connotations in many primate species, we expected to obtain ahigh frequency of allogrooming solicitations on this site. Therefore, we alsotested whether the subject variables—sex and dominance—affected theintragroup distribution of anogenital solicitations. Bearing in mind that

Functional Implications of Allogrooming in Cercocebus torquatus 257

anogenital presentations can be used as an appeasement signal and as asubmission gesture (Sade, 1973; Napier and Napier, 1985; Chadwick-Jones,1992; Gust and Gordon, 1993), we expected subordinate subjects to performmost of these presentations. Additionally, when a male smells or groomsa female’s genital area, apart from assessing her sexual receptivity, he mayalso be initiating the early stages of a sexual episode (Michael and Herbert,1963; Simonds, 1974; McFarland, 1981; Goosen, 1987). Accordingly, wealso expected females to perform most of these presentations and malesto receive most of them.

METHODS

Subjects and Housing

We conducted the observations on two groups of Cercocebus torquatuslunulatus, one belonging to the Barcelona Zoo (N � 9) and the other tothe Menagerie du Jardin des Plantes, Paris (N � 8). They were highlystable groups, whose members were used to interacting on a regular basis,because they shared the same facilities continuously day and night. Whenthe observations started, there had been no drastic change in the groupcomposition for a year and a half. During the observational period, thestudy subjects could be monitored continuously. Early in the morning (be-tween 8:30 and 9:00) the observation subjects received monkey chow, andbetween 16:30 and 17:30 they ate the main meal, which consisted mainlyof fruit, vegetables, cereals, and bread. The subjects had a permanenttrough—water ad libitum—fitted into the cage floor.

Materials

We used a Sony 8 CCD V 30 E video camera to record the reliabilitysessions and 1-m TAUMM tape measure, a 50-cm DFH ruler, and a pairof compasses to carry out bodily measurements.

Procedure

To sample the data, we used focal animal sampling (Altmann, 1974)and continuous recording. The category systems of the most relevant vari-ables are as follows.

258 Perez and Vea

Bodily Site

Section of the body surface: skin, fur, or both. Categories are illustratedin Fig. 1.

To estimate the percentage of body surface occupied by each site, wemeasured a subject previously narcotized. We chose the adolescent maleof the Barcelona group because he was the member that seemed to bestrepresent the mean body structure and size of the subjects observed (inter-mediate corporal proportions between females and males, on the one hand,and between mature and immature subjects, on the other).

The 5085.69 cm2 of body surface measured on the Cercocebus torquatuslunulatus were distributed as specified in Table I.

Fig. 1. Division of the body surface of Cercocebus torquatus lunulatus into 17 bodily sites(overall body surface: 5085:69 cm2).


Table I. Corporal distribution of allogrooming solicitations and level of adjustment of eachsite’s data to the reception pattern predicted from the compensation hypothesis for the inaccessi-

bility to autogrooming

BodyBarcelona Paris surface

frequencies (%) frequencies (%) (%) Barcelona Paris

InaccessibleFace 7 3.0 1 0.6 1.7 OK —Head 7 3.0 3 1.9 3.7 — —Neck 5 2.1 4 2.5 1.5 OK OKUpper back 17 7.3 12 7.4 3.4 OK OKLower back 11 4.7 7 4.4 2.8 OK OK

DifficultTail base 26 11.1 17 10.6 4.5 OK OKAnogenital 128 54.7 94 58.4 1.25 OK OKChest 5 2.1 3 1.9 5.0 — —Arm 4 1.7 1 0.6 11.0 — —Flank 10 4.3 5 3.1 5.8 OK OK

EasyDistal tail 0 0 1 0.6 3.2 OK OKBelly 1 0.4 5 3.1 5.3 OK OKForearm 0 0 0 0 9.5 OK OKHand 0 0 0 0 4.6 OK OKThigh 11 4.7 6 3.7 15.0 OK OKLeg 2 0.9 2 1.2 14.0 OK OKFoot 0 0 0 0 7.8 OK OK

Total 234 100 161 100 100 14/17a 13/17b

OK/(OK��)Without 106 67 13/16b 12/16b

ANOGOK/(OK��)

Legend: OK: relative quantity of allogrooming solicitations adjusted to predictions; —: relativequantity of allogrooming solicitations contradictory with predictions; OK/(OK��): quantityof cases in which the sing of the difference detected was consistent with the predictions/totalnumber of cases considered.ap � 0.01.bp � 0.05.

Degree of Accessibility to Autogrooming of the Various Bodily Sites

Extent to which a given bodily site is accessible to grooming by thesubject itself. We chose a mixed criterion of accessibility to autogroomingthat combines manipulative comfort and visibility (Ghiglieri, 1984; Boccia,1983; Borries, 1992).

Before conducting the analyses, we tested the empirical adequacy ofour classification, analyzing the corporal distribution of autogrooming.After this assessment, we decided to include the arm, which cannot bemanipulated bimanually as difficult to reach because of the few autogroom-ing bouts it actually received. The classification was:

260 Perez and Vea

1. Sites easy to reach: the groomer can see them and simultaneouslymanipulate them with one or both hands (n � 7): thigh, leg, foot,distal tail, hand, forearm, and belly. Percentage of body surfaceoccupied: 59.4%.

2. Sites difficult to reach: partially restricted possibility to see themand simultaneously to manipulate them with one or both hands oronly partial visibility; need to adopt somewhat forced positions inorder to autogroom them (n � 5): tail base, chest, flank, anogenitalarea, and arm. Percentage of body surface occupied: 27.6%.

3. Inaccessible sites: ones that are not visible to the subject (n � 5):head, face, neck, upper back, and lower back. Percentage of bodysurface occupied: 13.0%.

Preceding Behavior

Behavioral context immediately preceding a grooming bout (lag-1).Categories: this variable consists of 26 categories, but, we will exclu-

sively define those relevant for this report:Soliciting allogrooming: show a conspecific a given bodily site, orienting

it toward its face. This behavior is either preceded or not by an approxima-tion of both participants, provided that it does not occur within an agonistic-anagonistic context. This is a very wide concept of solicitation, similar tothose of Simonds (1974), Muroyama (1991), and O’Brien (1993), bothregarding the postures adopted by the subject soliciting allogrooming andthe bodily sites groomed by the receiver of the solicitation. ‘‘Presenting isnot at all a stereotyped body posture, it is a flexible set of variationsaccording to context and intention. For example, presenting-for-groomingmay vary across present-head, present-shoulder, present-side, as has beenrecorded for geladas (Theropithecus gelada, Dunbar, unpublished data)’’(Chadwick-Jones, 1992, p. 93).

In order to know which area was presented, we decided a priori onlyto record solicitations followed by actual allogrooming on the solicitingsubject. In addition, we only recorded successful allogrooming solicitations:ones that were followed by �3 sec of allogrooming emitted on a site. Wealso decided a priori to record distinctively bouts in which allogroomingwas performed on sites whose allogrooming was incompatible with theorientation adopted in the preceding solicitation, for example, offering theface—ventro/ventral orientation—and immediately receiving allogroom-ing on the tail base, or offering the rump—ventro/dorsal orientation—andimmediately receiving allogrooming on the belly. However, we saw no boutof this kind.


We conducted observations between 2 November 1992 and 15 June1993, and between 6 July and 7 September 1993, on the Barcelona and theParis groups, respectively. The half-hour sessions occurred during visitinghours of both zoos (9:00 and 16:30). We observed each subject during 63half-hour sessions: the overall observation time is 535.5 hours (283.5 hourson the Barcelona group and 252 hours on the Paris group). To ensure thereliability of observations, we used video recording and calculated the indexof reliability for nominal scales (Scott, 1955), obtaining results above 90%.

Data Analysis

Via two procedures we analyzed whether the sites for which mostallogrooming was solicited differed from the remaining sites vis-a-vis thecriterion of accessibility to autogrooming: 1) grouping the data in categoriesof accessibility (overall distribution of allogroooming), and 2) consideringeach bodily site singularly (fine distribution of allogrooming). In the lattercase, we distinguished between sites whose percentage of solicitations washigher than the percentage of body surface they occupied and those havinga percentage of solicitations lower than the percentage of body surfacethey occupied, and then applied the sing test. As we expected to obtain ahigh frequency of allogrooming solicitations on the anogenital area, wedecided a priori to conduct analyses both including and excluding this site.

Via the � 2 and Spearman rank tests we also analyzed whether sex anddominance class affected the intragroup distribution of anogenital solicita-tions.

RESULTS

Easily accessible sites received a percentage of solicitations distinctlylower than the percentage of body surface they occupied, while sites withaccessibility problems (inaccessible and difficult to reach), received a per-centage of solicitations higher than the percentage of body surface theyoccupied (Fig. 2).

Table I summarizes results obtained after applying the sign test to dataon the fine distribution of allogrooming solicitations. Accordingly, 1) allthe inaccessible sites except for the head (in both groups) and the face(only in the Paris group) adjusted to predictions; 2) three out of the fivesites that were difficult to reach adjusted to predictions in both groups;and 3) all the easily accessible sites adjusted to predictions. Each 1% ofinaccessible body surface received 3.4% and 3.0% of the solicitations in the

262 Perez and Vea

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Barcelona and Paris group, respectively; each 1% of body surface difficultto reach received 2.1% and 2.0% of the solicitations in the Barcelona groupand Paris group, respectively; and each 1% of easily accessible body surfacereceived 0.1% and 0.4% of the solicitations in the Barcelona group andParis group.

Figure 2 shows that allogrooming solicitations for the anogenital areawere distinctly predominant in both groups. This site, despite constitutinga small portion of the overall body surface, monopolized �50% of solicita-tions in both groups. The distribution patterns of both groups were verysimilar because: 1) three sites, all of which were easily accessible, hadnull frequencies: hand, forearm, and foot; and 2) four sites, which wereinaccessible or difficult to reach, accounted for most allogrooming solicita-tions: upper and lower back, anogenital area, and tail base.

Table II shows the frequencies of emission and reception of anogenitalsolicitations by the members of both groups. The results reveal that in bothgroups sexually receptive females were the main emitters of anogenitalsolicitations (Barcelona group � 2 � 50.04; Paris group � 2 � 43.57, p �0.001 in both groups); and males were the main recipients of solicitations(Barcelona group � 2 � 51.66; Paris group � 2 � 11.92, p � 0.001 in bothgroups).

Concerning the incidence of the factor dominance rank on the intra-

Table II. Emission and reception frequencies of anogenital solicitations by the differentmembers of each group

Barcelona Emissions Receptions Paris Emissions Receptions

M1 2 45 MM1 0 14MF2 14 12 MF2 2 10MM3 7 24 MF3 8 10MF4 27 11 IM4 8 24MF5 13 11 MF5 18 3IF6 6 3 MF6 24 13IM7 2 12 MF7 29 5MF8 11 3 MF8 5 15MF9 46 7Total 128 128 Total 94 94

Interpretation of the subject codes: First letter: age � M: mature; I: immature; second letter:sex � F: female; M: male; third letter: dominance rank. The hierarchy was established usingtwo independent dominance criteria: supplantings and other forms of agonism. In both groupsall the subjects as a whole, as well as the females on their own (both considering all of themand only the adult ones), could be ranked in linear dominance hierarchies (Barcelona: H �0.908 and 1, for agonism and supplantings, respectively, p � 0.001; Kr � 89, p � 0.0004. Paris:H � 0.798 and 0.714, for agonism and supplantings, respectively, p � 0.05; Kr � 42, p �0,0.186). In the following analysis, by lower class subjects, we mean those that occupied thetwo lowest positions in the dominance hierarchy (ranks 8 and 9 in the Barcelona group andranks 7 and 8 in the Paris group).

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group distribution of anogenital solicitations, we could not confirm theprediction that subordinated subjects would perform most of them (Barce-lona group: Spearman Rs � �0.229; Paris group Spearman Rs � �0.625;in both cases n.s.).

DISCUSSION

Although mainly expected, the most significant aspect of the resultsobtained is the distinct predominance of anogenital solicitations. In bothgroups this site monopolized �50% of the solicitations. In principle, wecannot deny that this result is compatible with the hygienic functionalhypothesis. As it is a site that is difficult to reach, according to thecompensation hypothesis, we should expect it to be associated with ahigh amount of solicitations. Further, as it is a site particularly liableto accumulate dirt, we should expect a similar outcome. But we mustalso consider that the anogenital area bears important social connotationsbecause when males smell or groom the female’s genital area, apartfrom assessing her sexual receptivity, they may also be initiating theearly stages of a sexual episode (Michael and Herbert, 1963; Simonds,1974; McFarland, 1981; Goosen, 1987). Moreover, presenting the hind-quarters to a conspecific can be used either to solicit allogrooming oras an appeasement signal aimed at deterring or avoiding a real orpotential attack and also as a proper submissive gesture (Sade, 1973;Napier, and Napier, 1985; Chadwick-Jones, 1992; Gust and Gordon,1993) not associated to the previous reception of any agonistic pattern.So, when a primate shows another its anogenital area without receivingany previous agonistic behavior by the latter, he or she may be solicitingallogrooming, communicating his subordination and/or the recipient’sdominance status, or, if female, may also be offering a sexually interestedmale her genital area to make him aware of her readiness to copulate.Indeed in both groups sexually receptive females were the main perform-ers of anogenital solicitations and males were the main targets of them.We think that the fact that females tended to solicit allogrooming tothe anogenital area more frequently than males did is compatible withthe hygienic functional hypothesis because their anogenital areas areespecially liable to accumulate dirt: menses and secretions associatedwith genital swelling. But the fact that males were the main receiversof this kind of solicitation cannot be explained in hygienic terms. Nothingsuggests that male mangabeys are better cleaners than females.

The results obtained in the analyses of the overall and fine distributionof allogrooming solicitations are compatible with the compensation hy-


pothesis for the inaccessibility to autogrooming, since they confirmedthat the sites involving accessibility problems received relative amountsof solicitation distinctly larger than those received by the easily accessiblesites. These results are consistent with Goodall’s (1968) findings withPan troglodytes. Moreover, although they do not fully confirm Boccia’s(1983) predictions, since the frequency of solicitations on the easilyaccessible sites was not null, we think that they are sufficiently compatiblewith her proposal. Receptors seemed to welcome more allogrooming onthe sites with accessibility problems, which is consistent with the hygienicfunctional hypothesis.

At any rate, neither all the inaccessible sites nor all the sites difficultto reach, nor all the easily accessible sites received similar relative amountsof solicitation. Solicitation was a highly selective behavior, which ratherthan being aimed at the sites involving accessibility problems on the whole,concentrated especially on a small number of sites: anogenital area, tail base,and upper and lower back. Barton (1983) also observed strong selectivity inthe corporal distribution of allogrooming solicitations in the Anthropoidea.It consisted of a tendency to favor the genital area and the ischial callosities,whose grooming involves ventral-dorsal orientation between the groomerand the groomee. Similarly, we have found that in both groups the foresites monopolizing 75% of the solicitations were ones whose allogroomingis incompatible with a ventral-ventral orientation between the groomer andthe groomee, which is not the case for five out of the six remaining sites,which are inaccessible and difficult to reach: face, neck, flank, chest, andarm. This may imply that exhibiting such sites, not only facilitates theirallogrooming and ensures their cleansing but also has acquired specificsocial connotations and/or encourages the reception of an allogroomingthat bears specific social connotations. Accordingly, we suggest that thetendency of many species of catarrhine primates to concentrate allogroom-ing on the dorsal and lumbar regions, especially on the back and anogenitalarea (Boccia et al., 1982; Boccia, 1983, 1986, 1989; Barton, 1983; Loy, 1992;Saunders and Hausfater, 1988; Goosen, 1987; Dunbar, 1991), may havebecome a mode of tactile communication, which besides cleaning, maytemper reluctance and/or facilitate relaxation of the groomee, per distensiveallogrooming (Terry, 1970). The compatibility of the overall results ob-tained with the hygienic functional hypothesis of allogrooming does notnecessarily rule out the relevance of other functional implications. Particu-larly attractive is the ritualization hypothesis, according to which allogroom-ing certain sites that are inaccessible or difficult to reach and that cannotbe groomed in ventroventral orientation between the groomer and thegroomee has sociocommunicative meaning (MacKenna, 1978; Boccia et al.,1982; Barton, 1983; Boccia, 1983, 1986, 1989).

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ACKNOWLEDGMENTS

This work was supported by a predoctoral grant (F.P.I: A9040898876),from the Spanish Ministry of Education and Science to A. Perez. We alsothank Mr. Xampeny, former director of the Barcelona Zoo and Mr.Berthier, director of the Menagerie du Jardin des Plantes, as well as theprimate curators and keepers and other staffers of both zoos for their assis-tance.

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Functional Implications of Allogrooming in Cercocebus torquatus

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