Author Institution: Division of Biological Sciences, University of Michigan, Ann Arbor, and New York Zoological SocietyExperimental walks with a tame primate reveal that free living primates are likely to be subject to frequent infestation by ticks. Observations on the grooming behavior of mangabeys, red colobus and blue monkeys demonstrated that self grooming is primarily directed to parts of the body not subjected to allo-grooming, and that its role is a cursory brushing away of loose particles rather than a detailed cleansing. Allo-grooming is directed towards the detailed cleansing of the skin and fur, and is associated with frequent particle removal. Length of body fur has a considerable influence on the amount of grooming different parts of the body receive. I suggest that sexual dimorphism, age, sex and dominance status are important in determining rates of ectoparasite acquisition, and so the amount of grooming individuals need and receive

Freeland, W. J.

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Copyright © 1981 Ohio Acad. Sci. OO3O-O95O/81/OOO4-O173 $2.00/0FUNCTIONAL ASPECTS OF PRIMATE GROOMING1W. J. FREELAND,2 Division of Biological Sciences, University of Michigan, Ann Arbor, and New York Zoological Society,Bronx, NYAbstract. Experimental walks with a tame primate reveal that free living primates arelikely to be subject to frequent infestation by ticks. Observations on the grooming behaviorof mangabeys, red colobus and blue monkeys demonstrated that self grooming is primarilydirected to parts of the body not subjected to allo-grooming, and that its role is a cursorybrushing away of loose particles rather than a detailed cleansing. Allo-grooming is directedtowards the detailed cleansing of the skin and fur, and is associated with frequent particleremoval. Length of body fur has a considerable influence on the amount of grooming differ-ent parts of the body receive. I suggest that sexual dimorphism, age, sex and dominancestatus are important in determining rates of ectoparasite acquisition, and so the amount ofgrooming individuals need and receive.OHIOJ . SCI. 81(4): 173, 1981Numerous workers have emphasized thesocial roles of primate allo-grooming (e.g.,Hall and Mayer 1967, Rowell 1968). In-vestigation of grooming's functional as-pects has been limited to casual field obser-vations (e.g., Schaller 1963, Struhsaker1967), or studies on captive primates andextrapolation to what grooming may dounder natural circumstances (e.g. Hutchinsand Barash 1976). In this paper, I give anexperimentally determined estimate of therate at which a primate is likely to acquireticks in Kibale Forest, Uganda, and pro-vide a detailed account of self and allo-grooming in three primate species: themangabey (Cercocebus albigena), the red co-lobus monkey (Colobus badius) and the bluemonkey (Cercopitbecus mitts).MATERIALS AND METHODSStudy Area. The study was carried out in the Kanya-wara study area of Kibale Forest, Uganda (0°13' to 0°41' Nand 30°19' to 30°32' E). Detailed descriptions of theKanyawara study site are available in Struhsaker (1975) andWaser(1974).Acquisition of Ectoparasites. During the monthsMay to October 1974, a pet Cercopithecus ascanius (an oldjuvenile male) was taken for a total of nine walks throughthe forest at Kanyawara. On each of these walks the mon-key's owner (Mrs. R. Rudran), the monkey and I spent onehour in the forest. During this time we walked a more or lessfixed path of 750 m. The monkey was allowed to roamfreely. Not all walks could be made to be one hour, but ac-curate time records were kept. The monkey did not behaveManuscript received 19 May 1980 (#80-23).Present address: Department of Biological Sciences,Wright State University, Dayton OH 45435.as is normal for Cercopithecus ascanius. In particular, most ofhis activity (usually gathering and eating insects, fruits andleaves) was confined to less than 20 ft above ground. WildC. ascanius spend most of their time at heights greater than20 ft (Freeland 1977). At the end of each walk the monkeywas thoroughly searched for ectoparasites. I recorded thenumber of ticks I acquired in more than 500 hours spent inthe forest during the months May to October 1974.Grooming Obervations. Observations of groomingwere made while following particular groups of each mon-key species. All grooming was recorded according to time ofday, whether it was self or allo-grooming, parts of the bodygroomed and the type of grooming motion employed. Dur-ing any single grooming bout, several observations werelikely to be made of grooming to different parts of the body.A single grooming observation was defined as groomingmotions to a particular part of the body. If grooming to aparticular body part continued for longer than two minutes,it was recorded as an additional grooming observation. Ifdifferent grooming motions were applied to the same bodypart, it was regarded as a single grooming observation withseveral different subcategories. A minimum sample of 500observations of self and allo-grooming was made for eachspecies.Division of the body into parts was made according towhich parts seemed to be distinguished by the monkeysthemselves (figure 1). Surface area of skin was not taken intoaccount. Where a part of a body was actually two parts {e.g.,there are two inner thighs) it was regarded as one. Recordswere taken with the aid of a tape recorder.Measurements were made of the length of hair on the dif-ferent parts of the body of all three species. The mangabeyskin used was that of an old juvenile male in the museum ofthe Zoology Department, Makere University, Uganda. Theblue monkey used was an adult female found dead atKanyawara. The red colobus (Colobus badius) was an adultfemale from the Tana River, Kenya (courtesy of the Amer.Mus. Nat. Hist.). The hair lengths used in the analyses arethe means of five measures of maximum hair lengths takenfrom each body part.RESULTSAcquisition of Ectoparasites. Theonly ectoparasites acquired by the tame C.173174 W. J.FIGURE 1. A drawing of a mangabey showing the way inwhich the body was divided into parts for recording groom-ing. a=top of head, b=face, c = cheeks, d = ears, e=top ofneck, f=side of neck, g=throat, h=outer upper arm,i=inner upper arm, j = outer lower arm, k = inner lowerarm, l=hands, m=chest, n = shoulders, o=mid back,p = lumbar back, q=chest side, r=stomach, s = lumbarside, t = hip, u = outer thigh, v = inner thigh, w = outerlower log, x = inner lower leg, y=feet, z=ano-genital re-gion, tb = tail base end and tt = tail.ascanius were ticks. The monkey often pre-sented to its owner in such a way as to revealthe location of a tick. During the nine tickwalks, the pet monkey acquired a total of74 ticks. This is a rate of ectoparasite acqui-sition of 8.2 ticks/hr. The number of ticksacquired on a single walk varied from 0 to26. During more than 500 hours in theforest, I acquired 7 ticks, giving amaximum estimate of 0.01 ticks/hr.Grooming Movements. The types ofgrooming motions used by each specieswere very similar. For all species, I classi-fied these motions as scratching or as furparting. Scratching consisted of a brisk rak-ing of the fingertips through the fur, usu-ally applied so as to be against or across thegrain of the fur. During these movements,the animal did not usually look at the areabeing groomed. The toes of the hind footwere also used for scratching. The foot wasbrought forward to the animal's side, arm,or under or over the arm. Fur parting was aFREELAND Vol. 81much slower motion than the scratch.When fur parting, a monkey watches whatit is doing. Fur parting consisted of themonkey slowly moving its fingertips acrossor against the fur. One hand was used, orboth were used in alternation. One handwas often used to hold back a layer of fur,while the other was used to carry out thelong raking motions of fur parting. A re-finement of this motion is found, particu-larly among the species having a well de-veloped thumb (i.e., not the red colobus).This motion consists of holding the fur be-tween the thumb and fingers and graduallydrawing the hand away from the base of thefur. The red colobus occasionally did this,but held the fur between the fingers, as thethumb is greatly reduced in size. These furdrawing motions may be related to removalof particles from the fur, but did not alwaysseem to be so. Definite particle removal wasoperationally defined as being associatedwith either a movement of the hand fromfur to mouth or with the direct applicationof the mouth to the area being groomed.Hand to mouth motions were rare in allspecies, mouth applications being rela-tively common. Direct mouth applicationwas frequently associated with the removalof a mouthful of fur. Inallo-grooming, thisfur removal was often associated with asmall but pronounced jump on the part ofthe recipient. This motion was particularlyso for the red colobus. Only when themouth was involved could particle removalbe relatively safely assumed. Fur drawingmotions lacking mouth involvement areclassed with fur parting. Fur drawing wasrelatively uncommon.Cercocebus albigena. The parts of thebody groomed during self and allo-groom-ing were significantly different (table 1)(X^ = 342.6, d.f.=27, P<.001). Signifi-cantly more particle removals occurred dur-ing allo-grooming than during self groom-ing (table 1). If the grooming observationsare broken down into scratches and furparts, 86.7% of self grooming was scratch-ing, while 100% of allo-grooming was furparting (table 2).The parts of the body groomed duringself and allo-grooming were to a certain ex-Ohio J. Sci. PRIMATE GROOMING 175TABLE 1Parts of the body groomed by Cercocebus albigena duringself and allo-grooming.Self Allo- Partical RemovalBody parts grooming* grooming*Self AlloHead topFaceCheeksEarsNeck sideNeck topThroatUpper arm, outUpper arm, inLower arm, outLower arm, inHandChestShouldersMid backLumbar backChest sideLumbar sideAno-genitalsHipThigh, outThigh, inLeg, outLeg,inTail baseTailFootStomachTotals131512182106221216191145003935236585155304102395262321173128121710126024524742554017132312346513 40*Number of observations.tent complementary. For example, no selfgrooming was observed on the mid andlumbar back, both of which received largeamounts of allo-grooming. Complementar-ity does not explain all the variation. Areassuch as the chest and lumbar sides receiveda great deal of attention from both types ofgrooming. If self and allo-grooming areTABLE 2Percentages of scratching and fur partingin self and allo-grooming.Scratching Fur partingC. albigenaSelf groomingAllo-groomingC. badiusSelf groomingAllo-groomingC. mitisSelf groomingAllo-grooming86.70.069.60.681.60.013.3100.030.399.418.4100.0summed, there is a significant correlationbetween total grooming attention areas re-ceived, and the average hair lengths in thevarious areas (rs=.53, N = 28, P<.01)(table 3).TABLE 3The relationship between hair length and number of grooms toparticular parts of Cercocebus albigena, Colobrus badius,Cercopithecus mitis.Hair length Total groomsBody parts ( m m )Cere Colo Cerp* Cere Colo Cerp*HeadFaceCheeksEarsNeck topNeck sideThroatUpper arm, outUpper arm, inLower arm, outLower arm, inHandChestShouldersMid backLumbar backChest sideLumbar sideStomachAno-genitalsHipThigh, outThigh, inLeg, outLeg,inFootTail baseTail57 168 1412 6— 10113 12103 1938 875 1971 1432 1229 1713 753 20138 25128 2388 18148 35105 3444 1424 985 2340 3732 1641 2636 1320 1573 865 292015385443416402620159446051526568333455536346421147223617232852183922282513857474294751719498163583423101834111320253916403024361441534738727130184777335528311660301536253159342815181712752343176512022342926271752320* Cere —Cercocebus albigena; Colo—Colobus badius; Cerp=Cercopithecus mitis.Colobus badius. Results for this specieswere very much the same as for the man-gabey. There is a significant difference be-tween the areas groomed by self and allo-grooming (table 4) (X2 = 276.1, d.f. = 27,JP<.001) , and a much greater amount ofparticle removal during allo-groomingthan during self-grooming (table 4). Selfgrooming involved mostly scratching,while fur parting predominated duringallo-grooming (table 2). When self andallo-grooming for each body part aresummed, a significant correlation existsbetween fur length and amount of groom-ing attention (rs=.6l, N = 28, P<.01)(table 3).176 W. J. FREELAND Vol. 81TABLE 4 TABLE 5Parts of the body groomed by Colobus badiusduring self and allo-grooming.Body partsHead topFaceCheeksEarsNeck topNeck sideThroatUpper arm, outUpper arm, inLower arm, outLower arm, inHandChestShouldersMid backLumbar backChest sideStomachLumbar sideAno-genitalsHipThigh, outThigh, inLeg, outLeg,inFootTail baseTailTotalsSelf*grooming16258601451722142914165042713323294622472328333501Allo-*grooming18551425251123810702548473445173915183111853132727Particle RemovalSelf1---------11---------3115--15Allo2-11235523--48236124121--2161Body partsHead topFaceCheeksEarsNeck sideNeck topThroatUpper arm, outInner arm, inLower arm, outLower arm, inHandChestShouldersMid backLumbar backChest sideLumbar sideAno-genitalsHipThigh, outThigh, inLeg,outLeg, inTail baseTailFootStomachTotalsduring self and allo-grooming.Self*grooming112119140856913063102611031422261401059238Allo-*grooming29325164531262399412149333150402231154132310011565Partial RemovalSelf-__2__2_4.8Allo224364112212352.111346*Number of observations.Cercopithecus mitis. Results were similarto those found with the other two species.Self and allo-grooming were directed to-wards different parts of the body (X = 274,d.f.=27,P<.001)(table5).Morefurpartsand particle removals occurred during allo-grooming than during self grooming (ta-bles 6 and 2), and a significant correlationexists between fur length and total amountof grooming attention (rs=.6l, N = 28,P<.01)(table3).DISCUSSIONAlthough there are reported observationsof monkeys carrying ticks {e.g., Schaller1963), a large sample of shot Ugandanmonkeys (Haddow 1952) failed to revealeven one tick or other type of ectoparasite.Experimental walks with the pet C. ascaniusindicated that monkeys in Kibale Forest areliable to tick infestation. Given the role ofticks in transmitting diseases among pri-*Number of observations.mates (e.g., Garnham 1957, Rajagopalanand Anderson 1971), tick removal is likelyto be important to individual primates.The importance of tick removal is furtheremphasized by the observation of solitaryred tail monkeys entering red colobusgroups and presenting so as to be groomed(Struhsaker 1975, personal observation).Juvenile and female red colobus do groomsolitary red tail monkeys. Juvenile red co-lobus were observed to attempting togroom red tail monkeys that were not soli-tary and were trying to avoid beinggroomed rather than presenting for groom-ing.Grooming observations on the threespecies revealed that self and allo-groomingin the wild serve somewhat different func-tions. The two types of grooming are di-rected to largely different parts of the body.Self grooming, mainly scratching, appearsOhio J. Sci. PRIMATE GROOMING 177to be rapid brushing of the fur and removalof loose dirt particles and perhaps unat-tached arthropods. Allo-grooming em-phasizes a slow, concentrated parting of thefur and fairly frequent removal of particles.It appears to be geared towards minute skinand fur cleansing, and the removal of at-tached arthropods.The significant correlation between furlength and amount of grooming is of par-ticular interest. Many monkey speciesexhibit a gross sexual dimorphism in termsof fur lengths and/or body size. It is fre-quently observed that sexually dimorphicmales receive more grooming attentionthan do other group individuals(g.g.,Struhsaker 1975). Fur length could beof importance in determining the numberof ectoparasites acquired and so the amountof grooming necessary. There is another pa-rameter that could influence the number ofectoparasites an animal receives and so berelated to the amount of grooming atten-tion required. This is the amount of time ananimal spends moving, and/or the distancean animal moves. Most primates do nothave a particular nest site. Ectoparasites arelikely to be scattered throughout a pri-mate's environment (some probably occur-ing in dense patches). The more often ananimal moves, or the further it travels, themore likely it is to encounter ectoparasites.As yet, there are no data on rainforest mon-keys giving estimates of the relativeamount of movement by different individu-als according to sex, age or dominancestatus. It is not unreasonable to assume thatthe functions and maintenance of domi-nance may increase the distance moved byand the frequency of movement of adultmales. If this is the case, a more dominantindividual may need more grooming than asubordinate animal, simply to remove ahigher ectoparasite load. If these param-eters prove to be of importance in determin-ing the amount of grooming needed and re-ceived, then the apparently excessivegrooming of dominant individuals may re-flect a liability of dominance, as well as thebenefits dominance brings. A full assess-ment of the social role of allo-groomingcannot be made without taking these fac-tors into account.Acknowledgments. The Department of Forestry and theNational Research Council, Government of Uganda, arethanked for making the study possible. The study could nothave been done without the able help of my field assistants.The New York Zoological Society, N.I.H. Grant 1 R01MH 23008-1, andN.S.F. Doctoral Dissertation Grant GB-43850 provided financial support.LITERATURE CITEDFreeland, W. J. 1977 Dynamics of primate parasites. Un-publ. Ph.D. thesis, University of Michigan, Ann Arbor.Garnham, P. C. C. 1957 Trees, ticks and monkeys: furtherattempts to discover the invertebrate host of Hepatocystiskochi. Zeit Tropenmed. Parasit. 45: 217-222.Haddow, A. J. 1952 Field studies on an African monkey,Cercopitbecus ascanim schmidti Matschie. Proc. Zool. Soc.(London) 122: 297-394.Hall, K. R. L. and B. Mayer 1967 Social interactions in agroup of captive patas monkeys (Erythrocebus patas). FoliaPrimat. 5: 213-236.Hutchins, M. and D. P. Barash 1976 Grooming in pri-mates: implications for its utilitarian function. Primates17: 145-150.Rajagopalan, P. K. and C. R. Anderson 1971 Furtherstudies on ticks of wild monkeys of Kyasanur Forest Dis-ease Area, Shimoga District. Indian J. Med. Research59:847-860.Rowell, T. E. 1968 Grooming by adult baboons in relationto reproductive cycles. Anim. Behav. 16: 585-588.Schaller, G. B. 1963 The mountain gorilla, ecology and be-havior. Univ. of Chicago Press, Chicago, 429 pp.Struhsaker, T. T. 1967 Ecology of vervet monkeys (Cer-copithecus aethiops) in the Masai Amboseli Game Reserve,Kenya. Ecologyt 48: 891-904.1975 The red colobus monkey. University ofChicago Press, Chicago, 311 pp.Waser, P. 1974 Intergroup interactions in a forest monkey:the mangabey Cercocebus albigena. Unpubl. Ph.D. thesis,The Rockefeller University, New York.

Functional Aspects of Primate Grooming

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