Behavioural Development in Male Mandrills (Mandrillus sphinx): Puberty to Adulthood

7/29/2019 Behavioural Development in Male Mandrills (Mandrillus sphinx): Puberty to Adulthood

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Behavioural Development in Male Mandrills (Mandrillus sphinx): Puberty to Adulthood

Author(s): Joanna M. SetchellSource: Behaviour, Vol. 140, No. 8/9 (Aug. - Sep., 2003), pp. 1053-1089Published by: BRILLStable URL: http://www.jstor.org/stable/4536078 .

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BEHAVIOURAL DEVELOPMENT IN MALE MANDRILLS(MANDRILLUS SPHINX): PUBERTY TO ADULTHOOD

by

JOANNA M. SETCHELL12)(CentreInternational e RecherchesMedicales,B.P.769, Franceville,GabonandCentre orResearch n EvolutionaryAnthropology,School of Life andSportsSciences,Universityof

SurreyRoehampton,London,UK)(Acc. 8-VII-2003)

SummaryAdolescence, the periodbetweenpubertyand the attainmentof full adult size and appear-ance, is a distinct and importantdevelopmentalperiod in primates.Althoughadolescencecan account for a significant proportionof a male's reproductiveifespan in highly sexu-ally dimorphicspecies, few studies have concentratedon adolescentdevelopment.In malemandrills,pubertybegins before 4 yr,but males continue to grow anddevelopfor a further6 yr, attainingadult size and appearanceat 10 yr. Concurrently,males become peripheralto the social groupof femalesandtheiroffspring.This studyaimedto describe behaviouraldevelopment n adolescent male mandrills,and to examine the processof peripheralisationandreintegrationnto the social group.I made 20 months of daily behaviouralobservationson 19 post-pubertalmales living in two semifree-ranginggroupsof mandrillsat the Cen-tre International e RecherchesMedicalesin Franceville,Gabon.As age andmorphologicaldevelopment ncreased,and malesperipheralised,ocial behaviours groomingandplay)de-creased,involvement n aggressionincreased,and sexual behaviour ncreasedpertime thatmales spentwith the social group.Behaviouralchangeswere gradualand male peripherali-sation was voluntary;males were not activelyevictedby the dominantmale or othergroup1) Correspondence o: Dr. Joanna M. Setchell, Departmentof Biological Anthropology,Universityof Cambridge,Downing Street,CambridgeCB2 3DZ, UK; e-mail: [email protected]) This study formed part of my doctoral research at the Sub-Departmentof AnimalBehaviour,University of Cambridge,UK, and the Centre Internationalde RecherchesMedicales, Franceville,Gabon.I am gratefulto JeanWickings,and the staff at the Centrede Primatologie,CIRMF, or makingthe study possible, and to Alan Dixson, Phyllis LeeandBenoit Goossens for encouragement, dvice and discussion.Two anonymousreviewersprovidedhelpfulcommentson the manuscript.The MedicalResearchCouncil,UK, fundeddatacollection,with additional ponsorship romCitibank,Gabon. KoninklijkerillNV,Leiden, 003 Behaviour140, 1053-1089Also availableonline-

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1054 SETCHELLmembers.At the end of adolescence one individual n each group took-over as alpha maleand re-entered he social group while other males remainedperipheralor solitary,and I dis-cuss the differencesbetweensuccessful males and theirpeers. Finally,I examinethe possibleproximate and ultimatecauses underlying peripheralisationn male mandrills,concludingthat peripheralisation epresentsa tactic to avoid feeding and male-male competition,whileundergoingdramaticdevelopment n body size andmorphology, n orderto compete effec-tively for access to mates as an adult.

IntroductionPrimatesare characterised y an extendedperiodof adolescentdevelopment,betweenjuvenile and adult stages (Tanner,1962). The juvenile stage endswith the onset of puberty,when increasesin gonadotrophichormonesandsex steroid productionduring sleep are induced by the onset of activity inthe hypothalamic-pituitaryxis (Plant, 1988). Pubertyends when an indi-vidual is reproductivelymature; .e. when a female is capable of bearingan infant to term,andwhen a male can impregnatea female. However,re-productivematuration enerallyoccurspriorto the attainment f adult sizeandappearancen primatesof both sexes, and is followed by an importanttransitionphasewhere individualsare reproductively ompetentbut not yetof adult size. The periodfromthe onset of puberty o the attainment f fulladultsize and appearance as beentermed puberty', subadulthood', youngadulthood',and'adolescence', depending o someextenton the definitionof'adult' used (Caine, 1986; Walters,1987;Setchell & Lee, 2003). HereI usethe term'adolescence'to describethisperiodof rapidmorphological,phys-iological and behaviouraldevelopment, eadingto the cessationof physicalgrowth,endocrinestability,and social competence.

The maturational rocesses of adolescencemay occur over a periodofyears in males of sexually dimorphicspecies (e.g. 4 yr in male rhesusmacaques,Macaca mulatta:Bernstein et al., 1991; and 6 yr in mandrills,Mandrillussphinx:Setchell & Dixson, 2002). This lengthy period,duringwhich males arephysiologicallycapableof siring offspringbut are gener-ally subordinateand physically inferiorto 'prime' adultmales, may thusaccount for a large proportionof a male's reproductive ifespan,and is anextremely importantelement in male life-history (Setchell & Lee, 2003).As well as sexual maturation,pubertalhormonalchanges lead to changesin physical growthanddevelopment.Males, and females of some species,showa massgrowthspurt Leigh, 1992, 1995),andcompleteadultdentition



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BEHAVIOUR IN ADOLESCENT MALE MANDRILLS 1055is attained Watts, 1985). The testes develop and mature,reaching adult di-mensions at approximately he same age as does the body (Kraemeret al.,1982; Nieuwenhuijsenet al., 1987; Setchell & Dixson, 2002), the produc-tion of gonadal steroid hormonescontinuesto increaseto adulthood,andsecondarysex charactersmature.As hormonalandphysical maturation ro-ceed, changes in behaviouralso occur as individualscontinue to make thetransition rom maternalassociationto integration nto the adult commu-nity or dispersal hat begins during he juvenile period (Pereira& Altmann,1985; Pereira& Fairbanks,1993), and adultbehaviourdevelops. By the endof adolescence,male primateshave attainedsexual maturity, ull size andappearance,adultdominancerank(in group-livingspecies), andmay havesired offspring.

By comparisonto adultand infant primates,and even juvenile (Pereira& Fairbanks,1993), and aging primates (Erwin& Hof, 2002), adolescentprimateshave been somewhatneglected in the primate literature,and re-lationshipsbetween physiological maturation nd behaviouraldevelopmentduringadolescence are not well understood butsee Kraemeret al., 1982;Pereira& Altmann,1985; Caine, 1986; Walters,1987; Pusey, 1990; Bercov-itch, 1993;Bernsteinet al., 1993; Pereira& Fairbanks,1993; Alberts& Alt-mann, 1995b;Dixson & Nevison, 1997;Kuester& Paul, 1999). Here,I use2 years of cross-sectionaland longitudinalbehaviouralobservations o ex-aminebehavioural hanges during his periodin adolescentmale mandrills.Mandrillsare one of the most sexually dimorphicprimatespecies, with anadult male body mass (31 kg) 3.4 times that of adult females (Setchell etal., 2001), and this paperforms partof a larger study of socio-sexual de-velopmentduringmale adolescence n this species, integratingmorphology,endocrinologyand behaviour Setchell, 1999;Setchell et al., 2001; Setchell& Dixson, 2002).

Mandrillsare foundin the dense rainforestsof Gabon, Congo, mainlandEquatorialGuineaand southernCameroon o the south of the Sanagariver(Grubb, 1973). They have been described as forest baboons(e.g. Stamm-bach, 1987), but are in fact more closely relatedto mangabeys (Disotell,1994). Verylittle is known about mandrillsocial organisation n the wild,and it has proved impossible to habituateand observe known individualslong-term(Harrison,1988; Abernethyet al., 2002). Most of ourknowledgeof mandrillbehaviourand reproductions thereforebased on studies of a



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1056 SETCHELLsemifree-ranging olony at the CentreInternationalde RecherchesMedi-cales, Franceville(CIRMF),Gabon. Studies of this colony have shownthattesticulardescentoccurs at 3.8 yr in male mandrills,and testicularvolumebegins to increase at 5.5 yr (Setchell & Dixson, 2002). At this age malesresembleadult females, are only 39% of their adult mass, and theirtesteswill continue to develop for a further ouryears (Setchell & Dixson, 2002).Shortlyafterthe testesbegin to develop,males beginto develop thespectac-ularsecondarysexualcharacters ound in adultmales, including ntensifica-tion of red, blue andviolet colorationon the face, rump andgenitalia,andactivityof the sternalscent-marking land(at 6-7 yr). Testosteronebegin torise at 7 yr and mass growthpeaks at 7-8 yr. By late adolescencemales (8-9 yr) malesare almostadult n size andappearance nd they attain ull adultbody mass andbody lengthat 10 yr (Setchell et al., 2001; Setchell & Dix-son, 2002). As in otherCercopithecidprimates andindeedmost mammals:Greenwood,1980; Dobson, 1982; Stenseth& Lidicker,1992), male man-drillsperipheraliseandemigratefrom theirnatalgroupduringadolescence(Setchell&Dixson,2002). Adult malesvarygreatly n groupassociationandmaybe group-associated, eripheral r solitaryboth in semi-captivity Wick-ings & Dixson, 1992; Setchell & Dixson, 2001a) and in the wild (Rogerset al., 1996). Recent data have shown that male group-associations sea-sonal in the wild, with fewer or even no adult males residentin the socialgroupoutsidethematingseason(Abernethy t al., 2002). However, n semi-captivity, hedominantmale of agroup s group-associatedear-round,whilevariabilityn thedegreeof groupassociationof otheradultmales and adoles-cent males does notappear o be related o thepresenceof sexuallyattractivefemales (Setchell& Dixson, 2001c).This studyaims to providea descriptionof changes in social behaviourduringadolescence,and to examinetheprocessof peripheralisationnd re-integrationnto the social group.The conspicuouschangesin male size andappearance hat occur as males increase in age duringadolescencemightbe expected to provokechanging responses from otheranimals with age,in terms of behaviourreceived,while hormonalchangesin males mightbeexpectedto relateto changesin adolescentmale behaviourwithage. Specifi-cally,developingmalesmaybe evicted fromthe socialgroupas theyincreasein size andsecondarysexualdevelopment,and becomerivalsto more dom-inant adult males. Finally,duringthe study two young males successfullytook over the top-rankposition in theirgroups,andI examine behaviouraldifferencesbetween these 'successful' males and theirpeers.



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BEHAVIOUR IN ADOLESCENT MALE MANDRILLS 1057MethodsSubjectsand behaviouralobservationThe mandrillcolony at the CentreInternational e RecherchesMedicalesinFranceville,Gabon(CIRMF),was established n 1983/4, when 14 animals(6 males, 8 females, originating rom the wild) were released into a 6.5 hanaturallyrain-forested nclosure(Enclosure1). All furtheradditionsto thegroup,subsequent o 1984, are due to reproduction f the founderanimals;some animalshave been removed.A second semifree-ranginggroupwasestablishedin 1994 (in Enclosure 2, 3.5 ha) by transferring17 mandrills(including4 adult males and 6 adult females) from the firstenclosure. Atthe beginning of 1996 there were 36 animals living in Enclosure 1, and24 in Enclosure 2. The animalseat a naturaldiet, supplementedby dailyprovisionof monkey chow, and seasonal fruits. Water s always availablefrom a stream,which runsthroughbothenclosures.

Subjectsfor this study comprisedall the post-pubertalmales (N = 19)living in the two enclosures(Table 1) during1996-1997. Adolescentmaleages rangedfrom 4-9 yr at the beginningof the study (N = 14), and fiveadult males (aged 15+ yr) were includedfor comparisonwith adolescents.Daily behaviouralobservationswere made over 20 months(March1996 -November1997) froma toweroverlooking he enclosures.The dense natureof the forested enclosuresallowed a good view of the animalsfor only afew hourseachday,and malesvaried n observabilityandgroupassociation.Lengthyfocal observationson individual males were not possible, and inorderto maximisecollectionof behaviouraldata undertheseconditions,alloccurrencesof the followingbehaviourswere recorded or eachsubject,withthe otheranimal(s) nvolved(all eventrecording,Martin& Bateson, 1994):groom,social play,threaten, hase,contactaggression(hit, graborwrestle),avoid, flee, presentation, exual presentation, nspect perineum,successful(ejaculatory)mount(for a detailedmandrillethogramsee Setchell, 1999).Male dominancerankwas calculatedusing a dyadic interactionmatrix foreach group, ncludingall interactionswhere one male avoidedor fled whenanothermale approached.

Proximitydatawere collectedevery2 minutesusing scan sampling.Thenumberandidentityof all neighbourswithin(a) arm'sreach and(b) 2 m ofeach male was recorded.This informationwas used to examinethe amount



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1058 SETCHELLTABLE 1. Male subjects

ID Date of Age at 01/03/96 Time observed withBirth (years, months) other animals

Enclosure 15D1 31/1/92 4,1 92 hr 01 min12C1 14/1/91 5, 2 90 hr 58 min2G 6/2/90 6,1 112 hr 10 min2F 12/6/89 6, 9 125 hr 52 min2C1 16/4/89 6,10 59 hr00 min5E 1/3/89 7, 0 60 hr 58 min12E 29/3/88 7,11 135 hr 04 min2E* 29/2/88 8, 0 89 hr 38 min12A1 3/2/87 9,1 53 hr 40 minSC 19/1/87 9, 2 70 hr 50 min18 founder l5yr 167hr46minEnclosure 217C 21/1/90 6,1 29 hr 26 min12F 20/3/89 6, 11 35 hr52minlOD 14/3/89 7, 0 55 hr 28 min16B* 1/3/88 8, 0 84 hr 36 min14 founder 16 yr 75 hr 24 min15 founder 16 yr 2 hr 28 min13 founder 17 yr 77 hr 22 min9 founder 17 yr (died during study) 53 hr 52 min* Indicates 'successful' males that became alpha male in their group during the study.

of time spentin proximityto other individualswhen males were observedwith other animals.Due to the colony conditions observationwas biased towardsperiodswhen more than one animal was in view, andfrequenciesof behaviourcal-culatedper total time observedfor an individualmale were unsatisfactory.Frequencieswere thus calculatedper time that a male was observed withother animals.This gives an idea of a male's social life when he is withthegroup, and yields informationsuch as whether male peripheralisationo-occurs with heightened evels of aggressiveinteraction.However, t shouldbe recognisedthat these rates are for association ime only and are not a re-liable indicationof a male's 'daily' ratesof behaviour.Forexample,a malewho is mostly solitarycan still have very high rates of social behaviouronthe rareoccasions he is with others.The totaltime that each individualwasin view was dependenton his degree of groupassociation,and varied be-



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BEHAVIOUR IN ADOLESCENT MALE MANDRILLS 1059tween 2 hr 28 min (forthe most solitaryadultmale) and 167 hr 46 min forindividualmales (Table 1). Observationswere spreadapproximately venlyacrossthe monthsof the study.Sexual behaviour n these mandrills s concentratedn females showingsexualswellings (Setchell, 1999), and s therefore xaminedhere for femalesthatshowed sexual swelling, butwere not yet at maximal tumescence (andtherefore ess likely to ovulate and be fertile), and for maximally swollenfemales (more likely to ovulate,Wildtet al., 1977; Schaikhet al., 1982).

Under the conditionsof this study it was not possible to determinetheactualpercentageof time that ndividualmales spent nearothergroupmem-bers. The group affiliationof each male was thereforescored during dailyobservationperiodsas being 'groupassociated':travelling, eeding, andin-teractingaspartof the socialgroup; peripheral': ftenmorethan 100mfromall othergroupmembers, ravellingand feedingon the edge of the group;or'solitary':travellingandfeeding alone (Wickings & Dixson, 1992). Periph-eral males appeared o trackgroupmovements n theenclosures,while soli-tarymalesappearedo activelyavoid contactwiththegroup.Both classes ofmale avoided other males. Observations uggestthatperipheralandsolitarymales also sleep alone (unpubl.data).The measurement f days spent 'pe-ripheral'meantthat%days solitary was not equal to 100 minus % days incentreof group,butwas the%days spentneither n thecentre,norperipheralto, thegroup.

For the purposes of this study, the term 'adolescentmale' is used forpost-pubertalmales that were not yet of adult size and appearance age 4-10 years), 'adult male' is used for males that had reached full size (all ofwhom were aged 15+ yrs at the time of the study), 'females' are femalesthat have alreadyshown one sexual swelling cycle, while 'juveniles' arepre-pubertal,weaned individuals of both sexes. Males whose motherwasno longer in the groupat the time of the study (9 of 19 adolescentmales)were termed'orphans'.Finally,the two adolescent males that succeededintaking-overas dominantmale in theirgroup duringthe studywere referredto as 'successful'males.MorphologicaldevelopmentThe morphologicaldevelopmentof the studyanimalshas been described ndetail elsewhere, and is closely related to age (Setchell, 1999; Setchell &



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1060 SETCHELLDixson, 2001a, 2002). Morphologicalmeasurementsare made during pe-riodic captures, ncludingbody mass and crown-rump ength (CRL), andblood samples are collected for endocrineanalysis.Coloration s quantifiedusing graduatedcolour charts (for details see Setchell & Dixson, 2001a,2002). All males increasedin body mass and degree of secondary sexualdevelopment rom one year of the study to the next. Physical developmentvaries between adolescent males of the same age, and physical appearanceis likely to be at least as important n social interactions s age itself. I there-fore includeda measureof the brightnessof the red colorationon the faceas an indicatorof secondarysexual development or each male in analyses(degreeof coloration s closely linked to generaldegreeof secondarysexualdevelopmentof a male, Setchell & Dixson, 2002).StatisticalanalysisPatternsof change in adolescentmale behaviourwith age and red coloration(as an indicatorof morphological development)were investigated usingSpearman's orrelations,using a single datapointfor each male (N = 14).The influenceof increasedage and secondarysexual developmentwas alsoinvestigatedby dividingthe behaviouraldata nto the two years of the study(1996 and 1997), providinga matchedpairof datapoints for each develop-ing male, and allowingthe use of Wilcoxon signed-rankests to investigatethe effect of a year's increase n age and secondarysexualdevelopmentonmale behaviour.These rates of behaviourduring1996 and 1997 areplottedvs age to illustrate he evolutionof behaviourduringadolescence(the samesymbolis usedforthe same individualadolescentmalethroughout llplots).Friedmanchi-squared ests were used to compare he rates at which behav-iourswere madeto or receivedfromothermales,femalesand uveniles,andWilcoxon signed-rank ests were used to comparethe rates at whichmalesmade and received behaviours.Means arequotedas mean+ standard rrorof the mean. Statisticalanalyseswere performedwith the significance evelset at p 15 years)forcomparativepurposes.



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1078 SETCHELL1993), play declined with age, showed a tendencyto transform nto aggres-sionin older adolescents apparentnvitations o play resulted n aggression),anddisappeared ntirelyas males reachedadulthood.The relatively ow ratesof play by younger males in this study may have been due to a lack of po-tential play partners,as there were few 3-5 yr old males in either group atthe time of the study;play is more common among young adolescentmaleswhenmore play partnersare available unpubl.obs.).

Older adolescent males were higher-ranking han younger adolescentmales, andit is thereforenot surprising hat adolescentmales threatened ndchasedotheradolescentmales moreoften(pertimespentwithotheranimals)as age increased.Males also foughtmore often with one anotherwhen theywerepresentwith the social groupas age and coloration ncreased.Submis-sion received increased with age, as expected from an increasein relativerank(and thereforean increasein the numberof subordinateanimals). In-terestingly,however,there were no clear patternsof changesin aggressionreceivedas males increased n age. Inparticular,males did notreceive moreaggressionfrom the dominantmale pertime thatthey spentwith the groupas theyincreased n age, implyingthattheywere not actively 'evicted'fromthegroupas theymatured.

As expected from their larger size, adolescent males threatened andchasedjuveniles, and received submission n return.Affiliative nteractionswere far rarer hanagonismbetween adolescents andjuveniles. Affiliationwith females was also relativelyrare.Adolescent males rarelyshowed sub-mission to females, probablybecause they become heavier than adultfe-males early in adolescence,at the age of 4.5 yr (Setchell et al., 2001), andsubmissionmade to females decreasedwith age (andthereforewith bodysize). As males increased n age andsecondarysexualdevelopment heydidnot receive more aggressionfrom females when they were with the socialgroup, suggestingthatmaturingmales were not chased out of the group byfemales.

Adolescentmales were sexually active,andsuccessfullymountedpoten-tiallyfertile femalesfrom theageof 6 yr.As in otherprimate pecies (Pereira& Altmann, 1985), dominantmales did not toleratesexual behaviour romthese rival males, and most adolescentmales mated surreptitiously nd ata low frequency,althoughthe 'sneak' natureof these copulations suggeststhat these may be more commonthanmy observationssuggest. Moreover,most adolescent males spentlittle time with the social group, limitingtheir



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BEHAVIOUR IN ADOLESCENT MALE MANDRILLS 1079opportunities or sexual interactionwith females. Mate-guarding ehaviourwas only shown by the two late adolescent males that gained alpha rank.Sneak matings by low-rankingand extra-groupmales have also been ob-served n geladas (Dunbar,1984), patasmonkeys (Ohsawaet al., 1993), rhe-sus macaques (Berardet al., 1994; Manson, 1996) and Japanesemacaques(Soltis et al., 2001). Such matingsare likely to be less successfulthan mate-guardingbehaviour e.g. Wickings et al., 1993; Soltis et al., 2001), but arealso less riskyfor the male involved.Finally,I should note thatall the malesin this study are natal, and thatthis may influence their sexualinteractionswith females, in particular emale cooperation n matingattempts.However,althoughno data are availablefor unfamiliaranimals for comparison, hesexual behaviourof mother-sondyads is not quantitativelydifferent fromthat of otherfemale-maledyads (Setchell, 1999).Behaviouraland morphologicaldevelopmentduringadolescenceThe behavioural hangesduringadolescencein male mandrillsdocumentedhere coincide with dramaticchanges in endocrinologyand morphology.Mostnotably,maleperipheralisationoincideswith thepeakin massgrowth(7-8 yr), suchthat males were only rarelygroup-associated t the heightofthe growthspurt.Unfortunately, owever, hemorphologicaldataand samplesizes availableare insufficient o determinewhetherperipheralisationoin-cided with the height of the growth spurt n individualmales. Whether hehormonaland morphologicalchanges during pubertyand adolescencearedirectly causallyrelatedto changesin male behaviour, uch as increasesinaggressionorperipheralisation,s unknown.Stageof genitaldevelopmentsmoreclosely correlatedwith a declinein associationwiththemother n malechimpanzeesthanare age or body mass (Pusey, 1990), suggestingthatbe-haviouralchangesare moreclosely related o physiologythanto chronolog-ical age. Similarly,adolescentmalemandrills hatdevelop secondarysexualcharacteristics arlier also peripheralise arlier(Setchell & Dixson, 2002).Due to the close relationshipbetween age andmorphologicaldevelopmentin these mandrills, t is not surprising hatcorrelationsbetween behaviouralandmorphologicaldevelopmentwere similarto those between behaviouraldevelopmentandage. However,even where correlations xist betweenphys-iological andbehaviouralchanges, these do not imply causalrelationships



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1080 SETCHELL(in eitherdirection).Relationshipsbetweenphysiology andbehaviour n pri-mates are complex (e.g. Sapolsky,1993), and male aggressionand hierarchi-cal behaviour n chimpanzees Nadleret al., 1987; Kraemer t al., 1982) ap-pearto be associatedwith adulthormoneproductionandfunction and adultsize, rather han to increases n hormone evels duringadolescence.Indeed,Coe et al. (1988) suggest thatcorrelationsbetween behaviour,growth andphysiology duringadolescencedo not indicatea causal relationship,but thatdevelopmentalprocesses simply occurin parallel.Dominance rankand takingover as dominantmaleTake-oversof top-rankby male primatescan occur in one of three ways:defeatof the previoustop-rankingmaleby aggressivechallenge;during heformationof a new group,eitherby acquiring emales from anothergroup,or during group fission; or via succession, where the previoustop-rankingmale dies or leaves the group with no aggressive challenge (reviewedinvan Noordwijk & van Schaik, 2003). The strategiesemployed dependonthe degree of paternityconcentrationn dominantmales, with males morewilling to takerisks where the benefits of top rankare high (van Noordwijk& van Schaik, 2003). In the CIRMFmandrills he dominantmale sires 80-100% of offspringin a matingperiod (Wickings, 1995). This predictsthatmales shouldemploy aggressivechallengeto achievetop-rank,andthe twotake-oversobservedduring his study suggestthat this is so, as in both casesthe previous alphamale sustainedseriousinjuriescoincident with the rankreversal.However, heactual ightswere notobserved,andtheidentityof themale that nflictedthe wounds s unknown,althoughcircumstantial videnceimplicatesthe successful malein Group2.

The males thattook-over as dominantmale in theirgroupdid so duringlate adolescence (9 yr). Males attainadultbody size andappearance hortlyafter the age of 9 yr, and are thus likely to be in their prime at this age.These malesre-integratednto the social group,while othermaturingmalesremained solitary or peripheral.Successful males also spent fewer scansalone when they were with the social group,and groomedmore often pertimespentwithotheranimals hanage-mates althoughnotoften), indicatingthatthey weremoreintegratednto the social group.Successfulmales werenot the most aggressivemales; they did not threatenor chase other animalsas often as some of theirpeers,and were involved in fewerfightsthan some



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BEHAVIOUR IN ADOLESCENT MALE MANDRILLS 1081other adolescentmales. They did not stand-out rom other males in the rateof threatsor chases received.As expectedfrom theirhigh social ranktheymade very few submissivebehaviours, and received relatively high ratesof submissionfrom other individuals.Finally, successful males were theonly adolescent males to show mate-guardingbehaviour,while all otheradolescentmales matedsurreptitiously.

Why do some maturingmale mandrillsmake an attempt o take-over hesocial group,while othersdo not? Characteristics f the currentalphamale,and the age and competitiveability of othermales present,are likely to beimportantn male decisions. In both groupsstudied here the existing adultmales (thecolony founders)were relativelyold (all > 15 yr), andwere likelyto have been past theircompetitiveprime.The groups were thus 'ripe' fortake-over.In Group 2, the eldest, largest, and most developed adolescentmale rose rapidly throughthe adult male hierarchybetweenthe ages of 8and9, and took-over he groupwhen he reached he age of 9 years.This ap-pearsto be a simplesituationof a younger,primemaledefeatingolder,post-primerivals.However, n Group1, two olderadolescentmales werepresentin the groupwhen a nine-year old took over as alphafrom the only adultmale.Furthermore,dolescentmalesmaturingn thepresenceof a primeal-pha male may or may not make a take-overattempt: ince this studyendedGroup 1 has experiencedseveralmale take-overs,while male 16B has re-maineddominant ince 1997 in Group2, althoughyoungeradolescentmaleshavegrownto full adult size in the meantime.Males that do not attainhighrank mmediatelyon reachingmaturitymay attempta dominance ake-overduringthe following few years of theirprime,or may never do so. Differ-ences among individualmaturingmales, as well as in groupdemography,must thereforealso play a role in male rankacquisitionstrategies.Differ-ences betweenmales thatstrive for and attainhigh rank andtheirpeersarelikely to be basedon differences n physical size, early experience,previousagonisticencounters e.g. defeatin male-male nteractionsdepressestestos-terone evels:Rose et al., 1975;Sapolsky,1987; Raleigh& Macquire,1990),andpossiblyeven 'personality' e.g. Sapolsky& Ray, 1989).

Dominanceranksamongadolescentmale mandrillsarerelativelystableover time (Setchell & Wickings, unpubl.results),and are likely to be es-tablishedduring mmaturity.Thus the rankacquisitionstrategiesemployedearly in life may be extremelyimportantn the ultimateattainmentof high



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1082 SETCHELLrankas an adult andcorrespondinghigh reproductive uccess. These strate-gies are as yet unknown or male mandrills,but studies of juvenilebaboonssuggest thatthey are likely to be relatedto slight differences n body mass,with heaviermalesdominating ighterage-mates Pereira,1989;Lee & John-son, 1991; Pereira,1992). Maternalpresence or absence andmaternal ankmay also be importantn rank acquisitionduringthe juvenile period, eitherdirectly (via intervention n social interactions,e.g. Pereira,1989) or indi-rectly, via a body mass advantage.At the ages studiedhere,male mandrillsinteractedvery little with their mothers,and there was little difference inbehaviourbetweenorphansand individualswiththeirmotherpresent.How-ever, sons of higher-rankingemale mandrillsare larger for their age thansons of lower-rankingemales both during early life and later during ado-lescent development Setchell et al., 2001; Setchell & Dixson, 2002), a dif-ference which is likely to influence their social development.Long-lastinginfluences of maternalvariableson male development, trategiesand repro-ductive success havebeen demonstrated or otherOld Worldmonkeys.Forexample,maternaldeathduring mmaturityeadsto earlierdispersal n malebaboons(Alberts& Altmann, 1995a), testicularenlargementoccurs earlierin sons of high rankingmothers,and attainment f adult dominancerank saccelerated n both sons of high-rankingmothers,and in orphanmales (Al-berts & Altmann,1995b). High maternalrank is also linkedto acceleratedphysical development n rhesusmacaques Dixson & Nevison, 1997),whilehigh-born Barbarymacaques begin to reproducesignificantlyearlierthanlow-bornpeers (Paulet al., 1992).Peripheralisation nd reintegrationA particular im of this studywas to investigate he proximatemechanismsunderlyingperipheralisationn adolescentmale mandrills.Opportunitiesordispersalare imited n thecolony,andmales cannotmigrate o anothergroup(althoughadolescentmales show a greatdeal of interest n the group ivingin the neighbouring nclosure).However,preliminary videnceforperipher-alisationanddispersalby adolescentmales has also been reported or wildmandrills,where a decreasein male groupmembershipoccurs at approxi-mately6 yr (Abernethyet al., 2002). Such a decreasemay be explainedbya numberof factors, includingdifferentialmortality,but also by males dis-persingandspendingtime solitary,as observed n this semi-captivecolony.



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BEHAVIOUR IN ADOLESCENT MALE MANDRILLS 1083Evidencefromboth semi-captivityandthe wild suggests thatboth adolescentand some adultmales areperipheral o social groups, or solitary (Wickings& Dixson, 1992; Setchell & Dixson, 2001a; Abernethyet al., 2002), ratherthantransferring irectlyto anothergroup.

Proximate auses of dispersal n primatesarereviewedby Pusey & Packer(1987), and include coercion (e.g. female hamadryasbaboons, Abegglen,1984), eviction (principallymales in one-male, multi-femalegroups) or at-traction o extra-group nimals.Colony conditions, and the difficultyof be-haviouralobservation,mean thatdataare insufficient o show whethergroupassociation statuschanges following majoragonistic interactions.However,peripheralisation ppeared o be voluntary n this colony, and there was noevidence for targetedeviction of adolescent males. The rate of aggressionreceived decreasedas males peripheralised, imply because they spent lesstime in the companyof other animals. However, males did not experienceincreased aggression when they were with the group as they increased inage andphysical development,eitherfromotheranimals n general,or fromthedominantmalein particular.A similarsituation s found in variousotherCercopithecidspecies, whereyoung males emigratewithout increasedex-pression of aggression from other animals (reviewedin Pusey & Packer,1987), although young male Hanuman angurs (Borries, 2000), blue mon-keys (Rudran,1978),red-tailmonkeysandblack-and-white olobus (Struh-saker & Leland, 1979) experienceincreased rates of aggressionwith age,which is assumedto provokeemigration.

In species with multi-male,multi-femalegroups,males may disperseinorderto improvetheir mating opportunities,by joining groupswith morecycling females, with a more favourablesex ratio, or by improvingtheirsocial rank Alberts& Altmann,1995a;Borries,2000;vanNoordwijk& vanSchaik, 2001, 2003). However attraction o females in anothergroupis anunsatisfactory xplanation or peripheralisation nddispersal n adolescentmale mandrills,as these males become solitary. Finally, dispersingmalemandrillsare not attracted o join an all male group (as in geladas:Dunbar& Dunbar,1975), or otheremigratingmales (reviewed n Pusey & Packer,1987), as theydo not form all male bands.

Hypothesisedultimatecauses for dispersalin primates nclude inbreed-ing avoidance,resourceexploitation,and avoidanceof intra-sexual ompe-tition(reviewed n Pusey & Packer,1987). Of these, the lattertwo explana-tions, citing intra-specific ompetition,seem the most relevant o mandrills.



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1084 SETCHELLMales in the CIRMF colony do not have the option of dispersing,but re-main solitary or peripheral,or re-integrate nto their natal group when theyattainadult size. Returningmales can, and do, mate with close female rela-tives (Setchell, 1999). The destinationof adolescent males in the wild, andwhether they disperse and join other groups or return o their natal group,remainsunknown.However, n groups that numberover 600 animals, withalmost 200 adult females (Abernethyet al., 2002), the likelihood of a maleaged9+ yr reproducingwith close relativesseems small, evenif he re-entershis natal group. Thus inbreedingavoidance seems an unlikely explanationfor male peripheralisation. y contrast, t seems likely that wild males maydisperseas a result of nutritionalpressureswithin very large groups.Dis-persingmalesavoid feeding competition,and also avoid ntra-sexual ompe-tition with larger,and presumablymore competitive,adultmales. Male-malecompetition s intense in male mandrills,and dominancerank is relatedtothe expression of secondarysexual charactersboth duringadolescence andadulthood Wickings& Dixson, 1992;Setchell & Dixson, 2001a, b, 2002).A solitaryphase may thus representa tacticto minimiseboth feeding compe-tition andsocial factorsthat act to constraingrowthanddevelopment,whileundergoinga dramaticgrowth spurt,as in long-tailed macaques (Macacafascicularis: van Noordwijk& van Schaik, 1985). When they reach adultsize, some individualsarecapableof taking-overas alphamale in a group,andbecoming group-associated.Lower-ranking dultmales, meanwhile,re-mainless group-associated, r solitary(Wickings& Dixson, 1992;Setchell& Dixson, 2001a). In the wild, such peripheralor solitarymales are likelyto face an increased risk of predation, mplying that the competitivecosts(nutritionaland/orintra-sexual)of being group-associatedare higherthanthose of remainingsolitary.A furtherquestionfor the futureconcernstherelevance of dominancestatusand,in particular, lpha rank,to male socialrelationshipsandreproductiveuccess in thelarge groupsfoundin thewild.ConclusionsAdolescence is an extremely importantbutrelatively neglected periodof amaleprimate's ifespan, duringwhich malesbecomereproductively apable,butare not yet adultin size or appearance. n mandrills,reproductive kewtowardsvery large,ornamentedmales (Wickingset al., 1993) has led to anadolescentperiod of 5-6 yr before males reach prime adulthood,become



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BEHAVIOUR IN ADOLESCENT MALE MANDRILLS 1085capable of taking over top-rank,and are likely to reproduce.This period islikely to representa significantproportion f a male'sreproductiveifespan,duringwhich competitively nferioradolescentmales employ a strategyofperipheralisation, ndmate opportunistically,voiding ntra-sexual ompeti-tion,while undergoingdramatic hangesin body size andmorphology.Thisstudy shows thatperipheralisations a gradualprocess, and males are notdrivenout of theirnatalgroupby othergroupmembers.Only males that at-tain high dominancerankrejointhe social group,while otheradult malesremainperipheralor solitary.As with all aspectsof mandrillbehaviour, hesituationin the wild remains almost completelyunknown. Studies of thissemifree-ranging olony can providehypothesesto guide field studies,andradio-trackingAbernethy& White, 1999) and non-invasivegenetic studies(Cliffordet al., 2002) currentlyunderwayat the Lope Reserve,Gabonwillshedfurtherighton male strategiesduringadolescence and adulthood.

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Behavioural Development in Male Mandrills (Mandrillus sphinx): Puberty to Adulthood