Short-term costs and correlates of play in cheetahs

13 Pages·1995·0.29 MB·English

by  Caro, T. M.

Anim.Behav.,1995,49,333–345
Short-term costs and correlates of play in cheetahs
T. M. CARO
DepartmentofWildlife,FishandConservationBiologyandCenterforPopulationBiology,
UniversityofCalifornia,Davis,CA95616,U.S.A.
and
SerengetiWildlifeResearchInstitute,P.O.Box661,Arusha,Tanzania
(Received2June1993;initialacceptance16July1993;
finalacceptance19December1993;MS.number:a6722)
Abstract. Costsandbenefitsofplaywereinvestigatedbyobservingcheetah,Acinonyxjubatus,cubsin
thewild.Cubsplayedeitherafterrestingornursing,orwhilethefamilywasmoving;cubswerenever
injuredduring2600hofobservation,anddidnotbecomeseparatedfromtheirmotherduringplay;and
mothersshowedfewsignsofuneasewhilecubsplayed.Itisarguedthatenergeticandindirectcostsof
play were insubstantial. Taking all these potential costs together, overall costs of play appeared low.
Veryyoungcubsshowedhighratesoflocomotorplaysuggestingthatplaymayhaveimmediaterather
than delayed benefits, possibly aiding cubs in escaping predation. Components of non-contact social
play may be functionally or causally related to approaching prey, whereas components of object and
contactplaymayberelatedtocontactingprey.Litter-matesthatstalkedandcrouchedatotherfamily
membersmorefrequentlyduringplayalsostalkedandcrouchedatpreymoreoften,andthoseshowing
morefrequentobjectplayandcontactsocialplayshowedhigherratesofcontactinglivepreyreleased
for them by their mothers. Distances that cubs chased each other and their success in catching each
other during play chases increased with age but the ability of cubs to remain concealed during play
stalks and crouches did not improve, implying that only certain aspects of play might be suitable for
rehearsingpredatoryskills.
Oneofthecentralissuesinthestudyofplayisto limited evidence from human and non-human
determineitsfunctionbecauseitsadaptivesignifi- primates indicates play may promote problem-
cance is poorly understood despite years of solving abilities and skill acquisition in the short
research (reviewed in Smith 1982; Caro 1988). term (human studies reviewed in Smith & Simon
Current functional theories fall into four major 1984; common marmosets, Callithrix jacchus;
categories: (1) those that suggest that play serves Chalmers & Locke-Haydon 1984), whereas evi-
to develop adult predatory and fighting skills, as denceoflong-termeVectsarealmostnon-existent.
wellasfosteringphysicalstrengthandendurance; Inthispaper,Iusenaturalisticobservationsof
(2) those that regard play as a means of social cheetah,Acinonyxjubatus,cubstoinvestigatethe
bonding and as a way to acquire skills for com- short-term benefits of play using correlational
munication; (3) those that see play as a way of approaches and arguments from design. I focus
increasing individuals’ cognitive and innovative on the first, motor-training hypothesis because
abilities; and (4) those that view play as a means currentevidence,suchasitis,supportsthismore
ofenergyregulation(BekoV&Byers1981;Barber than other adaptive hypotheses for play (Smith
1991). 1982). If play serves as practice for hunting, one
Mosttheoriesconsiderthatthebenefitsofplay might expect particular skills exhibited in play to
are delayed until adulthood (Muller-Schwarze improve with age, because this would provide
1984) but this view stems from observations that increasingly eVective rehearsal for hunting skills.
therearenoobviousbenefitsthatyoungmammals To explore such changes, aspects of play are
derivefromplay.Yetbenefitswouldhavegreater examined in detail focusing on cubs’ ability to
selectiveadvantageiftheyactedearlierratherthan remainconcealed,distancescoveredinplaybouts,
laterinontogenybecauseofthecumulativeeVects and cubs’ success in catching up and contacting
of mortality (Martin & Caro 1985). Moreover, playpartners.
0003–3472/95/020333+13$08.00/0 (cid:63)1995TheAssociationfortheStudyofAnimalBehaviour
333
334 AnimalBehaviour,49,2
First, however, short-term costs of play are Laurenson1993;G.Frame&L.Frame,personal
addressed.Afewstudies(e.g.Martin1984;Miller communication).Cubswithblackmanesandless
& Byers 1991) have attempted to assess the costs than one-quarter of their mother’s height at the
of play to gauge the magnitude of its potential shoulder were estimated as 2 months old; those
benefits but have usually considered only one or with black manes but less than a third of their
twotypesofcost.Ifonlytimeandenergycostsare mother’sheightas3months;thosethatweremore
examined, and are found to be low, while survi- than a third of their mother’s height with fluVy
vorship costs are high, interpretations based on shouldersas4months;thosejustunderhalftheir
the low costs of play will be problematic. Here I mother’sheightas5months;andthosejustabove
attempttoassessallthecostsofplayinonestudy halftheirmother’sheightas6months.Cubsolder
toprovidepreliminarydataontheoverallcostsof than this showed sexual dimorphism. I estimated
playinonespecies. theageofsonsthatweretwo-thirdsanddaughters
Carnivoresarethoughttoplaymoreextensively that were five-eighths of their mother’s height to
than individuals in other orders and, perhaps be 7 months old. If sons were three-quarters or
related to this, there is a large body of literature daughters two-thirds of their mother’s height, I
on carnivore play albeit of a qualitative nature scored them as 8·5 months old; if sons were
(Fagen 1981; BekoV 1989). Cheetahs have been seven-eighthsordaughtersthree-quartersoftheir
noted for their vigorous play (Adamson 1969) mother’sheight,Iscoredtheseas10·5monthsold.
which consists of crouching, stalking, pouncing If sons were as large or larger, or daughters
and chasing (Schaller 1972) and cheetah cubs were seven-eighths or as large as their mothers, I
knockeachotheroverduringplaywiththetypical estimated their age to be 12·5 months or older.
paw slap that is later used to knock prey oV Female cubs in this last age category before
balance (Prater 1935). Popular literature has also independence could be distinguished from their
drawn attention to cheetahs’ rapid and abundant mothersbytheirslighterbuild,fluYermanesand
play (Frame & Frame 1980; Estes 1991), making roundcub-likefaces.Ageingwasfacilitatedifthe
thespeciesapromisingcandidateforinvestigating family contained both sons and daughters but
thefunctionofplay. these criteria were also used in the seven families
inwhichonlyasingleoVspringwaspresent.
In some analyses, I combined the nine age
METHODS classes into three larger categories: cubs 2–4
months old were termed young; 5–7 months old,
StudySiteandObservationSchedule middle-aged; and dependent cubs 8·5 months or
olderwerecalledoldcubs.
The study was conducted on the central plains I conducted behavioural observations without
oftheSerengetiNationalPark,Tanzaniabetween radiotelemetry,anditprovedimpossibletorelo-
March 1980 and December 1983 (for details see cate a family at will a month after a period of
Caro 1994). I made observations on individually observation. Instead, I watched a minimum of
recognized mothers and cubs from a vehicle dur- four diVerent families at each age enabling onto-
ingdaylighthours.Iusuallymadeobservationsat genetic changes in behaviour to be monitored
a distance of 0–150m by eye or with the aid of using a minimum sample size. I observed only
8(cid:35)40 binoculars. I watched families all day for litters of up to four cubs because I could not
1–7consecutivedays;66·7%ofthesewatcheswere recordaccuratelythebehaviourofmorethanfive
4ormoredaysinlength. cheetahssimultaneously,especiallyatkills.Inany
case,littersizesofmorethanfourwereveryrare
in older age categories. In general, rates of play
AgeofCubs
diVeredlittleaccordingtolittersize.
Iobservedlittersthathademergedfromthelair
at nine diVerent ages at approximately 1-month
BellySizeEstimates
intervals. Because the exact birth dates of most
cubs were unknown, I estimated ages of cubs At the start of each day’s observation, I made
accompanyingtheirmotherbasedoncomparison an estimate of each family member’s level of
of body sizes with cubs of known age (following hunger by scoring each member’s belly size on a
Caro:Costsandcorrelatesofplayincheetahs 335
scale from 1 (very emaciated) to 14 (fully TableI.BehaviourpatternscomprisingdiVerenttypesof
extended)whentheywouldvoluntarilyleaveakill playandexplorationofcheetahcubsinthisstudy
if there was still meat on it. Belly size estimates
Typeofplay Behaviourpatterns Recipient
havebeenusedreliablybyotherresearcherswork-
ingoncheetahs(Frame&Frame1981)andlions,
Locomotorplay Boundinggait Norecipient
Panthera leo (Bertram 1978; Packer 1986) and Rushingaround
experienced observers of cheetahs almost always Contactsocialplay Patting Anyfamily
scoredindividualsidentically(seeCaro1987afor Biting member
detailsofinter-observerreliability). Kicking
Grasping
Objectplay Patting Object
Biting
BehaviouralDefinitions
Kicking
Cheetah cubs interacted with each other, with Carrying
their mother and with objects, and often ran Non-contact Stalking* Anyfamily
socialplay Crouching* member
around by themselves in a vigorous, active way
Chasing
which apparently served no immediate purpose.
Fleeing
Interactionswerephysical,orinvolvedchasingor Rearingup
seemingly, hunting, or fleeing from family mem- Exploration SniYng Object
bers. Because the cubs’ activity was apparently
non-functional and was often exaggerated and Definitions: bounding gait: slow run with stiV legs
causingarockingmotion;rushingaround:shortsprint
repeated, it conformed to classical definitions of
often including turns; pat: slap or touch with forepaw;
play (Fagen 1981; Martin & Caro 1985). To bite: close jaws on animal or object; kick: strike with
record play, I observed cubs from the time I first hindfeet; grasp: hold with forepaws or forelegs; carry:
found them until 0930 hours when they began to move with object in mouth; stalk: slow approach with
bodyheldlow;crouch:stationaryposturewithbodylow
rest, and from 1700 hours until dusk. During the
and belly often on ground; chase: run after another
firstminute,Ifocusedattentionononecub,then
animal; flee: run away from another animal; rear up:
switched to the next at the onset of the second forelegsoVtheground;sniV:placenoseclosetoobject.
minute, and so on, eventually returning to the *Crouches and stalks that continued from one cub’s
original cub. I recorded four main categories of focalminutetothenextwerescoredjustonce.
play and one category of exploration (Table I). I
derivedratesofplayforeachcubbysummingthe were discovered as their target would stare at
total number of times it performed all behaviour them intently. Cub activity was fast but the
patterns constituting a particular type of play sequential focal-animal recording technique
(TableI)anddividingitbythenumberofminutes enabledmetoconcentrateononesubjectwithout
thatcubwasactive(i.e.walked,ranorplayed;see beingdistractedbytheactivitiesofothers.
BekoV&Byers1992);Ithencalculatedanaverage At the start of each minute, I estimated the
for all the cubs in the litter (Abbey & Howard distance of the focal cub from its mother. To
1973;Martin&Bateson1986). determine whether play took cubs far from their
Ialsoestimatedthedistanceinmetresthatcubs mother,Idividedthesummeddistancesfromthe
rushedaround,orchasedeachotherduringplay. mother by the number of minutes in which cubs
Although distances were estimated by eye, I kept played, or were active but did not play. I then
my standards high by (1) estimating distances tookanaverageoverallthemorningwatchesfor
betweenobjectsbackatmybaseinSerengeti,then each type of measure. I also noted the mother’s
measuring them and mentally noting the discrep- posture at the start of each minute. These were
ancy and (2) by placing a line of cans at 10-m lying alert: lying with flank and hindquarters on
distances away from my porch that I could view the ground but forelegs tucked under the body;
repeatedly during leisure hours. In addition, I sitting up: sitting on backlegs with forelegs verti-
scored the percentage of chases that ended with cally supporting the body; crouching and stand-
the conspecific actually being contacted, and ing.Theformertwomeasuresrepresentedunease
whethercubswereseenbytheirtargetswhilethey on the part of the mother (Caro 1987a). The
were stalking or crouching at each other or their distance from the mother and her posture at the
motherduringplay.Itwaseasytoseewhencubs start of a minute was a reasonable reflection of
336 AnimalBehaviour,49,2
theplaysituationbecausethelengthofmanyplay Mann–Whitney U-tests or t-tests to determine
bouts were long and had often started before the whether short watches were unrepresentative of
minute under consideration. Finally, I recorded cheetahs’behaviour.IfsignificantdiVerenceswere
eachinstanceofcubsclimbingtrees(i.e.havingall found(P<0·1),Idroppedsingle-daywatchesfrom
feetoVtheground)throughouttheday. subsequentanalysesofthatmeasure.
I recorded the rate at which cubs exhibited Families were observed on 54 occasions, but
bouts of stalking and crouching during hunts of some litters were observed at more than one age
appropriate and inappropriate prey (see Caro (27 once; four twice; five, three times; and one,
1994) and compared these with rates of the same four times). Also some mothers were observed
behaviour patterns seen in play. Cubs were poor more than once either with the same or diVerent
at approaching prey undetected, however, and litters (22 once; five twice; two, three times; and
hence had minimal opportunities to interact four, four times). Previous analyses (Caro 1987a,
physicallywithprey.Thus,Icouldnotdetermine 1990) have examined whether individual diVer-
whether their ability to contact prey improved in ences between mothers were an important source
thecontextofhunts.Nevertheless,thereweretwo ofvariationinmaternalbehaviourbuttherewere
situations in which I witnessed cubs contacting few measures in which significant eVects were
prey: when their mother released live prey for found. This held particularly where sample sizes
them (Caro & Hauser 1992), and when she pre- (andhencereplicates)werereducedafterdropping
sented them with dead prey prior to the family single-day watches. Furthermore, in many non-
feeding.Accordingly,Irecordedthefrequencyof parametrictestsitwasverydiYcuttocontrolfor
contact(i.e.biting,kicking,graspingandpawing) any maternal eVects when examining how cub
with live and dead prey separately for each cub age influenced behaviour because of the uneven
and divided the first value by the time between number of replicate litters or mothers. For all
release and death, and the second value by the three reasons, individual diVerences between
timebetweendeathandbeingeaten.Icouldthen mothersorlitterswerenotinvestigatedhere.
compare the frequency of play seen on a daily
basiswithratesofcontactbehaviourinsituations
when live and dead prey were oVered and thus RESULTS
determine whether diVerences in play were
TheDevelopmentofPlay
reflectedindiVerencesinhuntingskills.
To monitor activity budgets throughout the Timecubsdevotedtoplay
day, I noted the following activities of each
Cheetah cubs that had recently emerged from
cheetahevery15minsincesubjectsrarelychanged
theirlairplayedforanaverageof3·4%oftheday
activities more often than this: resting: lying with
until they became independent. Two-month-old
flank and hindquarters touching the ground;
cubs played for a greater proportion of the day
observing: sitting on backlegs with forelegs verti-
than any other age group (Fig. 1), an average of
cally supporting the body, or standing; moving:
7·6%oftheday,or0·9hinevery12h.Onelitter
walking or running; eating: chewing meat or
playedforover15%oftheday.Thepercentageof
bones; and playing as defined above. Hunting
time cubs spent playing remained high, at an
started when the subject either crouched at,
averageofover5%untiltheywere4monthsold,
stalked,trottedtowards,rushedatorchasedprey.
and then steadily declined with age (Spearman
I also recorded churring, a single soft chirrup or correlation coeYcient, r =(cid:34)0·777, N=41 litters
series of chirrups that mothers used to call their S
watched for 2 or more days, P<0·0001). Never-
cubstothem.
theless, cubs at 8 months of age still played for
2·5%ofthetime,anditwasnotuntiltheywere10
Analyses months old that they played for less than 1% of
theday.
In general, non-parametric statistics were used
in analysis as most data could not be normalized
TimecourseofdiVerenttypesofplay
using standard transformations. For each behav-
iourpatternlistedinTableI,Icomparedwatches Thefourcategoriesofplayallshowedadecline
lasting a single day with longer watches using in frequency during development, in contrast to
Caro:Costsandcorrelatesofplayincheetahs 337
Figure 1.Percentage of 15-min scans that cubs in 41
litters (watched for 2 or more days) were seen playing
plottedagainstcubage;eachpointrepresentsanaverage
forallcubsinalitter.
exploratory behaviour, which rose steadily with
age (Fig. 2; N=43 litters: locomotor play:
r =(cid:34)0·802, P<0·001; contact social play:
S
r =(cid:34)0·738, P<0·001; object play: r =(cid:34)0·467,
S S
P<0·001; non-contact social play: r =(cid:34)0·660,
S
P<0·001; exploration: r =0·320, P=0·018).
S
Whereas locomotor play was at its highest point
at2monthsofageanddeclinedrapidlyfromthen
on,theotherthreeplaycategoriesrosebetween2
and3monthsofage.Thefrequencyofobjectplay
peaked slightly later than contact or non-contact
social play, and as a consequence there was no
significant diVerence between young and middle-
aged litters in object play as there was for other
Figure 2.Running mean values of non-contact social
play categories (Mann–Whitney U-tests compar-
play((cid:47)),contactsocialplay((cid:46)),locomotorplay((cid:45)),
ing the frequencies of play behaviour patterns/
objectplay((cid:44)),andexploratorybehaviour((cid:52))percub
active min/cub for young cubs, N=17 litters, and
per active minute during morning watches plotted
middle-aged cubs, N=12 litters: locomotor play: against cub age. Running means were used to reduce
Xs=0·27,0·08,respectively,U=29,P<0·002;con- variabilitycausedbysmallsamplesizesatsomeagesand
tact social play: Xs=1·25, 0·63, U=36, P<0·002; werecalculatedbytakinganaverageofthescoresfora
non-contact social play: Xs=0·37, 0·19, U=42·5, givenageandthetwoagesoneithersideofit.Numbers
P<0·02; object play: Xs=0·25, 0·16, U=82, oflittersareshownatthetop.
P>0·1).
was lower than at other ages, this loss could be
CostsofPlay attributedtonursingasmuchastoplaying.
Opportunitycosts
Injurycosts
Cubs spent approximately 80% of the time
playing, resting, nursing and moving and this During 2600h of observation, cubs were never
percentage was quite constant across diVerent permanently injured as a result of playing on the
ages.Cubsspenttheother20%ofthedayobserv- ground. Very occasionally a cub would place its
ing, eating and hunting (Fig. 3). Although time footinasmallholeduringaplaychase,andlimp
spentrestinginthefirst3monthsafteremergence briefly for perhaps 10min. In contrast, adults
338 AnimalBehaviour,49,2
not play (Xs=5·1, 4·2m for play versus active
minutes respectively, Wilcoxon test, z=2·114,
N=19 litters, P=0·025). Mothers, however, were
socloseinbothcasesthatitseemedunlikelythat
play could aVect their ability to defend oVspring
against predators. In older, less vulnerable age
groups, the estimated distance from the mother
did not diVer significantly between playing and
active cubs (middle-aged cubs: Xs=9·3, 9·4m,
respectively,z=(cid:34)0·311,N=12litters,P>0·7;old
cubs: Xs=12·9, 16·9m, z=(cid:34)0·075, N=20 litters,
P>0·9). In summary, play did not result in cubs
strayingfarfromtheirmother.
Maternalresponsestopotentialpredationrisk
Locomotor play and non-contact social play
werethemostvisuallyconspicuousformsofplay.
When viewed from afar, they often alerted me to
the fact that a female had oVspring and might
thereforehaveincreasedpredationriskfromlions
and spotted hyaenas, Crocuta crocuta, which are
knowntopreyoncheetahcubs(Caro1987a).
AlthoughIhadnodirectmeasuresofpredation
Figure3.Percentageof15-minscansinwhichcubsin41
risk, I used mothers’ responses to play as an
litters (watched for 2 or more days) were seen to rest
indirect measure. Mothers did not beckon their
( ), nurse ( ), move ( ) and play ( ) plotted against
cubage. cubstoreturntothembychurringmoreoftenin
thoseminuteswhencubswereplayingthanwhen
they were not. In only one out of 31 litters in
wereobservedhobblingmoreseverelyforperiods
whichthemotherchurredatleastonce,didchur-
lastingupto3daysprobablyasaresultofinjuries
ring occur significantly more often during play
sustained during high-speed hunting chases (per-
sonalobservation).InjuriessuVeredinplaythere- minutesthanduringnon-play.
Measuresofmaternaluneasewerenogreaterat
fore appeared much less important than those
thestartofminutesthatincludedplaythanatthe
sustainedbyadultsinnon-playactivities.
start of those in which cubs were simply active
Cubsalsoplayedbyjumpingupontothelimbs
offallentreestolookaroundandtosniV,biteand (N=51 litters averaged over morning watches,
mothers lying alert: Xs=16·5%, 15·5%, Wilcoxon
pat the bough itself. Furthermore, young cubs
test, z=0·169, P>0·8; mothers sitting up: 18·2%,
triedtoascendtheverticaltrunkoflivingtreesin
19·0%, z=(cid:34)0·138, P>0·9), nor did I notice
the same way as leopards, Panthera pardus. The
increased vigilance on the part of mothers when
average rate of tree climbing was 0·06/cub/h over
their cubs played, although this was not scored
the course of development and did not decline
with age (r =(cid:34)0·0142, N=41 litters, P>0·4). systematically. While mothers with young cubs
S spentagreaterproportionoftimecrouchingand
Ascending trees was potentially dangerous
standing at the onset of minutes containing play
becausecubsfellanaverageof18·1%ofthetime,
compared with those when cubs were simply
from as high as 5m; however, I never saw a cub
active (mothers crouching: Xs=2·6%, 0·6%,
injuredthroughfalling.
Wilcoxontest,z=2·429,P=0·015;mothersstand-
ing:11·6%,8·1%,z=2·052,P=0·040)theseusually
Risksofseparation
represented mothers about to join in on their
Young cubs were found significantly further cubs’ play. In summary, play did not provoke
awayfromtheirmothersatthestartofminutesin appreciable maternal unease, suggesting that
whichoneormoreplayboutsoccurredthanatthe cubs did not put themselves at increased risk to
startofminutesinwhichtheywereactivebutdid predatorsduringplay.
Caro:Costsandcorrelatesofplayincheetahs 339
Energycosts TableII.PearsoncorrelationcoeYcientsonrankeddata
comparingratesofdiVerentcategoriesofplaywithrates
Energeticcostsofplaycouldnotbeassessedin ofcontactonliveanddeadprey(averagedacrossprey
this study. Nevertheless, the percentage of time foreachlitter),controllingforcubage
thatlittersplayedwasstronglycorrelatedwiththe
Liveprey Deadprey
percentage of time they spent eating (partial cor-
released presented
relationcoeYcientonrankeddatacontrollingfor Typeofplay (N=15) (N=19)
cub age, r=0·570, N=48 litters, P<0·001)
although these activities were very rarely juxta-
Locomotorplay 0·299 0·084
posed in time. Correlations between mean belly P>0·1 P>0·4
size of litter-mates and proportion of minutes in Objectplay 0·631 (cid:34)0·022
whichcubsplayedeachmorningwerenotsignifi- P=0·003 P>0·4
Contactsocialplay 0·566 0·088
cant, however, based on the 21 litters in which
P=0·009 P>0·3
cubs were watched on 6 or 7 mornings. This was Non-contactsocialplay 0·293 (cid:34)0·192
becausecubswithlargebellies,ofsize8orabove, P>0·1 P>0·2
played comparatively little, possibly because they
were uncomfortable running or rolling around Nreferstothenumberoflitters.
when their bellies were stretched. Thus, better
nourishedoVspringplayedmorebutonlyafterthe
in close proximity. Only an average of 24·4% of
eVectsofabigmealhadwornoV.
play stalks (se=5·3, N=23 litters) and 20·3% of
play crouches (se=4·1, N=33 litters) remained
AssociationsbetweenPlayandPredatory undiscoveredbytargetfamilymembersandthese
Behaviour proportions did not alter with cub age (stalk:
r =0·086, P>0·3; crouch: r =0·024, P>0·4). In
In those litters in which cubs exhibited higher S S
contrast, an average ((cid:38)se) of 60·8(cid:38)11·8% of
rates of stalking and crouching at other family
crouches at prey (N=14 litters over 4 months of
members during non-contact social play, cubs
age, as this was the first time cubs crouched in
respectively stalked and crouched at prey more
hunts, and excluding litters in which only one
often (partial correlation coeYcient on ranked
crouch occurred) remained undiscovered as prey
data controlling for cub age, stalk: r=0·240,
wasfurtherawaythanfamilymembers,andcubs
N=51 litters, P=0·044; crouch: r=0·237, N=51
showed an age-related improvement in keeping
litters, P=0·044). There was, however, no signifi-
concealed while crouching at prey (r =0·447,
cant association between rushing during locomo- S
P=0·055). Stalking prey, however, still appeared
tor play, and chasing during non-contact social
diYcult because a high proportion of stalks were
play,andthesamebehaviourpatternswhilehunt-
detected by prey (67·1%, se=14·6, N=22 litters
ing (rush: r=0·050, N=37 litters, P>0·3; chase:
excludingthoseinwhichonlyonestalkoccurred)
r=0·127, N=51 litters, P>0·1). Litters that
andcubsdidnotgetappreciablybetteratstalking
showed higher total rates of object play, and
preyundetected(r =0·151,P>0·2).
contactsocialplay,exhibitedhighertotalratesof S
patting,bitingandgraspinglivepreyreleasedfor
them by their mothers (Table II). In contrast, Distancescoveredduringplayandhunting
ratesoflocomotorandnon-contactsocialplayin
Theestimateddistanceoverwhichcubschased
cheetahs were not significantly correlated with
each other (X=7·8m, se=0·5, N=44 litters
rates of contact of live prey. No category of play
excludingthoseinwhichonlyonechaseoccurred)
was significantly correlated with contact rates on
increased with age (r =0·574, P<0·001). It seems
deadpreypriortofeeding(TableII). S
unlikelythatgreaterdistancesweresimplyacon-
sequence of older cubs’ greater stamina because
AgeChangesinSubtleAspectsofSocialPlay estimated distances covered during bouts of
rushing around (X=6·3m, se=0·5, N=29 litters
Remainingconcealedduringplayandhunting
excludingthoseinwhichonlyonerushoccurred)
It was diYcult for cubs to remain concealed did not increase during ontogeny (r =(cid:34)0·006,
S
fromeachotherwhileplayingbecausetheystayed P>0·4). Increasing distances covered in play
340 AnimalBehaviour,49,2
Table III. Summary of subtle changes in non-contact
socialplaypresentedinthetext
Changeswithageinrelationto
Play Prey
Remainingconcealed
Stalking NoeVect NoeVect
Crouching NoeVect Increases
Distancescovered
Rushingaround NoeVect Notapplicable
Chasing Increases Increases
Successofchases
Contacting Increases Increases
Knocksover Decreases Tooinfrequent
tomeasure
Figure 4.Mean ((cid:38)se) percentage of play chases that contacts made at the end of play chases, the
resulted in cubs contacting (patting or grasping) either percentage of occasions that a family target was
theirmotherorsiblingplottedagainstcubage.Number knocked over after being patted or grasped by a
oflittersareshownatthetop.
youngsteractuallydeclinedwithcubage,presum-
ably because cubs put more eVort into getting
away, and were better at keeping their balance
chases mirrored the increasing distance that cubs
(r =(cid:34)0·387, N=41 litters, P=0·006 excluding
chased prey as they grew older (X=23·3m, S
se=5·1, N=33 litters, r =0·540, P=0·001 exclud- litters in which only one contact occurred). It
S seemed unlikely, therefore, that attempting to
ing litters in which only one chase occurred).
topple relatives in play provided helpful experi-
Becauseopportunitiesforplaywerevastlygreater
ence for bringing down prey, despite Prater’s
thanthoseforhuntingprey,distancescubschased
(1935) observations. These subtle aspects of
eachotherinplaymostlikelyrehearsedtheshort-
play and hunting behaviour are summarized in
distance sprints necessary to catch quarry rather
TableIII.
thanviceversa.
Measuresofsuccessinplay DISCUSSION
The proportion of chases in which a cub con-
TheDevelopmentofPlay
tacted(i.e.pattedorgrasped)afamilymemberat
the end of a play chase rose with age (r =0·307, Theaverageamountoftimespentplayingafter
S
N=43 litters, P=0·023 excluding litters in which emergence,3·4%oftheday,probablyrepresented
only one chase occurred; Fig. 4). Similarly, the theaveragepercentageoftimespentplayingdur-
proportion of occasions that cubs contacted live ing the whole period of dependence because,
prey after it had been released for them by their before 2 months of age, cubs had poorly devel-
mothers increased slightly as cubs grew older oped motor skills and were probably asleep dur-
(X=88·8% success, r =0·360, N=16 litters, ingmuchoftheirmother’slongabsencesfromthe
S
P=0·086)suggesting,perhaps,thatcontactingsib- lair (K. Laurenson, personal communication).
lings at the end of play chases might have served This figure is comparable to values from field
as practice for contacting live prey. However, studies of other carnivores, as well as ungulates
contactingcheetahsandlivepreywerenotsignifi- andprimates.Forexample,Schaller(1972)found
cantly correlated once the eVect of age was thatthreelioncubgroupsplayedfor1·5,1·6and
removed (partial correlation coeYcient control- 6·0% of the day, although their ages were not
ling for cub age, r=0·181, N=15 litters, P>0·2 specified.Miller&Byers(1991)showedthatplay
controllingforcubage).Finally,consideringonly represented 1–2% of the total time budget in
Caro:Costsandcorrelatesofplayincheetahs 341
pronghorn, Antilocapra americana, fawns. Free- species in which a similar developmental pattern
livingprimatesplaybetween1and20%oftheday of play has been reported (bighorn lambs, Ovis
(e.g. 3–14% for red colobus, Colobus badius: canadensis:Berger1980;gazellefawns:Gomendio
Clutton-Brock 1974; 3 or 20% for olive baboons, 1988;fursealpups:Harcourt1991a).
Papio anubis: Rose 1977 and Nash 1978, respec- Incheetahs,objectplaydevelopedmoreslowly
tively;3–5%forchacmababoons,Papiocynoceph- than social play, similar to domestic kittens in
alus: Cheney 1978; and 1–6% for rhesus which object play continues to rise after the
macaques, Macaca mulatta: Levy 1979) although seventh week of development, while cat contact
thesevaluesarenotnecessarilycomparablegiven and non-contact social play patterns such as rear
widely divergent methods of data collection and andarchfall(Bateson&Young1981;butseealso
calculation. Thus cheetahs did not play for an Caro 1981). In domestic cats, it has been argued
exceptionally greater percentage of time than thatthesediVerenttrajectoriescouldbelinkedto
other free-living species. Earlier reports of kittens gaining social skills by playing with sib-
cheetahs’ playfulness may have derived from lingsinthenest,andthenacquiringknowledgeof
cheetahs’conspicuousnessinopenareasandtheir their inanimate environment and prey through
diurnalhabits. objectplayatatimewhenkittensaresupposedto
DiVerent types of cheetahs’ play had distinct have left the nest (Bateson 1981). In cheetahs,
ratesofdevelopmentasreportedforotherspecies however, these arguments are unlikely to apply
(domestic cats, Felis domesticus: Barrett & because object play peaked 2 months after cubs
Bateson 1978; olive baboons: Chalmers 1980; had left their lair. In the intervening period, cubs
Cuvier’sgazelles,Gazellacuvieri:Gomendio1988; hadtheopportunitytoexperiencetheirimmediate
southAmericanfurseals,Arctocephalusaustralis; environment, had watched prey from afar, and
Harcourt 1991a). DiVerent types of play may had interacted with dead prey captured for them
come under the influence of several diVerent by their mothers. It therefore seems improbable
motivational systems as individuals mature that object play promoted acquisition of knowl-
(Caro1981),anddiVerentcomponentsmayserve edge about their environment. More likely,
diVerent functions (Bateson 1981; Gomendio increasing rates of exploratory behaviour seen
1988). All these studies suggest that play is not a during development enabled cubs to become
unitary category with regard to its development, betteracquaintedwiththeirsurroundingsasthey
causationorfunction(seealsoPellis1991). grewolder.
In the past, locomotor play in juvenile mam-
mals has been regarded as enhancing physical
CostsofPlay
stamina and motor skills of adults (BekoV &
Byers 1981). If play has energetic or injury costs, Typically, young cubs would be nursing at
however,selectionoughttodelaypractisingskills dawn when I found them (see also Laurenson
foradulthooduntiljuvenilesbecomestrongerand 1993)butstartedcontactplay,eitherontopof,or
less vulnerable. Therefore if we see play early in within1moftheirmotherataround0730hours.
development it suggests either negligible costs or The mother would rest until 0800 or 0815 hours
that play is needed to rehearse skills required and then move oV, followed by her cubs, which
during juvenile stages. In cheetahs, rates of loco- might continue to play intermittently until 0900
motorplaywerehighestbetween2and4months hours, although this was highly variable. Young
ofage,atatimewhenpredator-inducedmortality cubs sometimes also played between 1200 and
isextremelyhigh(Laurenson,inpress).Iflocomo- 1300 hours and again between 1730 and 1900
tor play has immediate benefits by reducing the hours while their mother was resting, suggesting
period of time that cubs are vulnerable to pred- thattheytoowouldhaverestedintheabsenceof
ators, this could explain why locomotor play play.Asplayoftenstartedattheendofaboutof
occurs so early in development, even when cubs restingorsuckling,Isuggestthatyoungcubswere
are temporarily jeopardized during locomotor notdeficientineitheroftheseactivitiesasaresult
performance(seebelow).Thisargument,basedon of play. OVspring aged 5–7 months would ordi-
design, suggests that locomotor play could be narilyplayinthemornings,andsometimesinthe
instrumental in developing an adequate flight evenings, usually while the family was walking.
responseinjuvenilesandaddstoagrowinglistof Here, moving was not displaced by play because
342 AnimalBehaviour,49,2
cubscouldkeepuporevenaheadoftheirmother wasitsmother,whichwasalwaysclosebyduring
through locomotor activity or non-contact social play.
play. These arguments are speculative but they Energy costs of play were not assessed in this
suggestthattimecostsofplaymayhavebeenlow. study but energy expended during play has been
Playing cubs suVered only minor damage to estimated for other species. Play in free-living
their feet or legs, which aVected them for only a pronghornfawnstookup3%oftotaldailyenergy
few minutes. Other field studies have demon- expenditureexcludinggrowth,and20%ofenergy
strated that play can result in a diverse set of expenditure in excess of resting metabolism and
injuries including falling (chimpanzees, Pan growth (Miller & Byers 1991). In 10-week-old
trogolodytes: van-Lawick Goodall 1968), being laboratoryreareddomestickittens,Martin(1984)
trapped in mud (elephants, Loxondata africana: found that the energetic costs of play accounted
Douglas-Hamilton & Douglas-Hamilton 1975), for 4–9% of total daily energy expenditure,
being washed out to sea (Galapagos fur seals, excludinggrowth.Similarly,Siviy&Atrens(1992)
Arctocephalus galapagoensis: Arnold & Trillmich found that play in domestic rats, Rattus norvegi-
1985), or being impaled on the spines of cacti cus, accounted for 2–3% of the total energy bud-
(bighorn sheep: Berger 1980). Nevertheless, the get, assuming a juvenile spends 3% of the day
extent of such injuries during individual onto- playing. As cheetah cubs spent less time playing
geniesandacrossthesepopulationswasnotdocu- thankittensandanequivalenttimetoratpups,it
mented and these incidents might have been is reasonable to argue that play in cheetahs
unusual, attracting observers’ undue attention. It accountedforanabsolutemaximumofbetween5
wouldbeinstructivetocarryoutsystematicobser- and10%oftotaldailyenergyexpenditureevenin
vations on juvenile ungulates in mountainous young cubs where non-contact and locomotor
regions,andonarborealprimatesbecausereports playwereattheirzenith.
emphasize the special risks of falling in play (e.g. A10%lossinenergyexpenditurewouldreduce
Welles&Welles1961;Budnitz&Dainis1975)but tissue growth in the short term (Miller & Byers
cheetahs were not subject to these risks most of 1991) but this might not aVect juvenile survival
thetime. undulybecausepredationwastheprincipalcause
Playmayhavemadecubsmoreconspicuousto ofmortalityincheetahcubs(Laurenson,inpress).
predators since it attracted my attention. Unfor- Moreover, a 10% loss of energy for a healthy
tunately, it was very diYcult to determine the individual may be small compared with a 30%
exact moment predators saw a cheetah family, averageoftotalmetabolizableenergyintakeused
sinceIwasnearthelatter.Therefore,Icouldnot in growth (Martin 1984); consequently, energy
test whether play specifically attracted predators’ costs of play in healthy cheetahs may not have
attention.Nevertheless,mothersshowedlittleevi- been overly large. In sick cubs, however, a 10%
dence of unease while their cubs were playing, loss was probably substantial: an ill 8-month-old
suggesting it did not increase risk of predation female cub showed no signs of play at all during
unduly. thefourmorningsandeveningsbeforedying.
In a recent study, Harcourt (1991b) showed Before concluding that the costs of play to
that animals were at risk to predators because cheetah cubs are trivial, eVects of play on other
play distracted them. He saw 26 south American indispensible family members need be considered
fur seal pups caught and killed by southern sea (Caro1987b).ThemostobviousindirecteVectof
lions,Otariabryonia,inthewild,22ofwhichwere cubplaywasonmaternalhuntingsuccess.Outof
playing at the time they were captured. Because 653 mothers’ hunts that I saw, 478 failed. Seven
pups played for only 6·1% of the time, survivor- ofthesefailures(1·5%)wereunequivocallydueto
ship costs of play were extremely high in this prey being alerted by seeing the cubs play (Caro
species.Harcourtinterpretedthehighmortalityas 1987b). For example, young cubs sometimes
resulting from pups being distracted during play clambered over their mother when she crouched
and failing to join the flight of non-playing con- or sat up to look at prey between bouts of
specifics, rather than play attracting attention as stalking, and older cubs went on chasing each
posedforcheetahs.Distractionwasunlikelytobe otheraftertheirmotherhadcommencedherstalk.
an important consequence of play in cheetahs As cubs caused a minimum of 78 hunts to fail,
becauseacub’sprimarydefenceagainstpredators playperseaccountedfor9·0%ofthesefailures.