Download Mammalian Play: Training for the Unexpected Author(s): Marek

Mammalian Play: Training for the Unexpected
Author(s): Marek Spinka, Ruth C. Newberry and Marc Bekoff
Source: The Quarterly Review of Biology, Vol. 76, No. 2 (Jun., 2001), pp. 141-168
Published by: The University of Chicago Press
Stable URL: http://www.jstor.org/stable/2664002
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VOLUME
76, No. 2
JUNE
THE QUARTERLY
REVIEW
of BIJOLOGY
MAMMALIAN PLAY: TRAINING FOR THE UNEXPECTED
MAREK SPINKA
EthologyGroup, Research InstituteofAnimal Production
CZ-104 01 Prague-Uhffneves,Czech Republic
E-MAIL:
[email protected]
RUTH C. NEWBERRY
CenterfortheStudy ofAnimal Welfare,WashingtonState University
Pullman, Washington 99164-6520 USA
E-MAIL:
[email protected]
MARC BEKOFF
DepartmentofEnvironmental,Population, and Organismic Biology, Universityof Colorado
Boulder, Colorado 80309-0334 USA
E-MAIL:
[email protected]
ABSTRACT
In thisreview,
wepresenta newconceptualframeworkfor
thestudyofplaybehavior,
a hitherto
puzzlingarrayofseemingly
and unrelatedbehavioralelements
thatarerecognizable
purposeless
as play throughout
themammalianlineage.Our majornewfunctionalhypothesis
is thatplay
enablesanimals to developflexiblekinematicand emotionalresponses
to unexpected
eventsin
a suddenlossofcontrol.
whichthey
weproposethatplayfunctions
toincrease
experience
Specifically,
theversatility
usedtorecoverfrom
suddenshockssuchas lossofbalanceandfalling
ofmovements
withunexpected
situations.
stressful
over,and toenhancetheabilityofanimalstocopeemotionally
" we suggestthatanimals activelyseekand create
To obtainthis "training
for theunexpected,
situationsin play through
unexpected
thatis, deliberately
self-handicapping;
relaxingcontrol
overtheirmovements
oractively
intodisadvantageous
puttingthemselves
positionsand situations.
in whichtheplayers
switch
between
moveThus,playis comprised
ofsequences
well-controlled
rapidly
The Quarterly
ReviewofBiology,
June 2001, Vol. 76, No. 2
of Chicago. All rightsreserved.
Copyright? 2001 by The University
0033-5770/2001/7602-0001$02.00
141
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2001
142
THE QUARTERLY REVIEW OF BIOLOGY
VOLUME
76
movements
thatresult
mentssimilarto thoseused in "serious"behaviorand self-handicapping
between
in-control
and outin temporary
lossofcontrol.Weproposethatthisplayfulswitching
elements
is cognitively
and ontogenetic
constraints
on
demanding,setting
phylogenetic
of-control
emotional
state
responses
thatproducea complex
play,and is underlainbyneuroendocrinological
weproposethatplay is often
prompted
byrelatively
novel
knownas "havingfun."Furthermore,
Wepresent
from,exploration.
orunpredictable
stimuli,and is thusrelatedto,althoughdistinct
examiningtheextenttowhichthey
24 predictions
thatarisefromournewtheoreticalframework,
evidenceand contrasting
themwiththepredictions
offour
empirical
aresupported
bytheexisting
" hypotheaboutplay. Wearguethatour "trainingfor
theunexpected
majoralternative
hypotheses
structural,motivational,
emotional,
sis can accountfor somepreviously
puzzlingkinematic,
a diversity
and phylogenetic
aspectsofplay.It mayalso accountfor
cognitive,
social,ontogenetic,
misfortunes.
ofindividualmethods
forcopingwithunexpected
A
forthosewho ethologistsagree in their classificationof beMAJORAREAofinterest
study "play behavior" centers on the
questions: Why and how has play behavior
evolved, and how has it been maintained in
populations of differentspecies bynatural selection (Bekoffand Byers1998; Power 2000)?
There has been little success in achieving a
generallyvalid and empiricallysupported answerto thesequestions.The extensivevariabilityof play patternssuggeststo some researchers that play may serve differentfunctionsin
animals of different
species,and in individuals
of differentages and sex withinthe same species (Gomendio 1988; Bekoffand Byers1998;
Pellegriniand Smith1998). Some authorseven
think that attemptsto find a single function
for all play behavior are doomed to failure.
For instance,Burghardt(1998a) regardsplay
as almost certainlya "heterogeneous category
linked togetherby characteristicsthatmaybe
superficiallysimilar,but have separate origins,
causes, functions,and ontogenies" (p 22).
While a pluralistic approach may be the
mostappropriatewayto tacklequestionsabout
the specific functions of differentmodes of
play, the implication that no comprehensive
understandingof playis possible is discouraging. If play is a heterogeneous categorywith
neither a traceable phylogenetic root nor a
common function,then whystudyit as a general phenomenon? Would it not be better to
tryto splitit into smaller homogeneous categories? Should we, in the end, treatplayjust
on a case-by-casebasis?
There are tworeasons to rejectthisposition.
First,playbehavior patterns,as diverseas they
mightbe, do have featuresin common (Fagen
1981; Burghardt1984; Bekoffand Byers1998).
In most cases, both novice and professional
havior as either play or nonplay (e.g., Rasa
1984). It is easier to see the unityof play than
to find any clear natural borders withinthe
richness of play that could be used to split it
into more manageable categories. Second,
playis nearlyubiquitous in all mammalian orders. This suggestseithera common ancestry
or a similarsetofselectionpressuresthatacted
in all divergingmammalian orders in the Cenozoic (Byers 1984). In our view, it is more
parsimonious to assume that there is a basic
phylogeneticand functionalunityunderlying
mammalian play than to assume thatthe "superficiallysimilar"playpatternswidelydistributed in mammalsevolvedindependendymany
times during mammalian phylogeny.Hence
the search fora major functionof play seems
to be justifiedand important,as it is forother
widelydistributedmammalian characteristics
such as sleep (Tobler 1995).
In this paper, we propose a major new hypothesis about the adaptive value of play behavior,withrelated structural,psychological,
and cognitiveconstituents.We followwith a
set of testablepredictions thatarise fromthis
theoreticalframework.
We then examine some
previous hypothesesabout the function(s) of
play, contrastingtheir performance against
thatof our new hypothesis,based on how parsimoniouslyand consistentlyeach hypothesis
accounts for the available empirical information on mammalian play. We argue that our
hypothesiscan account for some well-documented kinematic, structural,motivational,
emotional, cognitive,social, ontogenetic,and
phylogeneticaspects of play.
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JUNE
MAMMALIAN PLAY
2001
THE "TRAINING
FOR THE UNEXPECTED"
HYPOTHESIS
OF PLAY
THE ADAPTIVE VALUE OF PLAY
We hypothesizethata major ancestralfunctionofplayis to rehearsebehavioralsequences
in which animals lose full control over their
locomotion,position,or sensory/spatialinput
and need to regain thesefacultiesquickly.Animals learn how to improvisetheirbehavior by
chaining conventional movementswithatypical movementsto get themselvesback into a
standard position. Sequences thatlink highly
efficientspecies-typicalmotor patterns and
standard body positions with atypical movements necessary for recoveryfrom awkward
positions often occur in biologically significant situations.For example, when fleeing a
predator,an animal triesto use the most efficient patternof flight,but maybe disoriented
or interruptedunpredictablyby rapid changes
in visualinput,actions of the predator,or collisionswithother herd membersor inanimate
obstacles. The abilityof the animal to recover
rapidlyusing atypicalmovementscould mean
the differencebetween life and death in a
predator attack. Similar mishaps may occur
during intraspecificinteractionsand during
pursuit of prey.The opponent (or the prey)
adds significantunpredictabilityto the environment.Skilled movementsoftencannot be
completed or properlysequenced because of
interruptionby the other animal.
Besides the development of locomotor versatilityin unanticipated situations,we hypothesize that animals in play learn how to deal
with the emotional aspect of being surprised
or temporarilydisoriented or disabled. Loss
of controlin a serious situation,despite active
attemptsto cope, willnormallyresultin activationofbothsympathetico-adrenomedullary
and
pituitary-adrenocorticalsystems (von Holst
1998). These systemsprepare the animal for
immediate action, but can have long-term
costs, especially in suppressed immunocompetence (Apanius 1998). In adversesocial situations,emotional overreactionmaylead to undue escalation of conflicts.In the presence of
a predator,emotional overreactionleading to
aimlesspanic willdecrease an animal's chance
of survival.In general, adaptive responses in
serious situationsdepend upon the animal's
143
ability to avoid incapacitation via negative
emotions. We propose thatthe experience of
"self-induced"mishaps during play helps animals to avoid emotional overreactionduring
unexpected stressfulsituations.
The ultimate benefits obtained from play
are probably low,judging from the fact that
playis dropped fromthe behavioral timebudget under harsh conditions (Baldwin and Baldwin 1974; Berger 1980; Barrettet al. 1992).
However,itmaybe thatindividualdifferences
in retainingplayduringharsh timeswere beneficial during evolution. All in all, play could
probablybe counted among "opportunitybehaviors"(a termcoined byFraserand Duncan
1998); that is, those behaviors thatbring low
ultimatebenefitand are thereforeactuated at
moments when the cost of performingthem
drops to an even lower level.
In short,we propose that play: (i) results
in increased versatility
of movementsused to
recover from sudden "gravitational,""kinematic," or "positional" shocks such as losing
ground underfoot,fallingover,being knocked
over,being pinned down,or being shaken vigorously; and (ii) enhances the abilityof animals to cope emotionallywithunexpected situations. These mayinclude both "locomotor"
shocks as described above, and "psychological" shocks such as suddenlybeing faced with
frighteningor dangerous stimuli,unexpectedly meeting a stranger,or experiencing a
sudden reversalin dominance.
SELF-HANDICAPPING-SEEKING
AND
CREATING THE UNEXPECTED
IN PLAY
If play has the functionof trainingfor the
unexpected,thenunforeseensituationsshould
occur frequendyin play.We suggestthatmammalsactivelyseek and createunexpected situations in play. Specifically,we propose that
mammalian playis a sequential mixtureof: (a)
well-controlled vigorous locomotor movementssimilarto those used in "serious"behavior that load heavilyon fitnesstraitssuch as
escape frompredators,intraspecificagonism,
or hunting fast or dangerous prey; and (b)
movements during which postural control is
compromised, or the chance forrandom factors to influence movement is increased so
that the animal is more likelyto be knocked
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THE QUARTERLY REVIEW OF BIOLOGY
144
offbalance, fallover,lose controlof a play ob
ject, or fail to counter the actions of another
animal.
Animals can activelyseek and create unexpected events in play through self-handicapping; thatis,deliberatelyrelaxingcontrolover
their movements or activelyputting themselvesinto disadvantageouspositionsand situations. For example, animals may self-handicap by moving in a way that is less than fully
or byperformingobject mastable or efficient,
nipulation while positioned in a waynot best
suited for full control over the object. They
may also impair theirsensoryand spatial orientation throughhigh-speed angular and rotatorymovements of the head, puttingtheir
head into unusual positionsin relationto gravityor horizon, or twistingtheirbody in an unusual way.By using physicalpropertiesof the
environmentsuch as deep softsnow,a slippery
water, animals
slope, or gravity-attenuating
can enhance the probabilitythat theywill be
thrown off balance into unusual positions.
They can also increase the probabilityofexperiencingunexpected eventsbyplayingwithor
among relativelynovel environmentalfeatures
or among featuresthat are moving in unpredictable ways (e.g., due to wind). In social interactions,animals can self-handicapbyusing
positions and movements that impair their
competitiveabilityand enable theirplaymates
to gain the "attack" position. For example,
theymay inhibit the force of their bites and
pushes, and allow themselves to be pushed
overand chased, even when theyhave the abilityto harm or dominate a playmate.They may
also put themselvesat a self-induceddisadvantage byplayingwithlarger,stronger,or more
experienced play partners,or even with animals ofa different
species. Because playis only
performed when its costs remain low, however,there is an upper limitof unpredictabilityand loss ofcontrolabove whichanimalswill
not play.
THE RELATIONSHIP
EXPLORATION
BETWEEN
AND PLAY
Explorationcan be viewedas a seriouscounterpartto play. During an initial encounter
with a novel environmentalfeature,animals
firstinvestigateit through "serious" exploration, examining whetherit is dangerous and
VOLUME
76
whetherit has any resource value to them. If
theyfindthenovel featureto be relativelynonthreatening,play may follow. Through their
playfulbehavior the animals seem to address
the question, "What if it reallywere dangerous?" Although exploration is often temporallyassociated withplay, it differsfromplay
in three importantaspects. First,a function
of exploration may be to learn how to avoid
getting into trouble (by gathering information), whereas we propose that an important
aim ofplayis to learn how to get out of trouble
(throughenhanced improvisationskills).Second, there is no deliberate self-handicapping
in exploration. Third, whereas play is associated witha relativelyrelaxed and secure state,
exploration is more closely associated with
fear and perceived danger. If an animal loses
recontrolin play and has too much difficulty
gaining it, or the situation becomes dangerous, the animal should withdrawand reassess
the situationthroughfurtherexploration.
HAVING FUN-THE
EMOTION
UNDERLYING
IN PLAY
playenables aniAccordingtoour hypothesis,
byrehearsmals to develop emotionalflexibility
ing the emotional aspect ofbeing surprisedor
temporarily
disorientatedor disabled.Although
unexpected events thatoccur in a dangerous
in inexperisituationwould likelymagnifyfear
enced animals, we suggest that fear is modulated in play by the relativelysafe context in
which play occurs and the improbabilitythat
losing controlwillhave serious consequences.
In addition, regaining control following an
unexpected challengeis likelyto be rewarding,
and the positivenature of thisexperience may
be intensifiedby the rapid repetition of incontrol and out-of-controlelements that occur in play. Thus, we hypothesizethat play is
emotionally exciting(perhaps even thrilling,
thoughnot intenselyfrightening)and rewardwhile at the same
ing,maybe even pleasurable,
timebeing relaxed.
We suggestthatthiscombination of affectiveattributesis unique to play,
producing the complex emotional state that
is referredto as "havingfun" in human folk
psychology.We propose that the three phenomenological aspects of this "having fun"
feelingare directlyreflectedin the kinematic,
structural,and motivationalcharacterof play
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JUNE
MAMMALIAN PLAY
2001
behavior. The excitement is revealed in the
vigor and speed of play movements and sequences, thepleasurable aspect in thefactthat
animals activelyseek out and workforopportunitiesto play,and the relaxationby the willingnessofanimals to self-handicapin playand
play only when theyare relativelysafe or unstressed. It may also be that play behavior is
supported by a unique pattern of neurobiological response in the brain centers associated with complex somatosensation, motor
patterncontrol,emotionality,and reward.
RICH COGNITIVE
CONTENT OF PLAY
145
locomotion, increased speed ofbalance recoveryand heightened abilityto regain fullorientation aftera collision or fall; in agonistic behavior,knowledge to avoid undue escalation,
fasterconflictresolution, and fewerinjuries
sustained;in predator-preyinteractions,more
effectiveevasive movements in response to
movementsofthepredator,decreased chance
of panic and collision withobstacles, and increased chances of escape; in response to
novel physicalfeaturesin the environment,a
shorterlatencyto shiftfromfreezingto exploration and then to play (exploiting or ignoring the feature); and when encounteringunexpected situationsin a serious context,a less
pronounced physiological stress responseespeciallyin relation to the chronic elevation
of adrenal glucocorticoidsand compromised
immunocompetence.
Prediction 2: The benefitfromplaytowards
increased locomotorversatility
when handling
unexpected eventsis mostpronounced within
the currentphase of ontogeny,whereasthe improved abilityto cope emotionallywithunexcan be both immediateand
pected misfortunes
long lasting.Withongoing development,body
proportions and locomotor abilities change
and the body movement strategiesthat have
been rehearsed earlier may no longer be applicable. By contrast,there is no obvious reason whyincreasedemotionalflexibility
resulting
fromplaywould disappearwithincreasingage.
During play,rapid alternationbetweencontrolledand uncontrolled actions requires frequent and rapid assessmentand reassessment
of qualitativelydifferentsituationsthatdo not
normallyfolloweach other. This implies that
playis,even when a solitarylocomotor activity,
a cognitively
demandingactivity(Allen and Bekoff1997; Bekoffand Allen 1998). When (unpredictable) social interactionis involved,the
movements,their sequencing, and, presumably,the accompanyingmental statesbecome
even more complicated because theplaymates
change the situation with their everyaction.
Moreover, the abilityto experience the complex feeling of "having fun" may require a
richlydeveloped cognitivesystem.Hence, our
functional hypothesisabout play as training
forthe unexpected implies that,though such
trainingmightbe advantageous formanyanimals,playevolvedonlyin thosewiththe requiKINEMATICS AND STRUCTURE OF PLAY
site cognitivecapacity.Also, the level of cogniPrediction 3: Self-handicappingactions are
tivefunctionneeded forplay may set a lower
ubiquitous elementsofplaythatfrequentlyrelimiton the stageofontogeneticdevelopment
sult in temporaryloss of control. That is, play
at which play firstappears.
sequences in which an apparentlyself-handicapping action is followed immediately by
PREDICTIONS
being knocked offbalance, slipping, falling,
FUNCTIONAL CONSEQUENCES OF PLAY
sliding, rolling over, losing control of a play
Prediction 1: The amount of play experi- object, or losing the "attack" orientation toence obtained affectsthe abilityto physically ward another animal are frequent. This preand emotionally handle unexpected events diction followsfromour hypothesisthat aniand temporaryhandicaps. Animals deprived mals benefitfromplaybylearninghow to cope
ofplay,be itbynaturalcircumstancesor artifi- withsudden losses of control.
Prediction 4: Play is sequentially variable.
cial manipulation,willbe less able to deal with
such situations. Conversely, animals stimu- Play movements that closely resemble those
lated into higher-than-usualamounts of play used in "serious" behavior such as predation,
willsurpass othersin theirabilityto cope with aggression, or escape are interspersed with
such situations.Evidence of improvedcoping other movementsthatare seeminglycountermay include one or more of the following:in productive towards achieving the proximate
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146
THE QUARTERLY REVIEW OF BIOLOGY
goal ofthe "serious"behavior.In addition,elements usuallyperformedin differentmotivational contextsmayfolloweach other in rapid
succession during a play bout. This predicted
variabilityis derived fromour hypothesisthat
playenables animals to rehearse how to regain
controlafterunexpected interruptionsofnormal behavioral sequences.
Prediction 5: Under favorable conditions,
mammals of differentspecies are able to play
with each other, or at least stimulate each
other to play. This prediction arises because
certain common features of play, like performingvigorousrotationalmovements,moving body parts in the frontalplane, assuming
asymmetrical positions, and switching betweenhighlyskilledand deliberatelyawkward
movements,are universaland should be recognized by individualsof differentspecies.
SOCIAL ASPECTS OF PLAY
Prediction 6: Animalspreferto playwithfamiliarconspecificsover unfamiliarconspecifics, even if the latter are better matched in
terms of body size. This is because play involves self-handicapping,which is vulnerable
to cheating in animals thatdo not interactrepeatedlywitheach other.
Prediction 7: Among pairs of familiarconin bodysize or expespecificsthatdifferwidely
rience, play is more often initiated by the
smalleror less experienced partner.This predictionis derivedfromthe hypothesisthatthe
much smaller or less experienced individual
willgain a benefitfromthe experience of copingwithbeing at a disadvantagein the interaction. However,ifthe much largeror more experienced animal is unable to self-handicap
sufficiently-tolose some controland experience something unexpected from the movements of the playmate-it should terminate
the interactionor fail to respond to attempts
by the other individual to initiateplay.
Prediction 8: When the strengthor dominance statusof twoplay partnerschanges, the
relative degree of self-handicappingby the
twoindividualschanges. The strongerindividual will usually performthe most self-handicapping. This is because the main functionof
play is to train for the unexpected, not to
achieve dominance over,or predate, the playmate.
VOLUME
76
Prediction 9: Play is contagious and more
than two animals often interact simultaneously with each other in play. There are two
reasons forthisprediction. First,conspecifics
at play bring much unpredictabilityinto the
environment,increasing the number of opportunitiesto respond to unexpected situations.Second, an animal's assessmentthatthe
safe to encurrentenvironmentis sufficiently
gage in play is strengthenedby the fact that
other animals have already startedto play.
Prediction 10: Play signals-elements that
promote the initiationor continuationof play
interaction between two.or more animalsare often derived fromself-handicappingactionsused in play.This predictionarisesfrom
our functionalhypothesisthat play involving
conspecifics originallyserved as a lesson in
how to regain control in social and predatorprey interactions; thus play necessarily included vigorous species-typicalactions that,
when performedin a serious manner, would
pose a serious threator even immediate danger to the recipient. Hence, for play to be reciprocated, it would have been necessary to
informthe recipient thatthese actions would
be performedin a nonharmfulmanner. The
self-handicappingmovements and positions
used to practice for awkwardsituationswere
good precursorsforsignals of an individual's
playfulintention.When an animal perceives
another animal in a compromised position or
performinga self-handicappingmovement,
the informationthatthisanimal cannot attack
available.An animal
immediatelyis intiinsically
on itsback or side cannot charge immediately,
and an animal shakingitshead vigorouslycannot leap precisely,because itsjudgmentof distance and direction is momentarilyblurred.
Play signals may also be derived fromexpressions, sounds, and odors associated with"having fun."
NEUROPSYCHOLOGICAL
INVOLVED
MECHANISMS
IN PLAY
Prediction 11: Severe or prolonged negative
emotions, such as fear,pain, anger, hunger,
frustration,or malaise, suppress play behavior. This predictionarisesfromour hypothesis
that play allows animals to develop adaptive
responses to unexpected eventswithoutbeing
overwhelmed by negative emotions. Clearly,
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JUNE
MAMMALIAN PLAY
2001
the preexistence of overwhelmingnegative
emotions,or theirarousal during play,would
be counterproductiveto this process. Negative emotions are also incompatible with the
"havingfun" affectthatis integralto play.
Prediction 12: Vigilance decreases during
play. This relationship is predicted because
some playmovementsimpairthe acuityofsensoryinput. Also, because the rapid switchbetween in-control and out-of-controlmovements and positions makes play a cognitively
thereis,presumably,little
demanding activity,
cognitive capacity leftfor other mental processes to occur simultaneously.
Prediction 13: There is a similarityin the
neuroendocrinological basis that underlies
playbehavior acrossmammalian taxa. We predict thisbased on the hypothesisthatthe specific neurobiological processes that produce
the "havingfun" emotion are constitutiveancestralelements of play.
Prediction 14: Play results in measurable
changes and enhancementsin the brain structures that receive and integratecomplex somatic sensations,control complex motor patterns, and modulate emotional reactions,
whereas exploratorybehavior leads, primarily, to changes in associative centers of the
brain. We suggest this because, in play, the
brain mustdeal withsituationsthatcannot be
subsumed under reliable rules but must be
solved by kinematic improvisationand emotional flexibility.By contrast,exploration enables animals to gatherinformationabout regularlyoccurringcontingenciesbetweenevents.
ENVIRONMENTAL
CONDITIONS
FOR PLAY
Prediction 15: Members of species thattypically live in stable physical habitats perform
less locomotoryplay than membersof species
thattypicallylivein more changeable physical
habitatsor those thatmove between different
habitattypes.This is predictedbecause the latter are exposed to greaterenvironmentalunpredictability,and should therefore gain a
greater benefit from experience in coping
with sudden environmentalchanges that affect locomotion. By contrast, the former
should benefitmore fromrehearsingthe specificlocomotor skillsneeded to negotiate establishedroutesthroughtheirterritory
byperforming them repeatedly in a nonplayful
147
manner (i.e., throughmotor learning, as described by Stamps 1995).
Prediction 16: Play increases in frequency
afteranimals move between habitats,experience substantialchanges in habitatthataffect
locomotion, or encounter mildlyfrightening
or novel stimuli.Through play, animals gain
experience in coping withthe novel situation
(e.g., snowfallin temperateand arcticregions).
Prediction 17: Play occurs only under relativelysafe environmental conditions and is
stronglysuppressed when predators or other
dangers are detected. Because playappears to
produce only modest benefits,it should only
occur when the costs remain low. Self-handicapping duringplayincreasestheriskofinjury
and predation; however,when the riskof predation is reduced by the close presence of a
vigilantparent or caregiver,a large group of
similarconspecifics,or a saferefuge,the probabilityof play should increase.
ONTOGENETIC
DISTRIBUTION
OF PLAY
Prediction 18: In each species of mammal,
play occurs at those ages when there is the
greatestdanger of fitnessloss if the animal is
caughtin an awkwardsituation.Older animals
should playlesswiththe physicalenvironment
because theyare morefamiliarwithit.As a result
of theirpreviousexperience,the environment
is more predictableand there is less need for
trainingfor the unexpected. However, play
thatinvolvessocial and predator-preyscenarios should continue in adultsofrelativelyintelligentspecies (i.e., withhigh encephalization
quotients:Jerison1973; Eisenberg 1981) that
adjust their strategiesin response to the unpredictable behavior of intelligentconspecifics, predators,or prey.
Prediction 19: Play is most frequent and/
or intense during periods of rapid allometric
growth.Rapid changes in body proportions
make the control of movementsless precise,
resultingin more frequentmisjudged actions.
Hence, there should be greaterbenefitsfrom
playingat this time to gain practice in recovering frommisjudged actions.
Prediction 20: Neonatal mammals play less
than juveniles. Neonates, especially those of
altricialspecies, lack the physicaland neurological development forvigorous alternation
between in-control and out-of-controlposi-
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THE QUARTERLY REVIEW OF BIOLOGY
148
tions. Play should become more common as
the animals become more capable of intentional self-handicapping.
Prediction21: Differentmodes of playpeak
at differentphases of ontogenyand, typically,
a peak in locomotoryplay precedes a peak in
social play.Mammalian conspecificslearn and
adapt theirbehavior in response to the behavior of others;thereforethe unpredictabilityof
play interactionswithconspecificsis likelyto
persistlonger during ontogeny than the unpredictabilitythatoccurs in playstimulatedby
elements of the physical environment.Also,
the relativelyhigh cognitivedemands of play
withconspecificsmay delay the peak in social
playversuslocomotoryplay.
Prediction 22: Withina population, play is
expected in all juveniles of a particular age
class. Alljuvenile mammals can gain a benefit
from experience in coping with unexpected
situations-not just males or the most dominant or strongestindividuals.
Prediction 23: Sexual dimorphismin a particular mode of play is found in species in
which the twosexes differin how importantit
is to be able to cope with the typesof unexpected situations that arise in that mode of
play.For instance,ifmales engage more often
in forceful agonistic interactions than females, thisshould be reflectedin higherlevels
of play that enable males to train for unexpected mishapsin theseinteractions.In slowly
maturing species, however, dimorphism in
play should be related not only to behavioral
dimorphism in adult life, but also (and perhaps mainly) to dimorphismin serious behavior that occurs in the current ontogenetic
behavior
stage (e.g., "teasing"or showing-off
injuvenile or adolescent males thatremain in
natal herds, adolescent strivingfor dominance in bachelor herds). We predict that
has primartrainingfor movementversatility
ily immediate benefits,although benefits in
termsof emotional coping can be longer lasting. It followsthat,in most species, sexual dimorphismin play increases withage.
PHYLOGENETIC
DISTRIBUTION
OF PLAY
Prediction24: The occurrence ofplayis positively correlated with the encephalization
quotient (Jerison 1973; Eisenberg 1981)
ratherthan withbody mass or metabolic rate
VOLUME
76
withinbroad taxonomic groups. This is predicted due to the cognitivelydemanding nature of play.
ALTERNATIVE
HYPOTHESES
ABOUT PLAY
A wealth of explicit or implicithypotheses
about the adaptive value of play has been proposed (Bekoff and Byers 1998; Burghardt
1998b; Power 2000). Traditionally,emphasis
has been placed on the development of play,
because animals are usually more playful
when young than as adults (but for examples
of adult play, see Breuggeman 1978; Biben
1979; Fagen 1981; Zucker et al. 1986; Pellis et
al. 1993; Hall 1998). Consequently,functional
explanations have usuallyfocused on waysin
which play during early development could
benefitanimals as adults. Hypothesized functions of play have included motor training,
and social and cognitivedevelopment. However,examinationof thesehypothesesthrough
play deprivation(Miller-Schwartze1968; Caro
1980), naturalsuppressionof playunder harsh
environmentalconditions (Baldwin and Baldwin 1974, 1976; Bekoff 1976; Sommer and
Mendoza-Granados 1995), or correlationsbetween results of play fightsand later dominance (Adams and Boice 1989; Araba and
Crowell-Davis1994) has revealed surprisingly
little evidence for long-termeffectsof play;
attentionhas also been paid to more
therefore,
immediate benefitsof play in young animals.
For example, play may provide opportunities
for self-assessment(Thompson 1996, 1998),
learningroutesthroughthe natal area (Stamps
1995), gaining dominance (Pellegrini and
Smith 1998), modulatingjuvenile aggression
(Drea et al. 1996), masteringimmediatefoodrelated or spatial cognition skills (Chalmers
and Locke-Haydon1984; Bjorklundand Brown
1998), or achievingheat/energydispersal(Barber 1991). We brieflyoutline the four most
clearly delimited and frequentlypromoted
general hypothesesabout play (Bekoffand Byers 1998; Burghardt1998b).
A simple explanation forthe apparent unity
of mammalian play is thatplay is a side effect
of other specific featuresof mammalian life
historyand physiology.According to the "surplus resourcemodel"(Burghardt 1988, 1999)
and itsmodificationby Coppinger and Smith
(1989), young mammals, in contrastto rep-
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TUNE
2001
MAMMALIAN PLAY
tiles,can affordto play because theypossess
an aerobic metabolismthatenables prolonged
and because theyreceive pavigorousactivity,
rental care, which includes the provisioning
ofmilkand a degree ofprotectionfrompredators.Play,according to thismodel, is a wayin
whichjuvenilemammalian behavioris remodeled into adult behavior; this "metamorphic"
character of play explains its variability.The
surplus resource model is not an hypothesis
about the adaptive value of play. On the contrary,it proposes that the primaryprocesses
that lead to the phylogeneticappearance of
play are merelyside effectsof other typically
mammalian adaptations. Adaptive modifications of play evolved later and contributedto
the diversificationof play in various taxa.
Hence, this hypothesis does not propose a
general functionofplay,but ratherdelineates
theaggregateofproximate,phylogenetic,and
ontogeneticfactorsthatmake up the singularityof play.
The "surplusenergy
as originally
hypothesis,"
put forthby Friedrich Schiller and later by
Herbert Spencer (1898), noted that "higher
animals"obtain betternutritionthan "inferior
species" duringearlyontogeny,and therefore
have to let offthe excess energyin play.Barber
(1991) made the hypothesismore specificby
arguing that young mammals are often not
limitedin energy.They benefitfromplay because thevigorous,3-dimensionalmovements
and the associated emotional arousal activate
thesympathetic
nervoussystem.Resultantacute
and chronic increases in metabolic rate, and
especiallyin brownadipose tissuethermogenesis, may produce a defense against cold and
obesity,and enhance resistanceto pathogens.
According to the surplus energy hypothesis,
playprovidesimmediate benefitsthatare not
directlyrelated to the specificformof play.
Perhaps the most intuitiveand widely accepted theoryabout the benefitsof play is the
practice theoryof Groos (1898). According to
thistheory,playin earlyontogenypreparesthe
animal forlaterlifebyperfectingcriticalbehavioral patterns.Among numerous offshootsof
this theory,the motor traininghypothesisof
Byersis the best developed. Originally,Byers
(1984) suggested that the ancestral form of
playwas locomotoryplay and itsfunctionwas
motortrainingto avoid predators.During fur-
149
therevolution,playwas modified,specialized,
and diversifiedin differenttaxa according to
selective pressures acting on the respective
populations. For instance, in highlygregarious and polygynouslarge-bodied ungulates,
social play evolved which closely mimics agonistic competition, especially among males.
Later, Byers and Walker (1995) refined the
hypothesis.They argued that performancedependent muscle fiber differentiationand
cerebellar synaptogenesis are the probable
long-termeffectsof the specific movements
performed during play. Byers (1998) labels
this proposal the "sensitiveperiodhypothesis."
The sensitive period hypothesis propounds
veryspecific and permanent (neuro) physiological effectsof playwhich lead to enhanced
skill,an optimalspeed/forceratio,and greater
economy of important species-typicalmovement patterns.
Thompson (1998:192) recentlysuggested
another general functionof play,namelythat
it provides developing individualswithimmediate feedback on their physical abilities; in
other words, play is an efficientmethod for
"self-assessment."
According to thishypothesis,
young animals test themselvesby repeatedly
performinga challenginglocomotor or social
action, or object manipulation. If theyrepeatedlysucceed in performinga task,theyswitch
to a more challenging task; if theyfail, they
may switchto an easier task. The self-assessment hypothesissuggeststhatbenefitsof play
are immediate and mostlyin the cognitivedomain.
In Table 1, we have attempted to identify
how the predictionsderivedfromour hypothesis differfrom those of the four alternate
hypotheses.To do thiswe firstconsidered predictions listed explicitlyby Burghardt (1988)
and Barber (1991), and some predictionssuggestedbyByers(1998) and Thompson (1998).
Next we considered predictions which, according to ourjudgement, are clearlyimplied
bythe hypothesisin question. For each of our
predictions,we decided whethereach of the
other four hypothesesleads to: (a) an identical or similar prediction (Agreement), (b) a
differentbut not opposite prediction (Alternative), (c) an opposite prediction(Contrast),
or (d) no prediction.
In the next section, we examine our new
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THE QUARTERLY REVIEW OF BIOLOGY
150
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THE QUARTERLY REVIEW OF BIOLOGY
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76
JUNE
2001
MAMMALIAN PLAY
playhypothesisagainstthe above fourhypotheses. We discusstheexistingempiricalsupport
forour predictions,and suggestfutureresearch
needed to investigatethe validityof each hypothesis.
SUPPORT
FOR THE "TRAINING
THE UNEXPECTED"
FOR
HYPOTHESIS
AND ITS ALTERNATIVES
FUNCTIONAL
CONSEQUENCES
OF PLAY
In this section, we refer to correlational
studies that have investigatedwithin-species
naturalvariationin playand laboratorystudies
thathave examined the effectsof playdirectly
through experimental manipulation of the
amount of play. There is some correlational
support for Prediction 1 of the "trainingfor
theunexpected" hypothesisin human studies.
Pellegrini (1995) found that the ability of
young boys to switchactivitiesduring roughand-tumbleplay is correlated withtheirlater
scores on a testof social problem-solvingability.Thus, experience gained from switching
between activitiesin play may be associated
withgreaterbehavioralplasticity
in unexpected
or novel circumstances.Similarly,Saunders et
al. (1999) found a correlation between playfulnessand coping skillsin preschoolers.
To our knowledge,our predictionthatplay
experience increases movement flexibility
when recoveringfromawkwardpositions has
not been tested.On the other hand, thereare
experimental data that support our prediction that the abilityto cope emotionallywith
challengingsituationsis compromised byplay
deprivation in the juvenile period. Most of
these data stem from laboratoryrats (Rattus
norvegicus)
deprived of social playvia isolation
during the fourthand fifthweek of life and
testedlater (between 85 and 120 days of age)
in a varietyof social and nonsocial challenge
tests.Potegal and Einon (1989) showed that
these ratswere more prone to attack and injure another rat after receiving an electric
shock fromthe floor grid. This resultcan be
interpretedas showing thatsocial play deprivation produced a strongerreaction to an unexpected and unidentifiable aversive situation. Van den Berg et al. (1999a) found that
ratspreviouslyisolated as juveniles undulyescalated conflictswhen confrontedwitha resident rat in their territory,and had higher
155
plasma corticosteroneand epinephrine concentrations,compared withnonisolated controls.Rats isolated as juveniles also had a reduced motivationfor social contact with an
alien rat during the first10 minutes afterbeing placed in a neutral arena, although this
trendtended to reversein the second 10 minutes (Hol et al. 1999). In other studies, rats
isolated asjuveniles have displayedbehavioral
hyperactivityin open novel environments
(Gentsch et al. 1988), slowerhabituationrates
in an open field (Einon et al. 1978), and
greateravoidance of open spaces in a preference test (da Silva et al. 1996).
The disadvantageof thesestudiesis thatisolation deprives the juvenile not only of play
but also of other formsof contactand sensory
stimulationfrom companions. However, the
findingthat the daily provisionof a drugged
(nonplayful) partnerduring the isolation period did not prevent the effectsof isolation,
whereas providinga normal play partnerdid
prevent these effects(Einon et al. 1978; Potegal and Einon 1989), suggeststhatthe consequences of social isolation may indeed be
due largely to play deprivation. As a whole,
these resultssuggest that play deprivationresultsin increased fearand uncertaintyin novel
environments,and more escalated aggressive
behavior towardsconspecificsin serious conflicts,as predicted from our functional hypothesis.
Bycontrast,thereis littledirectevidence for
the adaptive effectsof play predicted by Barber's surplus energy hypothesis.The prevention of obesitythroughheat production does
not seem plausible,giventhatenergyexpenditure in play is generally low. Even playful
young kittens(Felis catus) allocate only 4% of
theirenergyexpenditureto play(Martin1984).
Furthermore,there are examples of intense
playin situationswhen the preventionof obesitywas not an adaptive goal. Kittenswhose
milksupplywas experimentally
limitedshowed
more play than normal (Martin and Bateson
1985), and young harborseals (Phoca vitulina)
were observed to play most at the time of fat
accumulation (Renouf 1993).
The motor training/sensitiveperiod hypothesisin itsstrongform(playduringa sensitive period is necessary
for normal behavioral
development) is rebuttedby the factthat,de-
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156
THE QUARTERLY REVIEW OF BIOLOGY
VOLUME
76
spitesuppressionofplaydue toveryharshnat- (Gentschet al. 1988; Potegal and Einon 1989).
ural conditions or laboratorymanipulation, These resultssuggestthat,contraryto the monormalprey-catch- tor training/sensitiveperiod hypothesis,the
animalsdisplayqualitatively
ing and social behavior (Baldwin and Baldwin behavioral effectsof play deprivationare not
1974, 1976; Bekoff1976; Caro 1988; Sommer (solely) mediated by permanent effectson
and Mendoza-Granados 1995). Even in itsless cerebellar synaptogenesis and muscle fiber
strongform (play experience during a sensi- differentiation.
tiveperiod affectsthe formand efficiencyof
KINEMATICS AND STRUCTURE OF PLAY
species-typicalmovements), there is contrathat
the
dictoryevidence. Caro (1980) found
The ubiquitous presence of self-handicapstimulation of extra object play in kittens ping positions and movements in play sethroughprovisionof suitable objects did not quences is themajorpredictionofour hypothealtersubsequentpredatorybehavior.Playdepri- sisabout theformofplaybehavior (Prediction
vationin rat isolation studies has generallyre- 3). Self-handicappingelements need not resulted in differencesin the quantity,rather semble any "serious" adult or juvenile motor
than quality,of adult social behavior. For ex- pattern,as theycan mimicmovementsthatocample, prior isolation of ratsincreased the la- cur withoutan animal's active contribution.
tencyand decreased the frequencyof social On the contrary,the motor training/sensitive
behavior elements,but did not alter theirba- period hypothesis implies that play movesic formand sequential patterning (van den ments are similar to "serious" adult moveBerg et al. 1999b). Given the similarityof cer- ments because optimal permanent tuning of
tain play movementsand elements of sexual muscle typesand cerebellar synapsescan only
behaviorin male rats (Pellis 1993), adult male be achieved ifthe "right"movementsare persexual behavior motor patternsshould be af- formed during the sensitiveperiod. The selffectedbyjuvenile playdeprivation,according assessmenthypothesisis also at variance with
to the motor training/sensitiveperiod hy- the occurrence of self-handicapping movepothesis.However,van den Berg et al. (1999a)
ments because animals should "play to win"
found thatthe capacityto performsexual mo- (Thompson 1998:197); thatis, theyshould try
tor acts was intactin ratsisolated as juveniles. to achieve success in a playbout withmaximal
Also, theirintromission/mountratio,whichis effortbecause, otherwise,theirself-assessment
reduced in exhausted or inexperienced male will be inaccurate. According to the surplus
rats,was unaffected;thustheircopulating skill resource model, "imperfect" elements are
was comparable to controls.
possible in play. They should stillbear some
hypoth- resemblance to adult "serious" behavior eleThompson's (1998) self-assessment
esis predictsthatreduced play experience re- ments,however,because play is, according to
sultsin an impaired abilityto assess risk,costs, that model, a behavioral bridge between the
and benefits.The effectsof social isolation on periods ofjuvenile dependence and adult reemotional coping abilityin rats are compati- sponsibilities(Burghardt 1988:130).
ble withthisprediction as well as our own.
In supportof our hypothesis,thereis ample
In regard to the timingof beneficial effects evidence thatself-handicapping-in thesense
of play (Prediction 2), Byers (1998) argued thatanimals deliberatelydo not exertfullconthat play has nonnegligible energy and sur- trolover theirmovementsor activelyput themvivalcostsforjuveniles,but no benefitsforju- selvesinto disadvantageous positions-is omvenile survivalhave been documented; there- nipresent in play. First,a prominent feature
fore the adaptive benefitsof play must occur ofplaybehaviorelementsis thattheyare exaglater in life. However, studies that investigate gerated (Bekoffand Byers1981; Fagen 1981;
the impact of play experience on short and Burghardt 1984). Playful running and aplong-termrates of mortalityfrom different proaches have been described as "bouncy"in
causes are lacking. As to the permanency of domestic dogs (Canis familiaris),wild canids,
play effects,rodent play deprivation studies and piglets (Sus scrofa) (Bekoff 1974; Biben
show thatmanyeffectson behavior can be re- 1983; Newberryet al. 1988); playfulsocial inversed or alleviated bylater social experience teractions as "capriciously exaggerated" in
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JUNE
2001
MAMMALIAN PLAY
chimpanzees (Pan troglodytes)
(Spijkerman et
al. 1996); hops as "frisky"
in punares (Thrichomysapereoides)(Wilson and Kleiman 1974;
Thompson 1998) and "frantic"in rats (Panksepp 1998); torsomovementsas 'jerky"in bighorn sheep (Ovis canadensis) (Berger 1980);
manipulation of objects as "boisterous"in cats
(Felis catus) (Hall 1998); and water play as
"ebullient" in harbor seals (Phoca vitulina)
(Renouf 1993). These adjectivesare shortcuts
for sayingthat the play elements are too disproportional, too distorted,too fast,too uncontrolled,or too quicklyrepeated in comparison with their "serious" counterparts and,
hence, are less suited to achieving the apparent proximategoal of those movements,such
as escape, effectiveobject handling, or overpoweringan opponent.
Second, vigorous rotational elements are
among themostfrequentelementsin playand
are prominentlyfeaturedin the play descriptions of many species. These movements include head shakes, tosses and jerks, neck and
torso twists,heel kickingwithlateral rotation,
high speed turns,somersaults,and pirouettes
(Mutller-Schwartze
1968; Gentry1974; Wilson
and Kleiman 1974; Byers 1977; Fagen and
George 1977; Berger 1980; Biben 1983; Pellis
and Pellis 1983; Byers 1984; Rasa 1984; Gomendio 1988; Rothstein and Griswold 1991;
Renouf 1993; Miller and Byers 1998; Byers
1999). In a systematicstudy,Byers (1984) observed head shakes, head jerks, or neck twists
in the play of all 12 ungulate familiesinvestigated; theywere the second most widely occurring type of behavior found in play after
running. Most rotatoryactions involve highspeed angular movement of the head and,
hence, impairsensoryand spatial orientation.
Third, play movementshave more degrees
of freedom than other typesof behavior (Golani 1992; Fontaine 1994). For instance,mammals usuallydo not use rotationin the frontal
plane in their"serious"behaviorbut oftenadd
thisdegree of freedomto theirmovementsin
play. Primatesuse head tiltsto communicate
playfulmotivation(Sade 1973), and ungulates
oftenkicktheirheels to one side duringlocomotoryplay. Baldwin and Baldwin (1974) reported thatsquirrelmonkeys(Saimirisciureus)
signal play intent by looking between their
legs. We may speak about deliberate kine-
157
matic plasticityin play that mimics the "enforced kinematicplasticity"that mightbe inflictedby an external force. These positions
are self-handicappingbecause the animal sees
the environmentfromunusual angles and is
placed in bilaterallyasymmetricpositionsthat
limitkinematicoptions in the next move.
Fourth, animals in play often performobject manipulation or social interactionsin disadvantageous positions. Differentspecies of
primatesexhibit play behavior while hanging
bytheirhands,feet,or tails(Baldwinand Baldwin 1974; Aldis 1975), or they replace the
usual quadrupedal walking withunstable bipedal locomotionduringplay (Fontaine 1994).
Young animals ofmanypredatorymammalian
species exhibitplaybehaviors (sociallyor with
objects) while lying on their side on the
ground (Fagen 1981).
Fifth,use of self-handicappingactions by
largeror strongeranimals thatengage weaker
partnersin play has been reported in, forexample, five species of macropodoids (MacM. rufogriseus,
M. ruropusparryi,M. robustus,
fus, Thylogalebillardierii)(Watson and Croft
1996; Watson 1998), Africanelephants (Loxodontaafricana)(Moss 1988:163), coyotes(Canis
latrans) (Bekoff,unpublished observations),
squirrel monkeys (S. sciureus)(Biben 1989),
hamadryas baboons (Papio hamadryas)(Pereira and Preisser 1998), and chimpanzees (P.
troglodytes)
(Mendoza-Granados and Sommer
1995).
Our second structuralpredictionis thatplay
is sequentiallyvariable (Prediction 4). High
sequential variabilityof play has been documented in several species. Bekoffand Byers
(1981) reported thatsequences of play in infant canids were significantlymore variable
than sequences of agonistic behavior. Newberryet al. (1988), observingpiglets (S. scrofa)
in a seminaturalenclosure, identifiedsix play
markers (elements occurring only in play)
and found that all 22 remaining behavioral
elements in the ethogram occurred at least
once just before or just afterone or more of
the play markers.Rasa (1984) observed that
dwarfmongooses (Helogale undulata) switch
veryfrequentlybetween behavior representativeof preycapture,social interaction,enemy
avoidance, and exploration during play, and
Gentry(1974) reported similarvariabilityin
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158
THE QUARTERLY REVIEW OF BIOLOGY
the play of Stellar sea lions (Eumetopiasjubatus). Where locomotory, social, and object
play occur in the repertoireof a species, the
relativefrequencies of these differentmodes
of play may change during ontogeny (Newberryet al. 1988), during the course of a day
(Byers 1977), or even within a play session
1968; Rasa 1984). Never(MfXller-Schwartze
theless,elements of these threemodes of play
(or at leastthoseof locomotoryand social play)
are often intermixedwithina single bout of
play (Inhelder 1955; Muller-Schwartze1968;
Gentry 1974; Aldis 1975; Biben 1983; Pellis
and Pellis 1983; Newberryet al. 1988; Pedersen et al. 1990; Mendoza-Granados and
Sommer 1995; Vanderschuren et al. 1997;
Thompson 1998).
thepresence ofself-handicapInterestingly,
ping elements in play is implied by the most
widelyused definitionof play: "playis all motor activitythat appearspurposeless" (Bekoff
and Byers 1981; Bekoff 1984; Pellegrini and
Smith 1998; Byers1999). This definitionis intuitivelyappealing despite the inclusion of a
subjectivejudgment. Play does appear purposeless, but not because it has no function.
The "purposelessness" of play is strikingbecause some movementsare inconsistentwith
the apparent purpose of the behavior thatimmediatelyprecedes or followsthe playfulbehavioralelements.For example, ifplayfulrunning bypigletsis viewed as trainingforescape
fromdanger, it seems pointless to performa
deliberateflop-overaftera fewmetersofscampering. However, this behavior does make
sense ifthe animals are preparing themselves
forthe possibilityofa fallwhilemakinga rapid
directional change-duringflight.
SOCIAL ASPECTS OF PLAY
Of the evaluated hypotheses,three (those
of Burghardt,Barber, and Byers) do not give
specificpredictions about the choice of partners in play or related social aspects. The selfassessmentand "trainingforthe unexpected"
hypothesesdo offerpredictions about social
play,but these predictions are opposing. Acis an imcording to our hypothesis,familiarity
portant criterionfor choice of play partners
hy(Prediction6), whereas theself-assessment
pothesis suggeststhat playmatesare selected
strictlyaccording to their physicalmatch. In
VOLUME 76
polycotous species, young often prefer siblings as playmates(Dobao et al. 1985; Holmes
1994). Several studies also document the tendency of young mammals to play preferentiallywithyoungstersof theirage (e.g., Berger
1980; Byers 1980; Rothstein and Griswold
1991; Mendoza-Granados and Sommer 1995;
Thompson 1996). However,itis oftenunclear
whether this preference is due to familiarity
or a match in body size.
Studies thatexplicitlyidentifythe role of reversus body size match
latedness/familiarity
give conflictingresults.For example, in sable
niger),relatedindividuals
antelope (Hippotragus
were not preferredif theywere not matched
in size (Thompson 1996), whereas in bighorn
sheep (Ovis canadensis)and chimpanzees (P.
familiarityaffectedthe choice of
troglodytes),
playmatesmore than age (Berger 1980; Markus and Croft 1995). Differences between
studiesmaybe related to the degree of differbetween
ence in bodysize, age, and familiarity
available play partners,and methodological
differencesin quantifyingchoice of playpartners. More long-termstudies are needed to
identifythe prevalentpatternover an arrayof
species. Such observationsshould also demonstratewhat happens when the strengthof two
previouslymatched partners diversifies.Achypothesis,the
cording to the self-assessment
animals will switchtheirpreferenceto bettermatched partners, whereas we predict that
theywillcontinue to playwitheach other and
use self-handicappingto compensate for the
difference(Prediction 8).
The "trainingforthe unexpected" and selfassessment hypotheses give two additional
contrastingpredictionsabout social aspects of
play.Regardingplayinitiation(Prediction 7),
the available evidence tends to support the
self-assessmenthypothesisin that the larger
partner more often initiatesplay or there is
no effectof body size (Owens 1975; Pellis and
Pellis 1991; Mendoza-Granados and Sommer
1995; Biben 1998; Thompson 1998). In some
species, however,younger animals are more
often the initiators (Gomendio 1988) or
weaker individuals initiate more escalated
formsof contactplay (Watson 1998). Regarding the contagious nature of play (Prediction
9), social play often involves more than two
animals (Gentry 1974; Pedersen et al. 1990;
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JUNE
2001
MAMMALIAN PLAY
159
is a conventional wisdom that sick, injured,
depressed, or angryanfrightened,frustrated,
imals do not play,littledirectevidence is available. Quantitativestudies could be used to assess whether animals are willing to expend
more timeor energyforan opportunityto play
in relation to their level of well-being (e.g.,
through demand curve methodology; Dawkins 1990).
The "trainingfortheunexpected" hypothesis predictsthatthereis a specificneuroendocrinological basis of play thatis similaracross
differentplaymodes and across various mammalian species (Prediction 13). On the contrary,
Burghardt'ssurplusresourcemodel, with
its claim about disparate origin and lack of a
general functionforplay, implies thatdifferent neuroendocrinologicalsubstratesand processes underlie differentplay patterns.Thus
far,the evidence collected on laboratoryrats
suggests that play may specificallytap brain
mechanisms involved in somatosensoryperception, emotional experience, and arousal
control.
First,thereis evidence thatregions of brain
thatprocess certaintypesofsomatosensoryinformationare particularlyrelevantfornormal
playto occur (Siviy1998:233-234). Cells in the
parafascicularnucleus of the thalamus (PF),
havinglarge receptivefieldsand high thresholds for excitation,receive somatosensoryinformation of a very diffusenature, whereas
cells in the ventrobasal thalamic complex
(VTC), having small receptivefields and low
thresholds, receive somatosensory information of a verydetailed nature. Lesions to the
PF substantiallyreduce "pinning,"an element
used in quantifyingrat social play,while having minimaleffectson otherbehavior.Bycontrast,lesions to theVTC have a minimaleffect
on play. PF activityalso increases substantially
duringplay episodes, as measured by the c-fos
Panksepp (1998:288)
technique. Interestingly,
reportsthatfullbody ticklingwas more effecMECHANISMS
NEUROPSYCHOLOGICAL
tivein inducing 50 kHz chirpingvocalizations
INVOLVED IN PLAY
in rats (presumablyconnected to play mood)
We predict thatplay is stronglysuppressed than tickling of individual parts of the rat
by negative emotional states (Prediction 11), body. Taken together,these findingssuggest
whereas the self-assessmenthypothesis pre- that nonspecific reticular nuclei involved in
whole-body
dicts that animals should "play to win," im- the perception of high-intensity
plyingthat theyshould be prepared to over- sensations, like those in the PF, specifically
come negative emotions in play. Although it mediate play urges. This is in agreementwith
Loranca et al. 1999), supporting our prediction over Thompson's prediction that play
should be dyadic. In domestic piglets,triadic
play amounted to about 20% of all interactions (M Spinka, unpublished observations).
Our prediction that play signals are often
behavior (Prederivedfromself-handicapping
diction 10) is supported by many examples.
Self-handicappingpostures, such as lyingon
side or looking between the legs, and movementssuch as playbows,roll-overs,pivots,and
head tosses,are used especiallyoftenimmediately before vigorous locomotory and social
play actions (Geist 1963; Miller-Schwartze
1968; Baldwin and Baldwin 1974; Wilson and
Kleiman 1974; Pellis and Pellis 1983; Gomendio 1988; Newberryet al. 1988; Rothsteinand
Griswold1991; Bekoff1995; Watson and Croft
1996; Miller and Byers1998); thustheyhave a
specificmetacommunicativefunction(Bekoff
1975, 1995). They affectthe behavior of the
receivinganimal in such a waythatthe sender
is able to sustain the playfulinteraction despite the vigorous action thatfollows.
There is a dramaticdifferencebetween the
movementsand posturesused to signal intent
to attack and those used to signal intent to
play. Threatening animals displaytheirbroad
side, use frontallysymmetricpositions, and
performsymmetricalmovements.Given that
are reliable indicators
body size and symmetry
of physical fitness (M0ller 1998), these displays express signaler condition. In contrast,
movementsand postures
theself-handicapping
used to signalplayfulintenthave elementssimilar to thoseused byweak,tired,subordinate,or
even sick,injured, or developmentallyhandicapped animals-lowering down, decreasing
apparent body size, gaping, shakingthe head,
and twistingasymmetrically.Compare the
threatstanceof dogs (C.familiaris)
standing-tall
withthe "play bow" signal in which the front
part of the body is lowered (Bekoff1977).
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160
THE QUARTERLY REVIEW OF BIOLOGY
our hypothesisthatplaytrainsanimalsforcoping with unexpected movements and positions rather than perfectingspecific skilled
movements.
Second, in the rewarddomain, opioids appear to be involved in play in a specificway.
For instance,low doses of morphine increase
playand opiate antagonistsreduce it,although
the same manipulations have opposite effects
on the desire for general social interaction
(Panksepp 1998:293). Ligands of ,-opioid receptors influence social behavior elements
that occur in play but not those unrelated to
play (Vanderschuren et al. 1995b). Also, neonatal cocaine exposure affects subsequent
learning based on a play rewardin a different
way than learning based on a food reward
(Willfordet al. 1999).
Third, play is dependent on monoaminergic systemsin a distinctway (reviewedby Siviy
1998). In the anticipatoryand warm-upphases
of a play bout, the ventrotegmentaldopaminergic systemis involved.Once a playbout is in
full stride, high noradrenergic activityenhances play. On the other hand, serotonergic
activitymustbe low forplay to occur.
Thus, forrats,evidence is accumulatingthat
play might,indeed, employ the brain in a specificway.However,we do not knowyetwhether
similarmechanisms are active during play in
other mammals because almost no studiesfocused on brain mechanisms underlyingplay
have been conducted in other species.
The "trainingforthe unexpected" hypothesis predictsthatplayactivityresultsin measurable changes in somatosensory,motor, and
emotional brain centers (Prediction 14). The
motortraining/sensitive
period hypothesisimplies thatchanges should be in motor control
areas, especiallyin the cerebellum,ratherthan
in emotional centers.The opposite prediction
follows from the self-assessmenthypothesis.
Depriving young rats of social play through
isolation during the age when playis mostfrequent resultedin long-termchanges in p-opioid receptorsin basolateral amygdalaand bed
nucleus of striaterminals,and in K-opioidreceptorsin severalcorticalareas (van den Berg
et al. 1999c). Rats reared in isolation also have
permanentlyaltered levels of dopamine, norepinephrine,and serotonin (reviewedbySiviy
1998:235). These monoamines are important
VOLUME
76
for coordinating an organism's response to
stress.Thus, it appears thatjuvenile play does
alter the neurochemistryof brain emotional
centers. More evidence is needed, however,
thatshould include species other than the rat
and should more preciselydistinguishwhether
the effectsare specificallydue to playdeprivationor some more general aspectsofthesocial
isolation procedure. Although the specificeffectsof play on motor centers have not been
tested,it is known thatin cerebellar Purkinje
cell axons, the selection ofwhich synapseswill
be retained is experience dependent and occursat about theage whenratsplaymost (Byers
1998). In sum, the limited available evidence
suggests that somatosensory,emotional, and
motorcentersof the brain are affectedbyplay
experience.
ENVIRONMENTAL
CONDITIONS
FOR PLAY
The "trainingforthe unexpected" hypothesis predicts more locomotoryplay in species
thatlive in veryvariable or changing environments (Prediction 15). The surplus resource
model suggeststhatanimals livingin more energyefficientenvironmentsshould playmore.
The surplus energyhypothesispredictsmore
playin species thatlivein habitatswithsurplus
food. Examples can be found of species that
fiteach of these predictions. Thus, bighorn
sheep (0. canadensis) living in variable hilly
terrain,harbor seals (P. vitulina)livingin an
energy-efficient
waterenvironment,and Hanuman langurs (Presbytis
entellus)living in a
food-richhabitatare all highlyplayful(Berger
1980; Renouf 1993; Sommer and MendozaGranados 1995). Systematicstudiesacross numerous, taxonomicallycloselyrelated species
habitatsare needed to deterlivingin different
mine which of these predictionsholds true.
Our hypothesispredicts that a change in
habitat or in a significantenvironmentalfeatureshould stimulateplay (Prediction 16). On
the contrary,Burghardt's surplus resource
model predictsmore playin an unstimulating
environment.There is evidence that animals
tend to play in new,rare,or more demanding
local habitats.The stimulatoryeffectof fresh
snow or shallowwateron playin dogs and humans is well known.Berger (1980) found that
bighorn sheep (0. canadensis)livingin British
Columbia's Chilcotin hills spent about one
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JUNE
MAMMALIAN PLAY
2001
fourthof their total play time in small sand
bowls at the base of the hills. Byers(1977) reported thatSiberian ibex kids (Capra siberica)
preferredto play on sloped rather than flat
ground. De Waal (1996:47) described rhesus
monkeys(Macaca mulatta)as beingverypreoccupied bya giantverticalwheel thattheycould
spin rapidly,release, and thus catapult themselvesmetershigh.It iswell knownthatcaptive
animals can be induced to play by the introduction offreshbedding into theiraccommodation or bymovingthem temporarilyinto an
alternativeenvironment(e.g., Pedersen et al.
1990; Wood-Gush and Vestergaard 1991; de
Passille et al. 1995;Jensen et al. 1998). Mildly
dangerous prey, sudden noise, or windy
weather can stimulate play as well (MullerSchwartze 1968; Biben 1979; Prescott 1985;
Newberryet al. 1988).
Onlyour hypothesismakes a specificpredictionin regardsto thesafetyoftheplayenvironment (Prediction 17). Interestingly,
iflaboratoryratsare keptin dim light(whichis natural
for them), exposure to intense light suppresses play but not other social behaviors
(Vanderschuren et al. 1995a; Knutson et al.
1998). This makes sense when viewedfroman
evolutionaryperspective,giventhatplayactivitybywild ratsduringperiods of high visibility
would probably increase their risk of predation. Our prediction thatanimals should play
only when the environmentis relativelysafe
ties in withour prediction thatvigilance is reduced during play (Prediction 12), and with
the observation of Biben et al. (1989) that
squirrelmonkeymothers(S. sciureus)increased
their level of vigilance when their offspring
were at play.
ONTOGENETIC
DISTRIBUTION
OF PLAY
Thompson (1998:192, 200) hypothesized
that the information gained through selfassessmentin play facilitatesnormal development in differingenvironments,therebyimplyingthatplay should decline when animals
reach adulthood. We predict, more specifically,thatplayshould startat low levelsin neonates, peak during the juvenile period, and
decline later (Predictions 18 and 20). This
prediction holds true for the vast majorityof
species examined (e.g., Biben 1983; Prescott
1985; Gomendio 1988; Newberryand WoodGush 1988; Renouf 1993; Byers1998).
161
Burghardt'ssurplusresource model and Byers's sensitive period hypothesis imply that
there should be no play (or verylimitedplay)
in adult mammals. Yet it is now well documented that adults of many species do play
(Breuggeman 1978; Biben 1979; Berger 1980;
Fagen 1981; Byers1984; Rasa 1984; Zucker et
al. 1986; Coppinger and Smith 1989; Enomoto 1990; Pedersen et al. 1990; Barber 1991;
Pellis et al. 1993; Renouf 1993; Hall 1998;
Millerand Byers1998; Watson 1998). Barber's
surplus energyhypothesispredicts adult play
in species that use brown adipose tissue for
thermoregulation,such as hibernators, but
thisprediction does not explain whyplay occursin,forexample, adult kangaroos,rats,primates, and pinnipeds, and whyno adult play
has been documented in hedgehogs (Erinaceus europaeus) (Fagen 1981). We expect to
find adult play,especially in more intelligent
species faced withthe unpredictablebehavior
of conspecificsand, possibly,withrelativelyintelligent predators or prey. More data are
needed to assesswhetherthisis a robustmammalian trend.
Two of the alternative hypotheses differ
from the "trainingfor the unexpected" hypothesisin theirpredictionsabout when, during the juvenile period, play should occur.
Where we predict that play will be most frequent during the period of rapid allometric
growth (Prediction 19), Barber's surplus energy hypothesispredicts that play will peak
when the consummation of solid food becomes prevalent.The sensitiveperiod hypothesis of Byerspredictsontogenetic parallelism
betweenplay,on the one hand, and cerebellar
synaptogenesisand muscle fiber differentiation on the other.This has been found in mice
(Mus musculus),rats,and cats (F. catus) (Byers
and Walker 1995). However, furtheranalysis
of the literatureis needed to assess the level
of supportforthe differentpredictionsabout
the precise timingof the peak in play during
thejuvenile period.
We predictthatdifferentmodes of playwax
and wane at different
ages withinthe same species (Prediction 21), whereas the surplus energyand sensitiveperiod hypothesesimplyan
ontogeneticallyparallel course forall formsof
play. Available evidence appears to favorthe
former prediction (Gentry 1974; Burghardt
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162
THE QUARTERLY REVIEW OF BIOLOGY
1998b). Our more specificprediction thatlocomotoryplay will precede social and sexual
play during ontogenyalso appears to be supported (Berger 1980; Berry and Signoret
1984; Prescott 1985; Gomendio 1988; Newberryand Wood-Gush 1988; Newberryet al.
1988; Haynes 1997). In spotted hyenas (Crocuta crocuta),by contrast,social play precedes
locomotoryplay (Drea et al. 1996). This exception is in accord withour prediction that
playhas immediatebenefits,giventhatwithinden aggression among hyena siblings precedes locomotion outside the den. Similardevelopmental patternsare observed in coyotes
(Canis latrans) and red foxes (Vulpesvulpes)
(Bekoff1974).
Withrespectto predictionsabout sex differences in play,Barber's surplusenergyhypothesis predictsnone; the optimal formforadaptive energyloss should be the same for both
sexes. The sensitiveperiod hypothesisimplies
that sexual dimorphism of play, where present, will occur throughout the sensitiveperiod. We predict that the sexual dimorphism
in play will increase withage (Prediction 23)
because, presumably, the serious situations
for which play provides trainingbecome increasinglydisparate in the two sexes and because thebenefitsofplayare partiallyimmediate. Examples of pronounced, moderate, and
nonexistent sex differencesin play can be
found in theliterature(e.g., Byers1977; Biben
1983; Prescott1985; Caro 1988; Pedersen et al.
1990; Renouf 1993; Watson 1998). However,
a majorityof the available data supports the
prediction of increasing sexual dimorphism
in play with increasing age (Gentry 1974;
Meaney et al. 1985; Newberryand Wood-Gush
1988; Newberryet al. 1988; Spijkerman et al.
1996; Haynes 1997; Smith et al. 1998). Available data also suggest that this differenceis
not dependent on concurrentlydivergingsex
steroidlevels (Meaney et al. 1985).
VOLUME
76
cies withmoderate body size and thermogenically active brown adipose tissue should be
the most playful.In the only systematicstudy
published so far,Byers(1999) found thatplay
in Australianmarsupialsis associated withrelativebrain size but not withbody size or metabolic rate; Ortega and Bekoff(1987) reported
similartrendsin birds.
DIRECTIONSFORFUTURERESEARCH
On the whole, our hypothesisappears to
fare better than the four alternativesthatwe
have evaluated. This assessmentmustbe considered preliminary,however,because: (i) the
evidence is fragmentary,(ii) there may be
other relevant papers that we have not reviewed, and (iii) it was difficultto assess data
fromdifferentsources using uniformcriteria
because ofvariationsin methodologyand emphasis.Consequently,further
efforts
are needed
to elucidate whichofthemanypredictionsdiscussed above are generallysupported across
mammalian taxa.
The most directevidence forany of the putative functional hypotheses of play could
come from controlled experimentsin which
the amount ofplayexperience is manipulated
and the predictedeffectson behavior,physiology, adult skill and/or coping, survival,and
reproduction are recorded. The difficulty
withthese studiesis thatplay deprivationusually removes other sources of stimulationas
well,as, forexample,when animalsare socially
isolated during the period when theywould
play the most. Thus, it is unclear whetherthe
resultingeffectsare due specificallyto the lack
ofplay.More refinedmethods,such as the use
of drugged play partners, employing short
daily periods of play in isolates (Potegal and
Einon 1989), or using a housing environment
thatinhibitsplayare promising,although typicallyrestrictedto species amenable to studyin
laboratorysettings.
Exciting progress has been achieved in asPHYLOGENETIC
DISTRIBUTION
OF PLAY
sessing the neurophysiological and neuroWhere we predictmore playin species with chemical basis of play (Vanderschuren et al.
highlydeveloped cognitiveabilitiesand, hence, 1997; van den Berg et al. 1999c), and promisa high encephalization quotient (Prediction ing investigationshave been made into the
24), Burghardt'ssurplusresource model pre- emotionalprocessesassociatedwithplay (Pankdicts that moderatelysized species with high sepp 1998). However,fora more complete unmetabolic ratesshould playthe most.Barber's derstandingof the relationshipbetween play
surplus energy hypothesissuggests that spe- behavior,the associated cognitive,emotional,
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JUNE
MAMMALIAN PLAY
2001
and motivationalprocesses, and the underlying brain machinery,considerable conceptual
and experimental difficultiesmust be surmounted.
we suggestthatsubGiven these difficulties,
stantial progress in understanding the function of mammalian play can be achieved by
focusing on the ontogenetic, phylogenetic,
and ecological distributionofplay,and on sex
differencesin play. Widelyscattereddata can
be drawn together,combined with available
strategies,and sibinformationon life-history
mittedto detailed analyses to verifyquantitativelywhich of the trendspredicted by the differenthypotheses are supported within and
across mammalian taxa.
FINAL REMARKS
THE" ONE FUNCTION-MANY
FUNCTIONS
PROBLEM REVISITED
163
(Siegel 1995).
typeslike herbivory/carnivory
Highly diverse functionsfor REM sleep have
been proposed, including the maintenance of
a high,stablebrain temperature(Wehr 1992),
ensuring recoveryfrom sleep (Vertes 1986),
memory and/or sensorimotor experience
processing (Winson 1993; Ribeiroet al. 1999),
compensation for brain processes that take
place during non-REM sleep (Benington and
Heller 1994), promoting brain development
(Mirmiran1995), and reinforcingpsychological individuation (Jouvet1998). Despite this
diversity
offormsand possible functions,REM
sleep is considered a homologous traitthat
originatedveryearlyin mammalian historyor
even in reptilian ancestors of mammals
(Siegel et al. 1998), probably to fulfilla substantial, although not yet fully elucidated,
originalfunction.In ourview,thereare strong
indications that mammalian play may have a
similarphylogenetichistory.
Our hypothesisprovides a plausible explanation about whyplay,specifically,could have
diversifiedinto such a rich arrayof formswith
various derived functions.According to the
constituentsof play presented in this review,
play should resultin flexible reactions to unexpected situations. Play may thus result in
more diverse behavior both within and betweenindividuals.In other words,individuals
may,throughplay,findand develop theirown
personal methods for coping with different
kindsofunexpectedmisfortunes.
Indeed, qualitativedifferencesbetween individualsand betweenlittersarise duringjuvenileplay (Wilson
and Kleiman 1974; Lund and Vestergaard
1998). Thus, playmayincrease phenotypicbehavioralvariabilitywithinpopulations, which,
in turn,mayopen the door to the Baldwin Effect,a process by which novel variations become geneticallyfixed (Baldwin 1896; Parisi
and Nolfi 1996). In this way, play may have
acquired novel kinematicforms,causal links,
developmental pathways,and beneficialfunctionsin variouslineages whilestillretainingits
basic nature.
While the core of our hypothesisis thatplay
in mammalshas one originalfunction,namely
to trainforunexpected situations,clearlyplay
behaviorin itsextantvarietycan fulfillvarious
other functionsin individualspecies and animals that differin age and sex. To illustrate
this "one ancestral-manyderived functions"
possibility,Byers (1984:44-45) compared the
diversificationof mammalian play to the evolution of the pentadactylforelimb.Although
the quantitativemodificationsof the mammalian manus are impressive(e.g., the prolongadetion of fingersin bats), the basic five-digit
sign is retained. Yet the ancestralfunctionof
walkinghas been complemented, or even replaced, by diverse new functionssuch as digging in anteatersand swimmingin dolphins.
Similarly,once play was established in mammalian behavioral design,itdiversifiedin individual taxa to fulfillvarious specificfunctions.
A perhaps closer phylogeneticparallel can
be drawnbetween mammalian playand mammalian rapid eye movement (REM) sleep,
whichis also omnipresentin mammalsbut absent in ectothermicvertebrates.Its modifications, including specializations such as unihemisphericsleep in dolphins (Tobler 1995),
A MULTIFACETED APPROACH TO PLAY:
are impressive. Its amount and distribution
THE PUZZLES OF PLAY
varysubstantiallyacross mammalian taxa and
From
our
major hypothesisabout the funcit is correlated with such ecological variables
as a safesleeping place, life-history
parameters tion ofplay,we have derivedanotherfourspeand niche cifichypotheses:thatself-handicappingis insuch as precociality/altriciality,
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164
THE QUARTERLY REVIEW OF BIOLOGY
tegralto play,thatplayis stimulatedbynovelty
and unpredictability,that play is associated
with a specificemotional state,and that play
presupposes high cognitivecapacity.Our hypothesis about function (i.e., ultimate causation) is complemented by hypotheses about
how thisfunctionis achieved (i.e., proximate
causation in termsofboth physicaland mental
processes involved in play), and why play is
more predominant in some animals than in
others (i.e., due to phylogeneticconstraints).
Strictlyspeaking, none of the four derived
hypothesesis a logical necessityfor our core
functionalhypothesisto be true.On one hand,
it may seem thatpresentingthese hypotheses
independentlywould be a more appropriate
approach; on the otherhand, function,proximatemechanisms,and phylogeneticconstraints
are intertwinedin numerous ways,and knowledge of these interactionsis essentialfora full
VOLUME
76
understandingof behavior (Curio 1994). This
is especially true for play. Play is a robust behavioral phenomenon with several puzzling
features,such as its kinematicand sequential
structure,and ontogenetic and phylogenetic
distribution.Anyfunctionalhypothesisabout
playmustbe comprehensiveenough to encompass these features,and most previouslypublishedhypothesesabout playhave attemptedto
do so. For instance, Burghardt's surplus resource model attemptsto incorporate physiological, life-history,
and ecological conditions
thatsupportthe evolutionofplay,and the sensitiveperiod hypothesisof Byersabout a neurodevelopmentalmechanism is closelylinked
to the motor trainingfunctional hypothesis.
This is whyour proposal, although centered
on function,is a complex theoryabout the natureofplay.We hope thatour new conceptual
frameworkwilllead to enhanced understanding of thisfascinatingbehavior.
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