CURRENT ANTHROPOLOGY
Vol. 25, No. 4, August-October1984
00
Research,all rightsreserved0011-3204/84/2504-0005$2
K 1984 by The Wenner-GrenFoundationforAnthropological
The EnergeticParadox of Human
Runningand HominidEvolution'
byDavid R. Carrier
FEATURE THAT DIFFERENTIATES
HOMINIDS fromother
primatesis notlargebrainsize, butthesetofcharactersassociated witherectbipedalpostureand a stridinggait.Long before
the rapid increasein relativebrainsize thattookplace during
thePleistocene,earlyaustralopithecines
possessedthepostcranial morphology
of an erect,stridingbiped (Lovejoy, Heiple,
and Burstein 1973). Evidence for the bipedal gait of early
hominidsis providedby the morphologyof the 3.5-millionyear-oldpostcranialmaterialfromthe Hadar Formationof
Ethiopia (Johanson, Taieb, and Coppens 1982, Lovejoy,
Johanson,and Coppens 1982),earlyPleistocenematerialfrom
eastern and southern Africa (Preuschoft1971), and the
Pliocenetrackways(3.6 to 3.8 millionyearsold) discoveredat
Laetoli in northernTanzania (Leakey and Hay 1979, White
1980). Together these suggest that early australopithecines
were relativelysmall-brainedcreatures,possessingstructural
adaptationsforuprightwalkingand runningthatin a broad
sense are remarkablysimilarto those of modernman. The
aspectsof locomotionthat unitethe hominidsas a groupare
also uniquelyhominidin characterand distinctly
peculiarfor
mammals.Consequently,the studyof human locomotion,in
additionto explainingmuchof the biologyof the one remaininghominid,mayproveto be one ofthemorepowerfulinductive approachesto the studyof hominidevolution.
The energeticcostoftransport
(oxygenconsumption
perunit
body mass per unit distancetraveled)forrunninghumansis
relativelyhighin comparisonwiththatforothermammalsand
runningbirds.Early comparativestudiesshowedthata mamTHE
1 This contribution
arose out of conversationswithD. M. Bramble
and S. C. Carrier.Furtherdevelopmentresultedfromdiscussionswith
C. Gans and M. H. Wolpoff.For criticalreviewand additionalimprovementof this manuscript,I am gratefulto S. L. Beck, D. M.
Bramble,S. B. Emerson,J. R. Fetcho,D. B. Jenkins,R. G. Northcutt,P. A. Pridmore,and R. 0. Whitten.
R. CARRIER is a doctoralcandidatein zoologyat the UniversityofMichigan(c/oDivisionofBiologicalSciences,University
of Michigan,Ann Arbor,Mich. 48109, U.S.A.). Born in 1955,he
was educatedat theUniversity
ofUtah (B.S., geology,1980;B.S.,
biology,1980; M.S., biology,1982). He views himselfas a functionaland evolutionary
morphologist
and is particularly
interested
in vertebratelocomotionand the ontogenyof themusculo-skeletal
system.His publicationsinclude"PostnatalOntogenyoftheMusculo-SkeletalSystemin theBlack-tailedJackRabbit(Lepuscalifornicus)" (JournalofZoology[London]201:27-55) and, withD. M.
Bramble, "Running and Breathing in Mammals" (Science
219:251-56). The presentpaperwas submittedin finalform9 I 84.
DAVID
Vol. 25
No. 4
mal thesize ofman shouldconsumeroughly0.10 ml ofoxygen
per grambodymass per kilometertraveled(Taylor,SchmidtNielsen, and Raab 1970), but the measuredvalue forman is
over twice this amount (0.212 ml). A recentanalysis of 64
speciesof runningbirdsand mammals(Taylor,Heglund,and
the initialobservationsthatthe cost of
Maloiy 1982) confirms
transportis relativelyhighforhumanrunners.
that among cursorial
It is somewhatsurprising,therefore,
mammalsman is one ofthebestdistancerunners.Whilegame
animalsare fasterovershortdistances,theygenerallyhave less
endurancethanman. Aside frompublishedaccountsofendurin thedomestichorseand camel,whichhave
ance performance
been bredforenduranceracing,verylittleis knownabout the
is available is
staminaof mammals.What littleinformation
usuallytakenfromanecdotalaccountsof animalsperforming
(see
in a varietyof climaticand topographicenvironments
comparisonsare
Howell 1965), and consequentlyinterspecific
hazardous.Comparisonsbetweenman and a numberofcursorial speciescan be made, however,in the contextof a contest
betweenpredatorand prey.
culturesare knownto run
Huntersof a numberof different
down preyby dogged pursuitoftenlastingone or two days
(Krantz 1968, Watanabe 1971). Bushmenare reportedto run
down duicker,steenbok,and gemsbokduringtherainyseason
and wildebeestand zebra duringthehotdryseason (Schapera
1930). TarahumaraIndians chase deerthroughthemountains
ofnorthern
Mexico untiltheanimalscollapsefromexhaustion
and thenthrottle
themby hand (Bennettand Zingg1935,Pennington1963). Paiutesand Navajo oftheAmericanSouthwest
are reportedto have huntedpronghornantelope(one of the
fastestof all mammals)withthissame technique(Lowie 1924;
AborigiFoster1830, citedby Lopez 1981:111).Furthermore,
nes of northwestern
Australia are known to hunt kangaroo
in thisway (Sollas 1924,McCarthy1957).In these
successfully
examplesthe staminaof preyanimals generallyconsideredto
be specializedforrunningand presumablyputtingforththeir
best effortprovesto be less than thatof man.
transportand endurancerunning
Energeticallyinefficient
would seem to be incompatible.The combinationofthesetwo
attributespresentsobvious morphologicaland physiological
problems.For instance,theremustbe a way ofdissipatingthe
mushighlevels of metabolicheat producedduringlong-term
cle action. In addition,extendedperiodsof high energydemand requirelargebodystoresofglycogenand fattyacids and
an effectivemeans of mobilizingthesestores.It is clear that
duringthe sequence of evolutionarysteps thatled fromprehominidsto Homo sapiens these problemshave been overcome. How this was accomplishedand what factorsmight
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1984
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483
have initiatedthissequence of specializationis the subjectof
the presentanalysis.
DISSIPATION OF METABOLIC HEAT
The normal core body temperatureof eutherianmammals
ranges from36?C to 38?C (Morrisonand Ryser 1952). The
lethalcore temperature
of thesemammalsis only6?C higher,
rangingfrom42?C to 44?C (Adolph 1947). Using empirical
measuresofthecostoftransport,
Taylor(1974) has calculated
that the maximal exerciseheat loads generatedby mediumsized and large animals (greaterthan 10 kg body mass) are
nearlyan orderof magnitudegreaterthan the maximalenvironmental
heat thattheyare likelyto encounterin nature.If
metabolicheat is producedmore rapidlythan it can be dissipated,bodytemperature
rises.Thus, adequate thermalregulationis criticalforanimalsthatrunforextendedperiods.For
and
example,cheetahssprintat speeds exceeding100 km/hr,
extrapolationof measurements
made at lowerspeeds suggests
thatat 100km/hr
heatproductionwouldbe morethan60 times
greaterthanat rest(Taylorand Rowntree1973a). The cheetah
storesmostof thisheat, and therefore
as it runsits bodytemperaturerises.Once therectaltemperature
reaches40.5?C the
animal refusesto run. Taylorand Rowntreeestimatethatifa
cheetahterminated
a sprintonce itsbodytemperature
reached
40.5?C, it could run for only 1 km. This approximatesthe
actual distancethatcheetahspursuetheirpreyin thewild. It
seems thatthe durationof the cheetah'ssprintmay be determinednot by fatiguebut by the amountof heat it can store
beforeit reachesa limitingbody temperature.
Mammals dissipateheat by evaporativeor nonevaporative
means. The Africanhuntingdog is exceptionalin thatit appears to dissipatelarge exerciseheat loads, forextendedperiods, throughnonevaporativemeans (Taylor et al. 1971).
Most medium-sizedto large mammals rely on evaporative
cooling to maintain body temperaturewhile running(see
Richards1970; Taylor 1974, 1977). Evaporativecoolingis accomplishedby two separatemechanisms:(1) respiratory
evaporationoccurringat thenasal mucosa,buccal, and tonguesurfaces(panting)and (2) evaporationof sweat fromthe general
body surface. Panting is almost universallyemployed by
medium-sizedto largemammals.The onlygroupsthatdo not
relyheavily upon pantingare the Old World Anthropoidea
(including man) (Robertshaw, Taylor, and Mazzia 1973,
Hanna and Brown 1983), horses, and camels (Robertshaw
1975). These threegroupsmaintainbody temperature
during
extendedexerciseby sweating.In additionto theseanimals,
some bovids (Taylor and Lyman 1972) and kangaroos(Dawson, Robertshaw,and Taylor 1974) also use sweat glandsfor
In contrast,suids (Robertshaw1975) and
thermoregulation.
some carnivores(Tayloret al. 1971)have sweat glandson the
generalbodysurface,but thesedo notappear to be associated
withthermoregulation.
Sweat glandson thegeneralbodysurface are lackingin Rodentia,Proboscidea(Robertshaw1975),
and Lagomorpha(Jenkinson1970).
SWEATING VS. PANTING
A numberofphysiologists
have consideredtheadvantagesand
disadvantagesof sweatingand pantingto achieveevaporative
cooling(Schmidt-Nielsen
1964,Hales 1974,Taylor 1977).The
presentdiscussionwill be confinedto thoseaspectswhichinfluencethermoregulation
duringexercise.
Evaporativecoolingfromthe respiratory
surfacesoffersthe
followingadvantagesover evaporativecoolingfromthe skin:
1. The skinof sweatinganimalsis cooler(as a resultof the
evaporation)than theskinof pantinganimals. When air temperatureexceedsskintemperature,
animalsgainheatfromthe
environment.
Accordingly,
pantinganimalshave a slowerin484
ward flow of heat fromthe hot environmentthan sweating
animals.Taylorand Rowntree(1974) have shownthatin a hot
environment
(47?C) heat flowsintosweatinganimalsat about
twicetheratethatit flowsintopantinganimals.For thesame
is low thecoolerskin
temperature
reason,whenenvironmental
in sweatinganimals resultsin a smallergradient
temperature
fornonevaporativeheat loss (heat loss by radiationwhenskin
temperatureexceeds ambient temperature).Thus, sweating
and are capaanimalsgain moreheat froma hotenvironment
ble of losingless heat by nonevaporativemeans than panting
ones.
evaporationto the nasal, buc2. Because pantingrestricts
cal, and pharyngealcavities,pantinganimals lose littlesalt.
Sweatinganimals,on theotherhand, mustdeal withlargesalt
losses (Schmidt-Nielsen1980).
3. Pantingprovidesforcedconvectionacross the evaporativesurfaces,whereassweatingrequiresanimalsto relyon free
convectionor wind. (This should not be a problemfora runif it lacks hair.)
ninganimal, particularly
Evaporative coolingfromthe skin offersthe followingadvantages:
1. Sweating provides an additional evaporative surface.
Taylor and Rowntree(1974) measuredthe maximumratesof
evaporativeheat loss froma groupof pantingand a groupof
sweatinganimalsin responseto exercise.They foundthatthe
ratesofevaporationfromtherespiratory
surfacesweresimilar,
but the sweatinganimals had much highermaximalratesof
evaporationbecause of the evaporationthat occurredat the
skinsurface.
cycle. As a
2. Sweatingis independentof the respiratory
runninganimal increasesspeed, its oxygenconsumptioninand Raab
creasesin a linearfashion(Taylor,Schmidt-Nielsen,
1970). However, as runningspeed changesit is unlikelythat
air flowrequiredformetabolismwillmatchthe
therespiratory
flowneeded forheat loss, since the rate at whichheat can be
and humidity.
dissipatedwill varywithambienttemperature
thebreathingcycleofquadrupedsis strictly
conFurthermore,
trolledby the body motionsof the runninganimal (Bramble
and Carrier1983). This couplingof locomotorand respiratory
cycleswill make it impossiblefora runninganimalto varythe
air flowover the respiratory
evaporativesurfacesto the same
degree that is possible in typicalstationarypanting.Conseof
and possiblythe total effectiveness
quently,the flexibility
pantingas a meansofevaporativecoolingmaybe limitedin a
runningmammal.Indeed, theamountof heat thatcan be lost
throughevaporationfromthe respiratorysurfacesseverely
limitsthemaximumrateofheat dissipationduringrunningin
animals that rely solely on panting (Taylor and Rowntree
1974).
In thiscontext,themechanismsofheatdissipationin thered
kangarooare ofinterest.This marsupialuses threeevaporative
coolingmechanisms:panting,sweating,and saliva spreading
(Dawson, Robertshaw,and Taylor 1974). However,it sweats
only during exercise. Under conditionsof severe thermal
stress,the restingkangaroopants and spreadssaliva. For the
redkangarooand othermammals,sweatingprovidesan additionalavenue ofheat dissipationthatmayoffermoreflexibility
and be morecompatiblewithrunningas a mechanismofthermoregulation.
RUNNING
HUMANS
The sweat glandsof man are distinctiveforthehighsecretory
levelat whichtheyoperate.No otherspeciesis knownto sweat
as much per unit surfacearea as man (Eichna et al. 1950,
Schmidt-Nielsen1964, Newman 1970). Human sweat glands
may also be subject to a higherlevel of neuronalcontrolthan
the sweat glands of otherspecies. At present,it appears that
onlycamels, horses,and Old WorldAnthropoideapossessdirectlyinnervatedsweat glands. The sweat glands of other
CURRENT
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ANTHROPOLOGY
groupseitherlack a nervesupply(e.g., canids) or possessone
thatdoes notmake directcontactwiththegland(e.g., bovids)
the neuronssupplyingthe
(Robertshaw1975). Furthermore,
glands of anthropoidprimatesare cholinergic,whereas the
glands of horses and camels are adrenergicallyinnervated.
of
Robertshaw(1975) has suggestedthatthe rapid hydrolysis
mayprovidethecholinerbyacetylcholinesterase
acetylcholine
gic glands of anthropoidprimateswithfinerneuronalcontrol
thanis possiblewithadrenergicmodes of transmission.
The rate at which heat is lost fromrunninghumans is
greatlyincreasedby theirrelativelack ofhair. The furcoat of
mostmammalsnotonlyinsulatestheanimalfromtheenvironfromheat promentalheat,but also insulatestheenvironment
duced by the animal. Accordingly,mammalswith thickindissipatingheat generated
sulatorycoats will have difficulty
throughexercise.The paucityof hair on the humanbody results in greaterthermalconductancethan would be possible
witha fullcoat ofhair. The thermalconductanceofa hairless
increasedby theincreasedconvecmammalshouldbe further
tion duringrunning,as the animal moves throughthe air.
Mammals withthickcoats will not experiencethisincreasein
convectionwhen running.Cena and Monteith(1975) have
shown that the thermalconductivityof sheep fleece(4 cm
In rabbits,
thick)is notaffectedby air flowofup to 18 km/hr.
of
wind speeds below 11 km/hr
do not affectthe conductivity
thefur(1.8 cm thick),but an increaseofwindspeed to 18 km/
It appears thatair movingparallel
hrdoublesitsconductivity.
to the surfaceof furcoats at speeds equivalentto endurance
failsto penetrate
runningspeedsofhumans(i.e., 10-20 km/hr)
or even disturbthe stagnantair trappedbetweenthe hairsof
othermammals.This stagnantair providesnearlyall thethermal resistanceof the system.The adaptive value of man's
largelyglabrousconditionmay, more than anythingelse, be
of heat dissipationwhile running.
the facilitation
In summary,the combinationof well-developedsweat
glandsand the relativeabsence of bodyhair in man makes it
probablethatrunninghumansdisplayveryhighthermalconductance,withmaximalvalues well above thoseofmostcursorial mammals. The human mechanismsof thermoregulation
(sweating,as opposed to panting,and hairlessness)are probably more effectiveat dissipatingmetabolicheat producedin
runningthan are the regulatorymechanismsused by other
mammaliancursors.Supportingthis is the observationthat
certainsweatingprimates(i.e., spider monkeys,stump-tail
macaques, baboons, and chimpanzees)are capable of greater
maximumrates of heat dissipationduringrunningthan are
mammals dependent upon panting (Taylor and Rowntree
of maximalratesof heat
measurements
1974). Unfortunately,
dissipationfrom large animals during exercise are almost
and so directcomparisonswithman cannotyetbe
nonexistent,
made.
Carrier:HUMAN
RUNNING
AND HOMINID
EVOLUTION
gariaet al. 1963,Cavagna and Kaneko 1977). Consequently,a
man runninga marathonwill consumethe same amountof
energyfor transportwhetherhe runs at a slow jog or at a
world-classpace.
WALKING
Unlikehumanrunning,humanwalkingis at least as economical as the walkingof typicalmammalianquadrupeds (Rodman and McHenry1980; also see Tucker 1975).The efficiency
in walkingis related,in part,to a finelytunedsystemof storage and recoveryof the energyused formotionwithineach
stride.Walkingbirdsand mammalsbenefitfroman exchange
betweenthe kineticenergyand the gravitationalpotentialenergyof the centerof mass withineach stride(Cavagna, Heglund, and Taylor 1977). Gravitationalpotentialenergyis
storedas thecenterof mass risesduringa step. This energyis
thenrecoveredas the body fallsforwardand is subsequently
convertedback into potentialenergyas the centerof mass
again rises over the otherleg. For this reason, walkinghas
been likenedto an invertedswingingpendulumor an egg rollingend overend (Cavagna, Saibene, and Margaria1963). The
bipedal postureof man is ideallysuitedforthispendularmotion.Throughoutmostofthesupportphase,thelimbpivotson
a plantigradefoot.In contrastto the situationof mostquadrupedal cursors,no musculareffortis requiredto maintain
ankle extension.Most importantly,
the centerof mass rollsin
an arc over the pointof support(foot)on a relativelystraight
leg, so that the potentialenergygained in the rise roughly
equals thekineticenergylostin thedescent(Alexander1976).
Energysavings due to this transferbetweenpotentialand
kineticenergyare substantial.In humanswalkingat a speedof
therecoveryofmechanicalenergyatapproximately
4 km/hr,
tains a maximumof 65-70% (Cavagna, Thys, and Zamboni
1976). Equivalentsavingshave beenmeasuredin bipedalbirds
(turkeyand rhea) walkingat similarspeeds (Cavagna, Heglund, and Taylor 1977). In contrast,the percentagerecovery
240200 v) 160 -
_ 120 -
\
>
_
COST OF TRANSPORT
twiceas muchenergy
Runninghumansexpendapproximately
per unitmass as typicalmammalianquadrupedsof the same
size but are neverthelessadept at endurancerunning.Man's
capacityforendurancelocomotion,bothrunningand walking,
may resultfromthe way in whichthe cost of transportvaries
with the speed of travel (fig. 1). First, humans walking at
optimalspeed consumeonlyhalftheenergy(used in transport)
requiredto cover the same distancewhile running(Cavagna
and Kaneko 1977, Rodman and McHenry 1980). This is
clearlynot the case forhorses(Hoyt and Taylor 1981) or for
otherlarge cursors(see Taylor, Heglund, and Maloiy 1982).
Second, while quadrupedal cursorshave specificspeeds at
whichenergyexpenditureis minimizedforeach of theirvarious gaits (Hoyt and Taylor 1981), the cost of transportfora
runninghuman does not depend on speed (Boje 1944, Mar-
80
40
4
8
12
16
Speed (km *hr-')
20
24
FIG. 1. The energeticcostsofwalkingand runningin thehorseand in
man. The oxygenconsumedin movinga unitdistanceis minimizedat
a narrowrangeofspeed in all threegaits-walk, trot,and canter-of
the horse (dashed curves)and in the walk of man (solid curve). In
contrast,the costoftransportis independentof runningspeed in man
(solid line). (ModifiedfromHIoytand Taylor 1981and Margariaet al.
1963.)
Vol. 25 * No. 4 * August-October
1984
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485
appears to be lowerin quadrupedalmammals.Rams walking
at intermediate
speeds(3-4 km/hr)
recovera maximumofonly
35%. Dogs and monkeysrecoverno more than 50% of the
mechanicalenergyused while walking(Cavagna et al. 1977).
The efficiency
ofwalkingchangeswithspeed (Cavagna and
Kaneko 1977, Hoyt and Taylor 1981). This is trueforboth
men and horses (fig. 1). There is an intermediatespeed at
whichthe energeticcost to walk a unitdistanceis minimized.
As velocityis increasedor decreasedaway fromthisoptimal
speed, thecostoftransportrisesrapidly.The costoftransport
fora walkinghumanis minimizedat speeds rangingfrom5 to
6 km/hr.The optimal walking speed of the largerhorse is
slower(4 to 5 km/hr).
Optimalwalkingspeedsare related,in part,to theenergetic
propertiesof the contractilecomponentof skeletal muscle.
There is a speed of muscle shorteningat which efficiency
is
maximized(fora review,see Goldspink1977). This demands
that,in termsofenergyexpenditure,
therebe an optimalstride
frequency.Also, the abilityof muscle to generateforcediminishesas themuscleis stretchedbeyondor shortenedbelow
itsso-calledoptimallength(Gordon,Huxley,and Julian1966).
Consequently,theremustalso be an optimalstridelengthwith
regardto muscle function.Because speed is the productof
stridelengthand stridefrequency,
thecontractile
of
properties
muscle can be expectedto limitanimals to energetically
optimal speeds in all gaits. However, forrunninghumans this
appears not to be the case.
RUNNING
whichthelungsare ventilatedduringrunning.When a quadruped trotsor gallops, the muscles and bones of the thorax
must absorb the shock of impactingon the frontlimbs. In
addition,duringa gallop all mammalsexhibitsome degreeof
axial bendingin thedorso-ventral
direction.This motioncompressesand thenexpands the thoracicspace witheach stride.
These aspectsof gait restrictthe ventilationof quadrupedsto
one breathper locomotorcycle (Bramble and Carrier 1983,
Hornicke,Meixner,and Pollmannn.d.). In contrast,the uprightbipedal gaitofhumansmakes possiblea largenumberof
breathingpatterns(e.g., two stridesper breath,threestrides
perbreath,etc.). Therefore,whilethebreathingfrequency
ofa
runningquadruped equals its stridefrequency,man can vary
breath frequencyrelativeto stridefrequency(Bramble and
Carrier1983).
The objective of lung ventilationis to meet the metabolic
demand for oxygen.However, in runningmammals this is
morecomplexthan is generallyrecognized.As runningspeed
increases,the need for oxygenincreasesrapidlyin a linear
manner(Taylor, Schmidt-Nielsen,and Raab 1970). For any
givenlevel ofaerobicexertion,thetissues'needforoxygenwill
be metby a specificlungminutevolume,whichis theproduct
of the breathingfrequencyand the tidal (lung)volume.However, as a consequenceof the elastic resistanceof the thorax,
airwayresistance,and dead-space volume,thereis a specific
rateand depthofbreathing,foranyminutevolume,thatmaximizes ventilatoryefficiency(Otis, Fenn, and Rahn 1950,
Crosfilland Widdicombe1961,Yamashiroand Grodins1973).
A furtherlimitationresultsfromthe way in which speed is
variedwhilerunning.There appears to be a specificcombinationofstridelengthand stridefrequency
thatminimizesenergy
foranyrunningspeed(Knuttgen1961,Cavanagh
consumption
and Williams1982). For sustainedeconomicaltransport
a runningmammal must therefore
(1) employan energetically
appropriateblendofstridelengthand stridefrequency,
(2) match
themetabolicdemandforoxygenvia lungventilation,
(3) ventilatethe lungs with an energetically
suitablecombinationof
breathfrequencyand volume, and (4) breathein synchrony
withthe locomotormotionsof the body.
The tight1:1 couplingbetweenbreathand stridefrequency
ofquadrupedsmay therefore
resultin a runningspeed,within
each gait, thatis energetically
optimalforbreathing.As running speed divergesfroma theoretically
optimalspeed, the
motionsofthebodynecessaryforbreathingmaybeginto interfere with the motionsrequiredfor running,decreasingthe
of the entiresystem.This would have the effectof
efficiency
making the cost of transportdependenton runningspeed
(withina singlegait),as ithas beenshownto be in thehorse.In
contrast,thecapacityofhumansto alterthebreathingpattern
while runningwould eliminatethis problem. The striding
bipedal gait of humans, by relaxingconstraintsimposedon
lung ventilation,may broadenthe rangeof speeds whichare
viable.
energetically
The lack of an optimalrunningspeed could be viewed as a
disadvantage,because everyspeed withintheaerobicscope of
man is as costlyas any other.This is particularly
in
significant
thatman is a relativelyinefficient
runnercomparedwithother
mammaliancursors.On the otherhand, giventhe physiology
necessaryto cope withhighlevels of energyconsumptionand
metabolicheat production,a constantcost of transportcould
providehumanswiththeoptionofrunningat a wide varietyof
speeds. Quadrupeds,such as thehorse,thatappear to be specializedfora narrowrangeofspeedswithineach gaitmayin a
practicalsense be limitedto theseoptimalspeeds.
As is the case forwalking,the energeticcost of transportfor
runningquadrupeds appears to change with speed, being
minimalat intermediate
speeds withineach gait. By training
horsesto extendtheirgaits beyondnormalspeeds, Hoyt and
Taylor (1981) have shownthatforeach gait thereis a specific
speed at which the amountof oxygenused to move a given
distanceis minimal(fig.1). When the horseswere allowed to
selecttheirown speeds, theychose speeds thatcoincidedwith
theenergeticoptimumwithineach gait. The optimalspeed for
each gait is also the preferredspeed. As a result,thereare
rangesof speed that the animals neveruse forany sustained
period. Evidence thatothercursorialmammalshave optimal
runningspeeds comes fromthe observationof Pennycuick
(1975) that migratingwildebeestand gazelle use only a restrictedrangeof speeds withineach gait.
Given theseobservationson whatmightbe expectedto be a
generalpatternforvertebrates,it is somewhatsurprisingto
findthat Homo sapiens does not have a singleenergetically
optimalrunningspeed. Over therangeof speeds(8-20 km/hr)
used byhumanswhenrunninglongdistances,thecostperunit
distancedoes notvarysignificantly
withspeed (Margariaet al.
1963, Cavagna and Kaneko 1977, Hagan et al. 1980). The
recognitionof this apparentdifference
betweenhumans and
quadrupedsraises two immediatequestions.First,what is it
about humansthat detachesthe cost of runningfromspeed?
Second, what advantagesor disadvantagesdoes thisunusual
situationcreatefortherunninghuman?Althoughtheanswers
to thesetwo questionsawait further
several
experimentation,
pointscan be made.
Thereis no evidenceto suggestthatthereis anythingparticularlyunusual about human skeletalmuscle. It seems to be
subjectto the energeticand mechanicalconstraintstypicalof
othervertebrateskeletalmuscle(see Thorstensson1976). Furthemarkedabilityofhumansto make use ofenergy
thermore,
storedelasticallyin the tendonsand muscles while running
(Cavagna and Kaneko 1977) is not unusual for mammalian
cursors(Cavagna, Heglund,and Taylor 1977). GiventheordiSTORAGE AND UTILIZATION OF ENERGY
narynatureofhumanskeletalmuscle,man would be expected
to exhibitan optimalrunningspeed.
Depletionof muscleglycogenstoresis one factorthathas been
implicatedin the developmentof muscle fatigueduringproMan does differfromquadrupeds,however,in the way in
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ANTHROPOLOGY
longed exercise,forcinganimals to stop or slow theirpace
(Ahlborget al. 1967,Bergstromet al. 1967). The rateat which
muscleglycogenis depleteddependson thelevel ofblood glucose (suppliedby liverglycogen)and the rateof fatoxidation
(Holloszyand Booth 1976). Consequently,thehighmetabolic
rate of runninghumans combinedwith theirgreat stamina
leads to the predictionthatconditionedpersonswill have unusuallylargereservoirs
of(1) muscleglycogenand triglycerides
(whichcan be hydrolyzedto freefattyacids), (2) triglycerides
storedas adipose tissue,and (3) liverglycogen.At presentthe
literature
does notcontaintheinformation
necessaryto address
thisissue. The body'sreservoirofglycogenand freefattyacids
variesdramaticallydependingon the diet and physicalconditionof the animal (Bergstromet al. 1967, Paul and Issekutz
1967). This combinedwitha relativelack ofinformation
from
species otherthan man makes interspecific
comparisonsimpossibleat thistime.
A diet enrichedin carbohydrates,maintainedfor several
days,doublesmuscleglycogenand enhancesendurancein humans (Bergstromet al. 1967, Karlssonand Saltin 1971). Conversely,a dietrichin proteinand fatdecreasesmuscleglycogen
and prematurely
depletesglycogenduringexercise(Gollnicket
al. 1972). Humans can adjust theconcentration
of glycogenin
the muscles,and thus theirphysicalperformance,
by shorttermchangesin diet. It is unknownwhetherthis allows humans to concentrateglycogenat higher levels than those
reachedby othermammals.Presumablytheoptionof "carboloading"is notavailable to thosepredatorsthatare strictcarnivores(e.g., canids and felids).
During exercisethe mobilizationand rate of utilizationof
carbohydrates
and fattyacids by musclesis controlledlargely
by the circulatingconcentrations
of fivehormones:epinephrine,norepinephrine,
adrenocorticotrophic
hormone(ACTH),
glucagon,and thyroxine
(Stryer1975). Because onlylow levels
of thesehormonesare storedin the body,a freshsupplymust
be synthesized
as theneed arises.Withtheexceptionof glucagon and ACTH, all are producedby the thyroidand adrenal
glands.As has been notedby Spuhler(1979), theseglandsare
relativelylarge in humans. Spuhler suggeststhat relatively
largeglandsize mayresultin higherlevelsofhormoneproductionand, in turn,could be associatedwiththe highenergetic
demandsof humanendurancerunning.
ENDURANCE RUNNING AND PREDATION
There are importantdifferences
in locomotionbetweenman
and typicalquadrupeds(fig.2). In mostquadrupeds,heat dissipationis coupled to the respiratory
cycle. This in itselfis
likelyto decreasethecapacityto dissipateheat whilerunning.
Added to it is thelimitationthatenergy-efficient
lungventilation requiresa specificcombinationof breathfrequencyand
volumeforany minutevolume.The breathingcycleis in turn
largely controlledby the locomotorcycle, which is energeticallylimitedto a specificcombinationof stridefrequency
and lengthforany givenrunningspeed. These suggestedconstraintsmay combineto forcea mammalto run at a narrow
rangeofspeedsin each gaitand limititsmaximumrateofheat
dissipation.In contrast,in man heat dissipationis not tied to
respiration,and lung ventilationis largelyindependentof
locomotion.Therefore,runninghumansshoulddisplaygreater
plasticityin thecriticalfunctionsof respiration
and heat dissipationthan runningquadrupeds.
Comparedto thatofothermammals,man'senergeticcostof
transportis relativelyhigh. Nevertheless,humanspossessexceptional locomotorstamina. Several of the charactersbelievedto contribute
to man'sendurancecapacitymaybe primitive charactersforOld WorldAnthropoidea:
1. The combinationofcholinergicsweat glandsand general
absenceofbodyhairprovidesman withan effective
meansfor
Carrier: HUMAN RUNNING AND HOMINID
EVOLUTION
dissipatinglarge exerciseheat loads. Sweat glands that are
controlledby synapsing,cholinergicneurons occur in Old
World anthropoidsand appear to be confinedto this group
(Robertshaw 1975). These primatesare capable of greater
maximalratesof evaporativecoolingduringexercisethanare
certaincursorialmammalsthat depend on pantingforthermoregulation(Taylor and Rowntree1974). Many of the great
apes (Pongidae)have large bald areas (lack hair) on the face,
chest,and rump.
2. The arborealmodes of locomotionof manyanthropoids
necessitatemodifications
ofthelimbsand trunkthatare transitional to uprightbipedal postureand allow limitedbipedal
locomotionin some modernforms(Tuttle 1975). This trend
towardsbipedalitypresentsthepossibility
ofenhancedtransfer
betweengravitationalpotentialand kineticenergywhilewalking. Bipedalityalso releases the mechanicalconstraintsimposed on the breathingcycle by locomotion,therebymaking
possiblea varietyof breathingpatterns.
3. The adrenal and thyroidglands of primatesare hyperplastic comparedwith those of othermammals(see Spuhler
1979). This hyperplasticity
may increasethe levels of those
hormonescriticalto the mobilizationand utilizationof fatty
acids and glucoseby muscles.
4. The omnivorousdiet of mostanthropoidsopens up the
ofincreasedglycogenstoragein themusclesthrough
possibility
carbo-loading.
Hence, in these respectshominidsmay have been preadapted to endurancerunning.However,in orderto become
an endurancerunnerman has had to overcomethe handicap
imposedby a relativelyhighenergeticcostoftransport.Given
thisconstraint,
thefactthathumanshave exceptionalstamina
suggeststhatat some pointin the evolutionof hominidsthere
was strongselectivepressureforendurancerunning.
Mammals runfora limitednumberof purposes.Runningis
oftena formof play, especiallyamongyoungcursorialmammals. This is likelyto be of value mainlyforthe conditioning
and trainingit provides for runningunder other circumstances.In someinstancesrunningis used formigration.However,mostspeciesmigrateat a walk, and runningis reported
to be rarein thiscontext(Pennycuick1975). Preyanimalsdepend heavily upon runningspeed and enduranceto avoid
predators.Because of the greatspeed of the large predators,
runningis unlikelyto have been of muchvalue to man's early
ancestorsas a meansofescape. Runningis also used by predatorsto captureprey.Predationis a behaviorin whichrunning
endurancerunning,mighthave been useability,particularly
ful to early hominids.Althoughmost mammalianpredators
relyon speed and accelerationto overtakepreyanimals,a few
groups(e.g., Lycaon)make use ofexceptionalendurance.The
physiologyand morphologyof modernman, combinedwith
what is knownfromhominidfossils,suggestthatlongbefore
the developmentof complex cultureand huntingweapons,
earlyhominidsmay have been endurancepredatorsequipped
withbiologicalweapons forhuntingverydifferent
fromthose
of othermammalianpredators.
of
If, as is thecase forrunninghumans,thecostoftransport
early bipedal hominidsdid not change with runningspeed,
thentheywould have been freeto pursuepreyat any speed
withintheiraerobic range. They could therefore
have picked
the speed least economicalfor a particularprey type. This
would have forcedthe preyto runinefficiently,
expeditingits
eventualfatigue.For example,a man in runningpursuitof a
horsewould do best to proceedat roughly16-17 km/hr.This
is thespeed midwaybetweentheoptimalspeed ofthetrotand
theoptimalspeed of thegallop (fig.1) and is a speed at which
the animal prefersnot to run (Hoyt and Taylor 1981).
An animal pursued at its least economicalrunningspeed
would he faced with two ontions.It could maintaindistance
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1984
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487
CONSTRAINTS ON SUSTAINED RUNNING
QUADRUPED
Stride Frequency
X Stride Length
MAN
Stride Frequency X Stride Length
Locomotor - RespiratoryCoupling
Breath Freq. X Breath Vol.
I
Respiration
B. F. X B. V.
Heat
Heat
Dissipation
Dissipation
on thecircled
possibleconstraints
and in man.Boxesrepresent
mammals
in typicalquadrupedal
running
on sustained
FIG. 2. Constraints
andheatdissipation.
ofrespiration
functions
fromthe predatorby runningat the nonoptimalspeed, or,
morelikely,it could race ahead at a fasterand moreefficient
speed. The latterof thesetwo escape strategieswould lead to
intermittent
runningand resting.The preyanimalwould outdistancethe predatorand, upon stoppingto catch its breath,
would findthatthe predatorwas stillin pursuit,forcingit to
chargeoffonce again. It would be forcedintoan intermittent
needsto avoid thepursuing
runningpatternby thecontrasting
fatigueand heatstressifthe
predatorand to avoid unnecessary
predatorhas given up the chase. This seems, frommy own
observation,to be what happens when pronghornantelope
(Antelocapra)are pursuedby a runninghuman.
runningprovidesbriefrestperiods,it
Althoughintermittent
is probablyless economicalthancontinuousrunning.Tests on
exercise
of intermittent
humansshow thatthe workefficiency
on cycleergometers
can be as muchas 26% lowerthanthatof
continuousexerciseat the same average power output(Edwards et al. 1973). Comparedwithcontinuousexercise,intermittent
exercisehas also been shownto elevatecorebodytemperatureand decrease evaporative heat loss as a resultof
reducedsweating(Ekblomet al. 1971).Therefore,whetherthe
preyran at thepace set by thetheoreticalpredatoror choseto
transthe end resultwould be inefficient
run intermittently,
port.In a contestofendurance,a predatorwhosecostoftransport did not vary with runningspeed would likelyhave a
substantialadvantage over a preyanimal that possessed reoptimalspeeds in each gait.
stricted,energetically
In theexampleofa man attempting
to rundowna horse,the
ofthehorsewould likelyoutweighany
muchgreaterefficiency
benefitthattheconstantcostoftransport
providedtheman. In
all probabilitythe man would become exhaustedlong before
the horse. However, part of the reasonthathorsesare much
in body size bemoreefficient
than humansis the difference
tween the two species. The cost of transportscales to the
-0.40 power of body mass (Taylor, Schmidt-Nielsen,and
Raab 1970). In general,largemammalsconsumeless energyin
locomotionthando smallmammals.Wherepredatorand prey
are equal in bodysize or thepreyis smaller,a constantcostof
488
transportcould give a predatora distinctenergeticadvantage
ifthe preyhad specificoptimalrunningspeeds.
Anotheraspectofhumanbiologythatwouldbe usefulforan
endurancepredatoris man's exceptionalabilityto dissipate
heat whilerunning.It is truethatthegreaterenergyconsumption of runninghumans generatesa relativelylarge exercise
heat load. However, the well-developedsweat glandsof man
make the whole body surfaceavailable forevaporativecooling. Since evaporativecoolingin humansis notlimited,as it is
in pantingmammals,by the rate and volumeof lung ventilaa meansofthermoregulation
thatis compattion,it represents
ible with running.In addition,one fortunateconsequenceof
the lack of body hair in humans is an increasein thermal
conductancewith increasingrunningspeed (apparent wind
speed). Higher rates of convectionwith increasingrunning
speedwillbe muchless prevalentin mammalsequippedwitha
moretypicalcomplementof bodyhair because of thestagnate
layer of air maintainedby the fur. These thermoregulatory
characteristics
of man would certainlybenefitan endurance
predator.
There is some anecdotal evidence which suggeststhat the
way in whichhumansdissipateheat whilerunningdoes playa
role in humanhunting.Dawson, Robertshaw,and
significant
Taylor (1974) found that in spite of sweatingand increased
respiratory
cooling,redkangaroosare unableto dissipateall of
the heat producedwhile runningat speeds between4 and 22
km/hr.
Theycalculatedthat,hoppingat speedsin thisrange,a
kangaroo would reach a lethal temperaturein one to two
hours.Consequently,itcomesas no surprisethatAboriginesof
thewarmdesertof northwestern
Australiaare reportedto run
down kangaroos(Sollas 1924, McCarthy1957). On veryhot
summerdays it is a relativelysimplematterfora man to chase
down the hare, Lepus californicus(Schmidt-Nielsen1964),
thoughin thecool ofearlymorningor duringthewinterthisis
a seeminglyimpossibletask. Hottentotsare reportedto run
swiftpreyanimalsto exhaustionin the heat of the sun (Schapera 1930). Furthermore,
Bushmenare knownto run down
wildebeestand zebra duringthehotdryseasonbutuse alternaCURRENT
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ANTHROPOLOGY
tivemethodswhenhuntingtheseanimalsduringotherseasons
(Schapera 1930).
This analysisof the morphologyand physiologyof human
locomotion,althoughincompleteand largelyspeculative,suggeststhat man is a primatethat has become specialized for
(among other things)endurance running.This points to a
scenarioconcerningthe originof hominidsthathas been proposed in one formor anotherby several authors(Dart and
Craig 1959,Ardrey1961,Morris1967, Krantz1968). Exercising anthropoidprimatescan dissipateheat morerapidlythan
certain cursorial mammals. This suggeststhat the earliest
at heatloss thanmany
hominidsmayhave been moreeffective
mammals. Furthermore,
early australoothercontemporary
pithecineswerefullybipedal. As a result,theywere probably
notconstrainedto thetypical1:1 breathingpatternof running
quadrupeds.Consequently,itis possiblethatone oftheimporhominidsfromother antant factorswhich differentiated
thropoids,and ultimatelyled to the evolutionof H. sapiens,
was the occupationof a new predatoryniche. This hypothetical nichewas thatofa diurnalpredatorwhichdependedupon
to disable
exceptionalendurancein hot(midday)temperatures
swifterpreyanimals.
These hypotheticalearly hominidswere endowed with a
physiologyand morphologythat (1) allowed runningspeeds
whichforcedpreyto escape in an inefficient
mannerand (2)
provided rates of maximumheat dissipationthat were far
above ratesobtainablebytheprey.Exploitingthisbroadrange
the
of runningspeeds and superiorabilityto thermoregulate,
early hominidswere able to capture swiftprey animals by
temperpursuingthemunderconditionsofhighenvironmental
atureand at speedsdifferent
fromthoseforwhichtheanimals
were physiologicallyspecialized. Initiallythe prey animals
would have been notthelargeungulatesbut theless cursorial
hares and small artiodactyls(such as Serengetilagusand
Raphicerus,whichoccurin theLaetolilBeds [Leakeyand Hay
1979]) and the relativelyhelpless infantsof the largerherd
animals.
it has been arguedon the basis of limb morAlternatively,
may not have been parphologythatearlyaustralopithecines
ticularlyskilled runners(Jungers1982, Stern and Susman
1983). Also, analysisof the tools and animal bones fromexcavated Oldowan campsites(Leakey 1971),alongwithwhatis
knownof dental morphology,suggeststhathuntingmay not
have been an importanthominidactivityuntiltheearlyPleistocene(Wolpoff1980). In thiscase, thisscenariowould better
applyto theevolutionoflocomotionin Homo and mightserve
to distinguish
Homo fromtheaustralopithecines.
Whetherthe
Hominoidea arose as a consequenceof a shiftto a predatory
or a divergingsubgroupbecame huntersat a much
life-style
laterpoint,thepredatorynicheis themostobviousexplanation
formany of the unique charactersof the primateknown as
man.
The modelofearlyhominidsas diurnalendurancepredators
to
leads to severaltestablepredictions.It would be worthwhile
ofman and modernprey
evaluatetheenduranceperformances
animals under a variety of temperatureregimens.If this
of man
scenariohas any validity,the enduranceperformance
relativeto thatof preyanimals shouldincreasewithambient
temperature.In addition,the speeds at whichmodernprimitivehuntersrundown preyshouldvaryfromspeciesto species
and shouldcorrespondto thepreyanimal'snonoptimalspeed.
The questionof whetherthe constantcost of transportof human runnersresultsfromthe wide varietyof breathingratios
used by runninghumansis also relevantto thisscenario.This
could be testedby measuringoxygenconsumptionin human
runnerswho have been trainedto extendtherangeofspeed at
which the different
breathingratiosare normallyused. The
scenarioalso predictsthatearlyhominidswerescantlyhaired.
Unfortunately,
thefossilrecordis unlikelyto yieldevidenceon
thispoint.
Carrier:HUMAN
RUNNING
AND HOMINID
EVOLUTION
Comments
byA. K. KAPOOR
DepartmentofAnthropology,
University
ofDelhi, Delhi 110
007, India. 12 iv 84
This enlighteningarticle on various aspects of bipedal and
quadrupedal locomotiondoes not call formuch commentexcept to link mode of locomotionwith brain size and human
evolution.Man can exhausta preyanimal duringtheheat of
the day, not in the cool of the morning.This phenomenon
requiresa senseof timing,i.e., of whento hunt,whichmeans
thinkingand hence the brain. When did the brain grow
large-at the beginningof bipedal locomotionor huntingby
early hominids?This question and the consequencesshould
have been discussedhere.
by TASUKU KIMURA
Primate Research Institute,Kyoto University,Inuyama,
Aichi 484, Japan. 13 Iv 84
Carrierproposesthenew hypothesisthatancestralman could
pursue a preyof a large body size at the speed energetically
least economicalfortheanimal. The hypothesisis veryattracit. An energetically
tive,buthe does notdemonstrate
optimum
mammalshas beenexperispeedin quadrupedalterrestrial
mentally
proven
toexistonlyinhorses(HoytandTaylor1981).
Horseschangegaitpattern
(walk,trot,or gallop)and select
speeds in a mannerthat minimizesenergyconsumption.
to terrestrial
mammals
Whether
thisfinding
appliesgenerally
Preas HoytandTaylorassumehas notyetbeendetermined.
onmanykindsofanimalsarecalled
ciseexperimental
analyses
for.On theotherhand,thisfinding
thelinear
doescontradict
and bodymass
relationship
betweenenergy
costoftransport
fordifferent
mammalsshownby Taylor,Schmidt-Nielsen,
and Raab (1970). That relationshipwas simplyobtainedfrom
oneunitofbodymassoveroneunit
theenergy
costofmoving
ofdistanceat infinite
oneunit
speed.Sincethecostofmoving
ofbodymassoveroneunitofdistance
dependsonthespeedof
fromtheslopeoftheregression
theanimal,itis notcalculated
linebetweentheenergy
costperunitbodymassand perunit
timeand speed as Schmidt-Nielsen
(1975:248)proposed.
Man'slackofan energetically
optimalrunning
speedis exwiththecapacityofhumans
plainedbyCarrierin connection
toaltertheirbreathing
tostride
He
relative
patterns
frequency.
andhiscoworker
(BrambleandCarrier1983)foundthatquadrupedalmammals(hares,dogs, and horses)normally
synchronize
theirlocomotor
and respiratory
cyclesat a constant
ratioofstrideperbreadth.Theiroriginal
datashowedthata
in humanrunning,
2:1 ratioappearedto be favoured
though
severalbreathing
wereavailable.It is difficult
to expatterns
costofhumanrunning
plainthecontinuously
regularenergy
relative
to speedin connection
witha ratiothatis discontinuous in character.
It is reasonable
thatthehumanmechanisms
ofthermoreguin running
andhairlessness,
aremoreadvanlation,sweating
this
usedbymanymammals,
tageousthanthepanting
though
is nota newviewpoint.
Readersshouldbe awarethatcutaneousevaporation
is important
notonlyin
forthermoregulation
thethreegroupsmentioned
butalsoinmanyungubyCarrier
lates,suchas donkeys,
llamas,andcattle(Whittow
1971).This
doesnot,however,
influence
thefactthathumansweatglands
maybe themosteffective.
Sakura(1983)has proposedthehypothesis
thatancestral
manoccupieda new nicheof diurnalpredator.
Mostcarnivoresin thetropicsare activeduringtimesoflow temperature
and not at midday. Early humans,as newcomers,may have
Vol. 25 * No. 4 * August-October
1984
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489
adopted the hot daytimefortheirhuntingactivity.This hypothesisexplainsman's highlydevelopedmechanismsof thermoregulation,
thoughit is insusceptibleto directproof.
The bipedal walking of living nonhumanprimatesis not
energeticallyeconomical compared with that of humans
(Yamazaki et al. 1979). In humanerectwalking,thecenterof
gravityof the body risesin the stance phase (Cavagna, Heglund, and Taylor 1977). In nonhumanprimates,on the contrary,the centerof gravityof the body drops in the stance
phase of walking because the knee joint continuesto flex
(Yamazaki et al. 1979; Kimura et al. 1983). Nonhumanprimatesdo not"run"bipedallyin thesenseofconstantly
having
a phase of freetransit(Kimuraet al. 1983). The locomotionof
man's ancestorscould not have differedentirelyfromthatof
living nonhumanprimates.On the otherhand, when man
regularlyhunted relativelylarge animals on the groundhe
must already have practisederectbipedal walkingand running.Man's acquisitionofbipedalwalkingand runningcannot
be explainedin termsof energycost alone.
by MARTIN K. NICKELS
DepartmentofAnthropology,
Illinois State University,
Normal, Ill. 61761, U.S.A. 29 III 84
That persistencehuntingbased on endurancerunningis employedbysomehunterstodayis notnecessarilygermaneto the
issue of whetherit was an aspect of the initialexploitationof
the hominids'diurnalhuntingniche. How prevalentis such
endurancerunningin thesemodernhuntinggroups?Is it the
primarytactic employed?Just how energy-efficient
is it in
termsofoptimalforagingtheory(Hill 1982)?Is thereevidence
that endurancehuntersengage in "carbo-loading,"or is this
merelya trainingpractice employed by competitivelongdistancerunnersforsportingevents?
Despite thesequestions,I am in basic agreementwithCarrier's (and others')conclusionthat occupation of a diurnal
hunting(and I wouldadd scavenging)nicheis a majorfeatureof
the hominidevolutionarypattern.The question is whether
endurance runningis necessaryto explain what we know
about early hominidsubsistencepatterns;I thinknot. The
ofanimalcararchaeologicalevidenceofdeliberatebutchering
casses at australopithecine-grade
(includingHomo habilis)sites
in East Africabeginningat about two millionyearsago does
not indicatehow theseanimals died (Isaac 1983). As Carrier
himselfadmits,the evidencecould equally supporteitherdeliberatehuntingor scavenging.Wolpoff(1980:151)pointsout
thatthenatureof theskeletalremainsfromthelargeranimals
is consistentwiththeirhavingbeen scavengedfromcarnivore
kills. Additionalsupportof scavengingis the reportof Shipman (1984) that some cut marks directlyoverlie carnivore
toothmarks on some early Olduvai Gorge faunal remains.
that chimpanzeesand baboons are capable of
Furthermore,
occasionalsmall-gamecooperativehuntingbased on suchtechniques as seizing,briefchasing,stalking(Teleki 1973:168),or
even synchronouspersistencehunting(Harding and Strum
1976)withoutendurancerunningsuggeststo me thataustralopithecinesand earlyHomo were capable of engagingin such
behavior. Combined with organized regular scavengingof
larger game animals and enhanced technologicaland communicativeskills,cooperativeshort-range
persistencehunting
seemssufficient
to explainthearchaeologicaland paleontological evidencefromas earlyas two millionyearsago. I see no
need to introduceendurancerunningas a necessaryingredient
in thisearlyadaptive pattern.Persistencein pursuitdoes not
requirethecontinuousphysicalexertioninvolvedin running;it
may involveperseverancein stalkingor scavenging,patience
while lyingin ambush, or completionof a preplannedcoordinatedencirclement
of prey.Such strategieswould be based
principallyon neurologicalchanges in the brains of early
hominidsratherthan in theiraerobicphysiology.
490
WhileCarrier'smodeldoes accountfortheenhancedhuman
physiologicalabilityto dissipate heat by sweating,it is not
necessaryto postulateendurancerunningas the cause of the
increased heat load in early hominids.Activitiesrelated to
short-rangehuntingand scavengingin the open duringthe
hottestpartof theday seem to me sufficient.
Consequently,in
is simply
whileinteresting,
myjudgment,Carrier'shypothesis,
unnecessary;theshort-range
huntingand scavengingexplanation is simpler and more compatible with the available
evidence.
One finalquestion:What "biologicalweapons forhunting
fromthoseof othermammalianpredators"did
verydifferent
earlyhominidspossess?Since such predatorspresumablypossess weapons of speed, power, and strength,what is leftfor
of
earlyhominidsifnotintelligence,
cunning,and employment
technology?But employmentof just such "weapons" seems
to explain the archaeologicalevidence
more than sufficient
withoutanyneedforan explanationbased on theenhancement
of aerobic physiology.
by SATWANTI
DepartmentofAnthropology,
University
ofDelhi, Delhi 110
007, India. 12 Iv 84
In discussinglocomotorstamina,theauthorhas describedthe
and capacity to
mode of locomotion,respiratoryefficiency,
rolein
dissipateheat,but thesystemwhichplaysan important
endurancerunning,i.e., theheartand circulatory
system,has
not been mentioned.
by EUGENIE C. SCOTT
Medical Anthropology,Universityof California at San
Francisco,San Francisco, Calif. 94143, U.S.A. 11 Iv 84
The relationshipbetweenhuman energetics,locomotion,and
evolutionis well summarizedhere.I liketheidea ofthecapacityof humansto varytheirspeed of pursuitaccordingto the
least efficient
speed of the preyanimal. This may well be a
pursuitstrategyspecificto persistencehuntersand could perhaps be testedby lookingat thespeeds at whichhumanhunters pursuepreywithdifferent
optimalspeeds(or by lookingat
nonhumanpersistencehunters?).
No one has fullyaddressedthequestionoftheprimateorigin
of the human coolingsystem.Newman (1970), cited by Carrier,has pointedout that human thermoregulation
requires
considerablewater forevaporativecooling.Man can "sweat
like a horse" but not drinklike one; we are not capable of
"tankingup" largeamountsofwaterat one timeas are equids
and camelids. As a result,in hot, dryenvironments
we must
drinkmorefrequently
thanothersavannahdwellers.As Newman has pointedout, thishumancoolingsystemwas movedto
the savannah; it did not evolve there.The humaninabilityto
consumelargeamountsofwaterat one timeis a definite
handicap to a savannahhunterand likelyrequiredculturalcompensationbeforethe specieswas able to engagein lengthypersistencehunting.
Carrierstatesthatthe efficient
coolingsystemof humansis
paralleledin Old World anthropoids,which are assumed to
have originatedin moist,foresthabitats.The imageoffrugivorous,herbaceous,or folivorousprimatesmoseyingaroundcool,
shady forestsdoes not encourage the expectationof strong
selectionforsuperefficient
thermoregulation.
What are nonhuman primatesdoingwiththeirefficient
heatdissipationmechanism?Cursorialprimatesare rare.
I would like to know (1) how efficient
nonhumanprimate
thermoregulation
is comparedwiththatof humans(I predict
thatthehumanformis moreefficient,
beingan elaborationof
the anthropoidpatternselectedforimprovedcoolingduring
persistencehunting)and (2) how much "use" nonhumanpriCURRENT
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ANTHROPOLOGY
matesmakeoftheirenhancedsweatingcapacity(I predictthat
extensiveperiodsof intensephysicalactivityare rare except
I would
perhapsforPatas). If I am correctin thesepredictions,
like to know if some otherfunctionexistsforthe cholinergic
enervationof primatesweat glands, accountingnot only for
thelarge amountof sweat productionbut also forsome other
abilitiesof prithermoregulatory
factor.Perhaps the efficient
matesare a pleiotropiceffectof selectionforanotherfunction,
such as pheromoneproduction,likewise effectedthrough
sweat.
byJOSEPH K. So
Department of Anthropology,Trent University,Peterborough,Ont., Canada K9J 7B8. 7 Iv 84
Carrieris to be commendedforhis thought-provoking
theory.
thatthe huCitingphysiologicaldata, he arguesconvincingly
mechanismforheat dissipaman speciespossessesan efficient
tionand endurancerunning.It is safeto say thatthesebiological attributesare uniquely human and may have played a
role at some pointin our evolution.I am less comsignificant
fortablewithhis assertionthatthe successof hominidsas endurancepredatorsand theabilityto outlastgame animalswas
theprimaryselectiveforce.This modelis based on theassumption that huntingwas the dominantmode of subsistence.As
Carrierhimselfpointsout, the paleontologicalevidenceindicates the contrary(Jungers1982, Stern and Susman 1983).
There also existsa body of data thatquestionsthe validityof
the"man-the-hunter"
schoolof thoughtrepresented
by Washburn and Lancaster (1968). Cross-culturaldata indicate
gatheringas theprimarymode of subsistencein 58% ofthe90
societiessurveyedcomparedwithonly25% forhunting(Martinand Voorhies1975). Observationson huntingby chimpanzees and commonbaboonsindicatethatmeatis a minorpartof
primatehuntingdoes not retheirdiets. More importantly,
quire greatskill,strength,or physiologicalenduranceas Carriersuggests.Thereis a tendencyto overemphasizetheimportance of the predominantlymale activityof huntingas a
selectiveforcein hominidevolutionat theexpenseoftheroleof
food gathering(Fedigan 1982, Slocum 1975). A model that
accounts for only half of the human species is in my view
incomplete.
Even acceptingthe premisethatendurancewas important,
cooperativehuntingought to be considered.It seems that
whilehumanscan chase preyanimalsat speeds uneconomical
forthe animals,success is possibleonlywhen severalhunters
trailthe animal fromdifferent
directions.Physiologicalexplaare but one of manyapnations,while valid and significant,
oftheevolutionofhumansocial
proachesto theunderstanding
life.
by ERIK TRINKAUS
Universityof New Mexico,
Departmentof Anthropology,
Albuquerque,NM. 87131, U.S.A. 20 III 84
Carrier'smodelofhominidsas bipedalendurancerunnerswho
wereable to becomepredatorswithoutgreatstrength
or elaboratetechnologyis well conceivedand convincing.Most interof the
estingly,its implicationsfitwithcurrentinterpretations
Pleistocenearcheologicaland humanpaleontologicalrecords.
ArchaicmembersofthegenusHomo (H. habilis,H. erectus,
and archaic H. sapiens) exhibitpronouncedand consistent
postcranialhypertrophy
(Day 1971; Susman and Stern 1982;
Susman, Stern,and Rose 1983; Trinkaus 1983, n.d.a). This
forthesehominids.However,it
impliesconsiderablestrength
primarilyindicatesan adaptationforhabituallyhighlevelsof
is essentially
a response
activity,sinceosteologicalhypertrophy
to fatiguestress(Lanyon 1982).
Theymusttherefore
have been
exertingconsiderableefforton a regularbasis, and predatory
Carrier:HUMAN
RUNNING
AND HOMINID
EVOLUTION
endurancerunningis an excellentexampleofthetypeofactivTheir
itythatwould promoteand maintainthishypertrophy.
associatedenergeticcost duringthisendurancerunningwould
have been accentuatedby theirrelativelysmall staturesand
hence stridelengths(statureestimates:H. habilis, 150-159
cm, N = 3; H. erectus,158-172 cm, N = 4; Neandertals,166
+ 6 cm,N = 18),mostofwhichare towardthelowerlimitsof
recenthuman rangesof variation.
Recent analyses of the archeologicalrecord(e.g., Binford
1981,1982, 1984;Camps-Fabrer1974;Clark 1983;Klein 1978;
Oakley et al. 1977; Potts 1982; Straus 1982) suggesta similar
pattern.They indicatethe absence of effectivehuntingprojectileswithhaftedpointspriorto the terminalMiddle Paleolithic(Aterian)and Upper Paleolithicand onlyfire-hardened
wooden thrusting
spears (e.g., Clacton and Lehringenspears)
fromearlierin thePleistocene.In conjunctionwiththis,Lower
faunal assemblages
and Middle Paleolithichominid-derived
appear to be dominated by small mammals and probably
scavengedportionsofmedium-sizedto largemammals.There
hunting
is littleto indicatethatarchaichumanswereroutinely
of the aranimalslargerthan themselves.This interpretation
cheologicalrecord clearlyfitswith both the paleontological
evidencefromarchaic humansand Carrier'smodel of endurance-running
predationon smallermammals.
thatthe earliestappearance in the arIt is also interesting
cheologicalrecordof haftedprojectilesthatwould removethe
need forhabitualendurancerunningto capturepreyis associated with the appearance of early anatomicallymodernhumans,who show a markedreductionin postcranialrobusticity
(as
(Trinkaus 1983) and an increase in locomotorefficiency
indicatedby an increase in statureand hence stridelength
[European and Near Eastern earlyanatomicallymodernhuman statureestimates:178 + 9 cm, N = 27], relativelylonger
distal limb segments[Trinkaus 1981], and narrowerpelves
[Trinkausn.d.b]). These are combinedwithevidenceof more
systematicexploitationof a diversityof fauna and of more
routine monitoringof available environmentalresources.
enthatthepredatory
suggest,therefore,
These considerations
durancerunningproposedby Carriermayhave been veryimportantamong archaic membersof the genusHomo, permitting (among otherthings)theirexpansioninto regionswith
markedseasonal variationin plant-foodavailability,but that
it decreasedin importanceas logisticallyorganizedand essenemergedduringtheUptiallymodernhumanhunter-gatherers
per Pleistocene.
Reply
byDAVID CARRIER
AnnArbor,Mich., U.S.A. 14 v 84
In recentyears therehas been a tendencyto emphasizethe
ofscavengingand gathering
formsof
evolutionary
significance
subsistenceof early hominids.This view is reflectedin the
commentsof Nickels and So. Althoughthe available archaeologicaland paleontologicalevidenceof earlyhominidsis
ofteninterpreted
as consistentwithgathering,
scavenging,and
formsof hunting,the possibilityof
short-range
opportunistic
persistencehuntingcannotbe excluded.A scavengingand opportunistic
huntingnichewould imposefewselectivepressures
and could be filledbymanygeneralizedlargemammals.However, humans are not generalizedmammals. Man's unique
cannotbe easilyexplainedbysuch
physiology
and morphology
an unspecializedsubsistencepattern.If, forinstance,man's
exceptionalcapacityto dissipateheatweresimplya responseto
generaldiurnalactivity,as Nickels suggests,thenone might
expectto see similaradaptationsin otherlargesavannahmain-
1984
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491
mals (e.g., heavilysweatingand hairlessantelope).Hairlessness,transport
costindependentofspeed, and thecapacityfor
inferior
runnerare feasuperiorendurancein an energetically
turesso unique that any explanationdemandsextremeselection. This selection,I believe, could best be providedby a
diurnalenduranceformof predation.
Scott'sreference
to Newman's (1970) thoughtful
paper warrantssome discussion.Newman's thesisis based on the assumptionthatman's exceptionalthermoregulatory
capacityresultedfroman adaptiveresponseto environmental
heatloads.
He speculatesthathominidslosttheirhairin an ancientforest
habitat beforethe move to open savannah. The change in
habitat fromshady forestto sunnysavannah would greatly
increasethe radiant-heatload, particularlyif the animals in
questionlacked hair. Man's enhancedabilityto sweat is arguedto be a responseto thisincreasedimpactofradiantenergy
on his naked ancestors.There are two problemswith this
scenario.First,Newman does notprovidea functionalreason
for the loss of hair. If the forest-dwelling
predecessorsof
hominidslost theirfurcoats simplyfroma lack of need, why
have otherforestprimatesretaineda fullcomplementofhair?
Second, man's exceptionalcapacityforheat dissipationis unlikelyto have resultedfromthe impositionof the relatively
minorenvironmental
heat loads to which all large savannah
mammalsare subjected.It is moreprobablethatitis a reaction
to the much largerthermalloads producedduringsustained
exercise.Newman's paper providesmanyinsights,but I disagreewiththebasic premisethathairlessnessin man is largely
disadvantageousand thatthe humancapacityforsweatingis
an adaptive responseto environmental
sourcesof heat.
Scott raises a difficultissue for the persistence-hunting
modelin theseeminglylargediscrepancybetweenman's great
need forwater in thermoregulation
and his limitedabilityto
carrya substantialreservoirin his gut (Newman 1970). As
Scottsuggests,beforetheinventionof water-carrying
devices,
hominids'inabilityto drinklarge quantitiesof water at any
one timewouldhave placed limitson thedurationofhuntsand
the distance covered. This in turn would have limitedthe
speciesof preythatcould have been acquiredthroughpersistence running.Certaintypesof preywould have been more
vulnerablethan others.Hares (Leporidae), forexample, are
cursorialopen-countryrunnersthat are severelylimitedby
theirinabilityto dissipate exerciseheat loads. To facilitate
passive heat loss and to conservewater, on hot days hares
allow theirbody temperature
to rise. This leave littlemargin
for the additionalheat that must be storedduringexercise.
Storageof metabolicheat while runningin theseanimalscan
proceedat ratesmorethan fivetimesthe standardmetabolic
rate. Consequently,thecore temperature
of a hare pursuedin
theheat can reacha lethallevel in a fewminutes(Shoemaker,
Nagy, and Costa 1976). Hares of the genera Lepus and
Serengetilagus(Leakey 1965) were likelyto have been easily
accessibleto earlyaustralopithecines
on shortexcursionsaway
fromsourcesof water.
I am somewhatsurprisedby Scott'ssuggestionthatnonhuman primatesdo not need effective
mechanismsof heat dissipation.The dynamiclocomotorperformance
of primatessuch
as spidermonkeys,langurs,and gibbonssuggeststhat these
animals commonlyplace very large demands on theirthermoregulatorysystem. Because of the large accelerations
againstgravity,climbingand leapingfrombranchto branch
will always requiremore energythan movingan equivalent
distanceon a continuoushorizontalsurface.Indeed, brachiation,theformofarboreallocomotionthatcould be expectedto
be mosteconomicalbecause of the possibilityof passive supportand the storageand recoveryof energyin the pendular
motionof each swing,has been shownto be less efficient
than
walkingin spidermonkeys(Parsonsand Taylor 1977). Vigorous arboreallocomotionwillclearlygeneratesubstantialmetabolic heatloads, and dissipationofthismetabolicheatis likely
492
to be veryimportantin the day-to-daylives of manynonhuman primates.
Nickelsand So raisetheissue of thesignificance
offoraging
practicesof modernhunter-gatherers
to the subsistencepatternsof man's ancestors.That some modernhuntersrunprey
to exhaustion demonstratesthat modern humans possess
greaterstaminathanthe animalspursued,notthatman's ancestorshuntedthis way. Moreover,the observationthatthis
methodis not the primaryhuntingtacticemployedby extant
hominids,withtheirpoison arrowsand rifles,is irrelevantto
thequestionof how earlyhominidsacquiredprotein.There is
further
reasonto questionthevalue ofextrapolating
thepractices of modern hunter-gatherers
back in time to early
hominids.Beforetherecentinventionofcookingfires,muchof
thecaloricand proteincontentofmanyplantfoodsused today
may not have been digestible(Stahl 1984). This suggeststhat
animalproteinin someformmayhave beenmoreimportant
in
thepast in meetingnutritional
thanit is at presrequirements
ent.The presumablyrecentadventofgreatlyincreasedintelligenceand culturemakestheextrapolation
ofmodernbehavior
backwardin timemoretenuousthanis thecase fornonhuman
paleontology.
The questionposed by Nickels of the costs and benefitsof
persistencehuntingis critical.Runningpreyforextendedperiodsin hot temperatures
is an energetically
expensiveundertaking. If diurnal endurance predation had a significant
influenceon the course of hominidevolution,it must be an
viable strategy.The occasionaluse of endurance
energetically
predationby modernhunterssuggeststhatat least forHomo
sapiens it is cost-effective,
but thishas yetto be measured.In
additionto the caloricexpenditure,thistypeof huntingcould
have been exceptionallyhazardous because of the prolonged
exposureto thesun's radiation,potentialfordehydration,
and
increasedexposureto the largersavannah predators.These
would have represented
obstaclesto a primateemsignificant
ployingthe run-downtechnique and could have provided
strongselectionforincreasedintelligence,
groupcooperation,
and precisecommunication.
Several of the commentators
(Kapoor, Nickels, So) address
the issue of the relationshipbetweena huntinglife-style
and
neurologicalfunctions
such as intelligence
and social behavior.
rolein thehuntingof all
Groupcooperationplaysa significant
thesocial carnivoresand modernman. Withanimalsas intelligentand social as mostoftheanthropoidprimates,itwouldbe
ridiculousto suggestthat group cooperationwould not have
been importantin increasedhuntingactivity.What is really
moreinteresting
is the rolethatpersistencehuntingmayhave
playedin the evolutionof humanintelligence
and way of life.
A numberof authors(Schaller and Lowther 1969, Laughlin
1968,Washburnand Lancaster1968,Wolpoff1980)have consideredtheprobableinfluenceofa shiftto a predatory
nicheon
the developmentof hominidintelligenceand social structure.
These authorsand othershave stressedthattheshiftinvolved
muchmorethana changein diet. Huntingis suggestedto be a
way oflifethathas dominatedthecourseofhominidevolution
producingmodernman's intelligence,
interest,
emotions,communication,and basic social life.
At no point have I suggested,as So states, that primate
huntingrequiresgreat endurance,skill, or strength;I have
arguedonlythatendurancerunningmay have providedearly
hominidswitha reliablemechanismforincreasingtheirintake
of animal protein.Nor can I agree with So's assertionthat
huntingby earlyhominidswould necessarilyhave been a predominantlymale activity.Excludingtheosteologicalevidence
of sexual dimorphismin body size (Wolpoff1976), I see no
reasonto supposethatfemaleswould have been completelyor
partiallyexcludedfromhunting.Female membersofthesocial
carnivoresregularlytake an active and sometimesdominant
rolein hunting.Oftenyoungare leftat a den sitein thecare of
a singleadult while the restof the adults engagein hunting.
CURRENT
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ANTHROPOLOGY
Severalof the pointsraisedby Kimurarequireclarification:
(1) It is unlikelythatancestralman could have forcedpreyto
speed. It is moreprobablethatprey
runat theirleast efficient
and therefore
could have been driven to run intermittently
In additionto the relevantdata fromhumans,
inefficiently.
runninghas been shownto producefatiguemore
intermittent
rapidlythan continuousrunningin rats (Gaesser and Brooks
runningis reportedto be the escape strat1980). Intermittent
egy used by prey animals fleeingBushman runners(Bjerre
1960). (2) The breathingof a runningquadruped is tightly
coupledto thelocomotorcycle,usuallyat a rateof one breath
per stride(Bramble 1984). The breathingof conditionedhuman runnersis typicallyalso synchronizedto the locomotor
cycle. The differenceis that in humans the integerratio of
strideperbreathvariesdramaticallydependingon theindividual and conditions.This abilityto shiftratiosis exactlythe
thatis
mechanismsuggestedhereto providea costoftransport
independentof speed in runninghumans. (3) The reader
shouldbe aware thatdonkeysare membersofthehorsegenus
Equus, llamas are a species of South Americancamel, and
cattleare membersof the familyBovidae.
ofthe
I am intrigued
byTrinkaus'salternativeinterpretation
functionalsignificanceof the relativelyrobustbones of early
a responseto
is primarily
hominids.If osteologicalhypertrophy
fatiguestressand hence to habituallyhighlevels of activity,
thenthisshouldbe readilyapparentin allometriccomparisons
activitypatterns.A
of thebones of speciesthathave different
comparativeinterspeciesanalysis of bone dimensionsand
would help clarifytheextentto which
locomotorperformance
thisrelationship
can be used to estimatelocomotorbehaviorof
extinctspecies.
is that
A view thatseemsto be heldbymanyanthropologists
huntingcould not have been an importanthominidactivity
until the early or mid-Pleistocene.Given the available archaeologicaland paleontologicalevidence,thisis a reasonable
position.However,I would like to emphasizethatpersistence
rolein the acquisition
huntingcould have playeda significant
of meatlong beforethe firstclear evidenceof hominidpredawere fully
tion. We know that the early australopithecines
bipedal. Althoughtheirrunningis likelyto have been less
efficient
than that of Homo, it was probablyno more costly
than the quadrupedal runningof theirprehominidancestors.
Over the range of speeds at which measurementshave been
fromthecost
made, thecostofbipedal runningis notdifferent
of quadrupedal runningin chimpanzeesand capuchin monkeys (Taylor and Rowntree 1973b). Instead of imposingan
energetichandicapon theinitialbipeds,theshiftto runningon
increasedthe rangeof availtwo legs may have significantly
able speeds by uncouplingrespirationfromlocomotion.It is
were
also safe to assume that the early australopithecines
superiorto the othersavannah mammals in theirabilityto
dissipatemetabolicheatloads. These featurescould have been
used effectively
againstcertainpreyanimals,suchas thecursorial but thermallysusceptiblehares. Evidence of thistypeof
predation,ifitexists,maybe recognizablein thefaunalassemblages associatedwiththe earlyaustralopithecines.
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Wanted
* Correspondenceand suitable bibliographicreferences
from
anthropologists
interestedin the ethnography
of blindness,in
connectionwith fieldworkamong the blind in Israel. Please
write: Shlomo Deshen, Departmentof Sociology and AnBar-Ilan University,Ramat-Gan,52100 Israel.
thropology,
* Papers dealingwiththe lives, careers,and achievementsof
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* Manuscriptson a varietyof biopoliticaltopics,including(1)
Carrier:HUMAN
RUNNING
AND HOMINID
EVOLUTION
. n.d.a. Does KNM-ER 1481A establishHomo erectusat 2.0
myrBP? AmericanJournalof PhysicalAnthropology
64. In press.
[ET]
. n.d.b. Neandertal pubic morphologyand gestationlength.
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public-policy-related
works on biomedicaltechnologies,human ecology,health and environment,
aging, food, populaofbiologtion,and reproductive
technologies;
(2) theinfluence
ical factors on political behavior; (3) the relationshipof
ethologyand sociobiologyto the concernsof traditionalpolitical scienceand ethics;and (4) therelationship
ofbiopoliticsto
otherperspectivesin the social and naturalsciences,forthe
journal Politics and the Life Sciences. Data-based empirical
studies are especially welcome. Please write: Thomas C.
Wiegele, Editor, NorthernIllinois University,DeKalb, Ill.
60115, U.S.A.
* In connectionwith a dissertationon incipientcultivation
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quantitativedata on rice
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uncropped. Please write: Thomas N. Headland, Bagabag,
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1984
Vol. 25 * No. 4 * August-October
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