CURRENT ANTHROPOLOGY Vol. 25, No. 4, August-October1984 K 1984 by The Wenner-GrenFoundation for Anthropological Research, all rightsreserved 0011-3204/84/2504-0005$2 00

The EnergeticParadox of Human Runningand HominidEvolution'

byDavid R. Carrier

THE FEATURE THAT DIFFERENTIATES HOMINIDS fromother mal thesize of man shouldconsume roughly 0.10 ml of oxygen primatesis notlarge brain size, but theset ofcharacters associ- per grambody mass per kilometertraveled (Taylor, Schmidt- ated witherect bipedal postureand a stridinggait. Long before Nielsen, and Raab 1970), but the measuredvalue forman is the rapid increasein relativebrain size thattook place during over twice this amount (0.212 ml). A recentanalysis of 64 thePleistocene, early australopithecines possessed the postcra- speciesof runningbirds and mammals(Taylor, Heglund, and nial morphologyof an erect,striding biped (Lovejoy, Heiple, Maloiy 1982) confirmsthe initialobservations that the cost of and Burstein 1973). Evidence for the bipedal gait of early transportis relativelyhigh for human runners. hominidsis provided by the morphologyof the 3.5-million- It is somewhatsurprising, therefore, that among year-oldpostcranial material from the Hadar Formationof mammalsman is one ofthe best distance runners. While game Ethiopia (Johanson, Taieb, and Coppens 1982, Lovejoy, animalsare fasterover short distances, they generally have less Johanson,and Coppens 1982), earlyPleistocene material from endurancethan man. Aside frompublished accounts of endur- eastern and southern Africa (Preuschoft1971), and the ance performancein thedomestic horse and camel,which have Pliocenetrackways (3.6 to 3.8 millionyears old) discoveredat been bredfor endurance racing, very little is knownabout the Laetoli in northernTanzania (Leakey and Hay 1979, White stamina of mammals. What littleinformation is available is 1980). Together these suggest that early australopithecines usuallytaken fromanecdotal accounts of animals performing were relativelysmall-brained creatures, possessing structural in a varietyof climatic and topographicenvironments (see adaptationsfor upright and runningthat in a broad Howell 1965), and consequentlyinterspecific comparisons are sense are remarkablysimilar to those of modernman. The hazardous.Comparisons between man and a numberof curso- aspects of locomotionthat unite the hominidsas a groupare rial species can be made, however,in the contextof a contest also uniquelyhominid in characterand distinctlypeculiar for betweenpredator and prey. mammals. Consequently,the studyof human locomotion,in Huntersof a numberof differentcultures are knownto run additionto explainingmuch of the biologyof the one remain- down prey by dogged pursuitoften lasting one or two days inghominid, may proveto be one of themore powerful induc- (Krantz 1968, Watanabe 1971). Bushmenare reportedto run tive approachesto the studyof hominidevolution. down duicker,steenbok, and gemsbokduring the rainy season The energeticcost of transport (oxygen consumption per unit and wildebeestand zebra duringthe hot dryseason (Schapera body mass per unit distancetraveled) for humans is 1930). TarahumaraIndians chase deer throughthe mountains relativelyhigh in comparisonwith that for other mammals and of northernMexico untilthe animalscollapse from exhaustion runningbirds. Early comparativestudies showed that a mam- and thenthrottle them by hand (Bennettand Zingg 1935,Pen- nington1963). Paiutes and Navajo of theAmerican Southwest are reportedto have huntedpronghorn antelope (one of the 1 This contributionarose out of conversationswith D. M. Bramble fastestof all mammals)with this same technique(Lowie 1924; and S. C. Carrier.Further development resulted from discussions with Foster 1830, citedby Lopez 1981:111).Furthermore, Aborigi- C. Gans and M. H. Wolpoff.For criticalreview and additionalim- nes of northwesternAustralia are known to hunt kangaroo provementof this manuscript,I am gratefulto S. L. Beck, D. M. Bramble,S. B. Emerson,J. R. Fetcho, D. B. Jenkins,R. G. North- successfullyin thisway (Sollas 1924,McCarthy 1957). In these cutt,P. A. Pridmore,and R. 0. Whitten. examplesthe staminaof preyanimals generallyconsidered to be specializedfor running and presumablyputting forth their best effortproves to be less than thatof man. Energeticallyinefficient transport and endurancerunning DAVID R. CARRIER is a doctoralcandidate in zoologyat the Uni- would seem to be incompatible.The combinationof thesetwo versityof Michigan (c/o Division of BiologicalSciences, University of Michigan,Ann Arbor,Mich. 48109, U.S.A.). Born in 1955, he attributespresents obvious morphologicaland physiological was educatedat the Universityof Utah (B.S., geology,1980; B.S., problems.For instance,there must be a way ofdissipating the biology,1980; M.S., biology,1982). He views himselfas a func- highlevels of metabolicheat producedduring long-term mus- tionaland evolutionarymorphologist and is particularlyinterested cle action. In addition,extended periods of high energyde- in vertebratelocomotion and the ontogenyof the musculo-skeletal mand requirelarge body stores of glycogenand fattyacids and system.His publicationsinclude "Postnatal Ontogeny of the Mus- an effectivemeans of mobilizingthese stores.It is clear that culo-SkeletalSystem in theBlack-tailed Jack Rabbit (Lepus califor- nicus)" (Journalof Zoology [London] 201:27-55) and, withD. M. duringthe sequence of evolutionarysteps that led frompre- Bramble, "Running and Breathing in Mammals" (Science hominidsto Homo sapiens these problemshave been over- 219:251-56). The presentpaper was submittedin finalform 9 I 84. come. How this was accomplishedand what factorsmight

Vol. 25 No. 4 August-October1984 483 This content downloaded from 155.97.178.73 on Fri, 27 Nov 2015 17:24:13 UTC All use subject to JSTOR Terms and Conditions have initiatedthis sequence of specializationis the subject of ward flow of heat fromthe hot environmentthan sweating the presentanalysis. animals.Taylor and Rowntree(1974) have shownthat in a hot environment(47?C) heat flowsinto sweating animals at about twicethe rate thatit flowsinto panting animals. For the same DISSIPATION OF METABOLIC HEAT reason,when environmental temperature is low thecooler skin temperaturein sweatinganimals resultsin a smallergradient The normal core body temperatureof eutherianmammals fornonevaporative heat loss (heat loss by radiationwhen skin ranges from36?C to 38?C (Morrisonand Ryser 1952). The temperatureexceeds ambient temperature).Thus, sweating lethalcore temperatureof thesemammals is only6?C higher, animalsgain moreheat froma hot environmentand are capa- rangingfrom 42?C to 44?C (Adolph 1947). Using empirical ble of losingless heat by nonevaporativemeans than panting measuresof the cost of transport,Taylor (1974) has calculated ones. that the maximal exerciseheat loads generatedby medium- 2. Because pantingrestricts evaporation to the nasal, buc- sized and large animals (greaterthan 10 kg body mass) are cal, and pharyngealcavities, pantinganimals lose littlesalt. nearlyan order of magnitudegreater than the maximal en- Sweatinganimals, on theother hand, mustdeal withlarge salt vironmentalheat thatthey are likelyto encounterin nature.If losses (Schmidt-Nielsen1980). metabolicheat is produced more rapidlythan it can be dis- 3. Pantingprovides forced convection across the evapora- sipated,body temperature rises. Thus, adequate thermalregu- tivesurfaces, whereas sweating requires animals to relyon free lationis criticalfor animals that run for extended periods. For convectionor wind. (This should not be a problemfor a run- example, sprint at speeds exceeding100 km/hr,and ninganimal, particularlyif it lacks hair.) extrapolationof measurementsmade at lowerspeeds suggests Evaporative coolingfrom the skin offersthe followingad- thatat 100 km/hrheat productionwould be morethan 60 times vantages: greaterthan at rest(Taylor and Rowntree1973a). The 1. Sweating provides an additional evaporative surface. storesmost of thisheat, and thereforeas it runsits bodytem- Taylor and Rowntree(1974) measuredthe maximumrates of peraturerises. Once the rectaltemperature reaches 40.5?C the evaporativeheat loss froma groupof pantingand a groupof animal refusesto run. Taylor and Rowntreeestimate that if a sweatinganimals in responseto exercise.They foundthat the cheetahterminated a sprintonce its bodytemperature reached ratesof evaporation from the respiratory surfaces were similar, 40.5?C, it could run for only 1 km. This approximatesthe but the sweatinganimals had much highermaximal rates of actual distancethat cheetahs pursue their prey in the wild. It evaporationbecause of the evaporationthat occurredat the seems that the durationof the cheetah'ssprint may be deter- skin surface. mined not by fatiguebut by the amountof heat it can store 2. Sweating is independentof the respiratorycycle. As a beforeit reachesa limitingbody temperature. runninganimal increasesspeed, its oxygenconsumption in- Mammals dissipateheat by evaporativeor nonevaporative creasesin a linearfashion (Taylor, Schmidt-Nielsen, and Raab means. The Africanhunting dog is exceptionalin that it ap- 1970). However, as runningspeed changesit is unlikelythat pears to dissipatelarge exerciseheat loads, forextended pe- therespiratory air flowrequired for metabolism will matchthe riods, throughnonevaporative means (Taylor et al. 1971). flowneeded forheat loss, since the rate at whichheat can be Most medium-sizedto large mammals rely on evaporative dissipatedwill vary withambient temperature and humidity. cooling to maintain body temperaturewhile running(see Furthermore,the breathing cycle of quadrupeds is strictlycon- Richards1970; Taylor 1974, 1977). Evaporativecooling is ac- trolledby the body motionsof the runninganimal (Bramble complishedby two separatemechanisms: (1) respiratoryevap- and Carrier1983). This couplingof locomotorand respiratory orationoccurring at thenasal mucosa,buccal, and tonguesur- cycleswill make it impossiblefor a runninganimal to varythe faces (panting)and (2) evaporationof sweat fromthe general air flowover the respiratoryevaporative surfaces to the same body surface. Panting is almost universallyemployed by degree that is possible in typicalstationary panting. Conse- medium-sizedto largemammals. The onlygroups that do not quently,the flexibilityand possiblythe total effectivenessof relyheavily upon pantingare the Old World Anthropoidea pantingas a means of evaporativecooling may be limitedin a (including man) (Robertshaw, Taylor, and Mazzia 1973, runningmammal. Indeed, the amountof heat thatcan be lost Hanna and Brown 1983), horses, and camels (Robertshaw throughevaporation from the respiratorysurfaces severely 1975). These threegroups maintain body temperatureduring limitsthe maximumrate of heat dissipationduring running in extendedexercise by sweating.In additionto these animals, animals that rely solely on panting (Taylor and Rowntree some bovids (Taylor and Lyman 1972) and kangaroos(Daw- 1974). son, Robertshaw,and Taylor 1974) also use sweat glandsfor In thiscontext, the mechanisms of heat dissipation in thered thermoregulation.In contrast,suids (Robertshaw1975) and kangarooare ofinterest. This marsupialuses threeevaporative some carnivores(Taylor et al. 1971) have sweat glandson the coolingmechanisms: panting, sweating, and saliva spreading generalbody surface,but thesedo not appear to be associated (Dawson, Robertshaw,and Taylor 1974). However, it sweats withthermoregulation. Sweat glandson the generalbody sur- only during exercise. Under conditionsof severe thermal face are lackingin Rodentia,Proboscidea (Robertshaw 1975), stress,the restingkangaroo pants and spreadssaliva. For the and Lagomorpha(Jenkinson 1970). red kangarooand othermammals, sweating provides an addi- tionalavenue ofheat dissipationthat may offer more flexibility and be morecompatible with running as a mechanismof ther- SWEATING VS. PANTING moregulation. A numberof physiologists have consideredthe advantages and disadvantagesof sweatingand pantingto achieveevaporative RUNNING HUMANS cooling(Schmidt-Nielsen 1964, Hales 1974,Taylor 1977). The presentdiscussion will be confinedto thoseaspects whichin- The sweat glandsof man are distinctivefor the high secretory fluencethermoregulation during exercise. levelat whichthey operate. No otherspecies is knownto sweat Evaporativecooling from the respiratorysurfaces offers the as much per unit surfacearea as man (Eichna et al. 1950, followingadvantages over evaporativecooling from the skin: Schmidt-Nielsen1964, Newman 1970). Human sweat glands 1. The skin of sweatinganimals is cooler(as a resultof the may also be subject to a higherlevel of neuronalcontrol than evaporation)than the skin of pantinganimals. When air tem- the sweat glands of otherspecies. At present,it appears that peratureexceeds skin temperature, animals gain heat fromthe onlycamels, horses,and Old WorldAnthropoidea possess di- environment.Accordingly, panting animals have a slowerin- rectlyinnervated sweat glands. The sweat glands of other

484 CURRENT ANTHROPOLOGY This content downloaded from 155.97.178.73 on Fri, 27 Nov 2015 17:24:13 UTC All use subject to JSTOR Terms and Conditions groupseither lack a nervesupply (e.g., canids) or possess one Carrier:HUMAN RUNNING AND HOMINID EVOLUTION thatdoes not make directcontact with the gland(e.g., bovids) (Robertshaw1975). Furthermore,the neuronssupplying the gariaet al. 1963,Cavagna and Kaneko 1977). Consequently,a glands of anthropoidprimates are cholinergic,whereas the man runninga marathonwill consumethe same amountof glands of horses and camels are adrenergicallyinnervated. energyfor transportwhether he runs at a slow jog or at a Robertshaw(1975) has suggestedthat the rapid hydrolysisof world-classpace. acetylcholineby acetylcholinesterasemay provide the choliner- withfiner neuronal control gic glands of anthropoidprimates WALKING than is possiblewith adrenergic modes of transmission. The rate at which heat is lost fromrunning humans is Unlikehuman running, human walking is at least as econom- greatlyincreased by theirrelative lack of hair. The furcoat of ical as the walkingof typicalmammalian quadrupeds (Rod- mostmammals not only insulates the animal from the environ- man and McHenry1980; also see Tucker 1975). The efficiency mentalheat, but also insulatesthe environment from heat pro- in walkingis related,in part,to a finelytuned system of stor- duced by the animal. Accordingly,mammals with thickin- age and recoveryof the energyused for motionwithin each sulatorycoats will have difficultydissipating heat generated stride.Walking birds and mammalsbenefit from an exchange throughexercise. The paucityof hair on the human body re- betweenthe kineticenergy and the gravitationalpotential en- sults in greaterthermal conductance than would be possible ergyof the centerof mass withineach stride(Cavagna, Heg- witha fullcoat of hair. The thermalconductance of a hairless lund, and Taylor 1977). Gravitationalpotential energyis mammalshould be furtherincreased by the increasedconvec- storedas the centerof mass risesduring a step. This energyis tion duringrunning, as the animal moves throughthe air. thenrecovered as the body falls forwardand is subsequently Mammals withthick coats will not experiencethis increase in convertedback into potentialenergy as the centerof mass convectionwhen running.Cena and Monteith(1975) have again rises over the otherleg. For this reason, walking has shown that the thermalconductivity of sheep fleece (4 cm been likenedto an invertedswinging pendulum or an egg roll- thick)is not affectedby air flowof up to 18 km/hr.In rabbits, ing end overend (Cavagna, Saibene, and Margaria 1963). The wind speeds below 11 km/hrdo not affectthe conductivityof bipedal postureof man is ideallysuited for this pendular mo- thefur (1.8 cm thick),but an increaseof wind speed to 18 km/ tion.Throughout most of the support phase, thelimb pivots on hrdoubles its conductivity.It appears thatair movingparallel a plantigradefoot. In contrastto the situationof mostquad- to the surfaceof furcoats at speeds equivalentto endurance rupedal cursors,no musculareffort is requiredto maintain runningspeeds ofhumans (i.e., 10-20 km/hr)fails to penetrate ankle extension.Most importantly,the centerof mass rollsin or even disturbthe stagnantair trappedbetween the hairsof an arc over the pointof support(foot) on a relativelystraight othermammals. This stagnantair providesnearly all thether- leg, so that the potentialenergy gained in the rise roughly mal resistanceof the system.The adaptive value of man's equals the kineticenergy lost in the descent(Alexander 1976). largelyglabrous condition may, more than anythingelse, be Energysavings due to this transferbetween potential and the facilitationof heat dissipationwhile running. kineticenergy are substantial.In humanswalking at a speed of In summary,the combinationof well-developedsweat approximately4 km/hr,the recoveryof mechanicalenergy at- glandsand the relativeabsence of body hair in man makes it tains a maximumof 65-70% (Cavagna, Thys, and Zamboni probablethat running humans display very high thermal con- 1976). Equivalentsavings have beenmeasured in bipedalbirds ductance,with maximal values well above thoseof most curso- (turkeyand rhea) walking at similarspeeds (Cavagna, Heg- rial mammals. The human mechanismsof thermoregulation lund, and Taylor 1977). In contrast,the percentagerecovery (sweating,as opposed to panting,and hairlessness)are proba- bly more effectiveat dissipatingmetabolic heat producedin mechanismsused by other runningthan are the regulatory 240- mammaliancursors. Supportingthis is the observationthat certainsweating (i.e., spider monkeys,stump-tail macaques, baboons, and chimpanzees)are capable of greater - maximumrates of heat dissipationduring running than are 200 mammals dependent upon panting (Taylor and Rowntree 1974). Unfortunately,measurements of maximalrates of heat - dissipationfrom large animals during exercise are almost v) 160 nonexistent,and so directcomparisons with man cannotyet be made. _ 120 - \ > _

COST OF TRANSPORT 80 Runninghumans expend approximately twice as muchenergy per unit mass as typicalmammalian quadrupeds of the same size but are neverthelessadept at endurancerunning. Man's 40 capacityfor endurance locomotion, both running and walking, may resultfrom the way in whichthe cost of transportvaries with the speed of travel (fig. 1). First, humans walking at optimalspeed consumeonly half the energy (used in transport) 4 8 12 16 20 24 requiredto cover the same distancewhile running(Cavagna Speed (km *hr-') and Kaneko 1977, Rodman and McHenry 1980). This is clearlynot the case forhorses (Hoyt and Taylor 1981) or for FIG. 1. The energeticcosts of walking and runningin thehorse and in The consumedin a unitdistance is minimizedat otherlarge cursors(see Taylor, Heglund, and Maloiy 1982). man. oxygen moving a narrowrange of speed in all threegaits-walk, trot,and canter-of Second, while quadrupedal cursorshave specificspeeds at the horse (dashed curves)and in the walk of man (solid curve). In whichenergy expenditure is minimizedfor each of theirvari- contrast,the cost of transportis independentof runningspeed in man ous gaits (Hoyt and Taylor 1981), the cost of transportfor a (solid line). (Modifiedfrom HIoyt and Taylor 1981 and Margariaet al. runninghuman does not depend on speed (Boje 1944, Mar- 1963.)

Vol. 25 * No. 4 * August-October1984 485 This content downloaded from 155.97.178.73 on Fri, 27 Nov 2015 17:24:13 UTC All use subject to JSTOR Terms and Conditions appears to be lower in quadrupedal mammals.Rams walking whichthe lungsare ventilatedduring running. When a quad- at intermediatespeeds (3-4 km/hr)recover a maximumof only ruped trotsor gallops, the muscles and bones of the thorax 35%. Dogs and monkeysrecover no more than 50% of the must absorb the shock of impactingon the frontlimbs. In mechanicalenergy used while walking(Cavagna et al. 1977). addition,during a gallop all mammalsexhibit some degreeof The efficiencyof walkingchanges with speed (Cavagna and axial bendingin thedorso-ventral direction. This motioncom- Kaneko 1977, Hoyt and Taylor 1981). This is true forboth pressesand thenexpands the thoracicspace witheach stride. men and horses (fig. 1). There is an intermediatespeed at These aspects of gait restrictthe ventilationof quadrupedsto whichthe energeticcost to walk a unitdistance is minimized. one breath per locomotorcycle (Bramble and Carrier 1983, As velocityis increasedor decreased away fromthis optimal Hornicke,Meixner, and Pollmannn.d.). In contrast,the up- speed, thecost of transportrises rapidly. The costof transport rightbipedal gait of humansmakes possiblea largenumber of fora walkinghuman is minimizedat speeds rangingfrom 5 to breathingpatterns (e.g., two stridesper breath,three strides 6 km/hr.The optimal walking speed of the larger horse is perbreath, etc.). Therefore,while the breathing frequency of a slower(4 to 5 km/hr). runningquadruped equals its stridefrequency, man can vary Optimalwalking speeds are related,in part,to theenergetic breath frequencyrelative to stridefrequency (Bramble and propertiesof the contractilecomponent of skeletal muscle. Carrier1983). There is a speed of muscle shorteningat which efficiencyis The objective of lung ventilationis to meet the metabolic maximized(for a review,see Goldspink1977). This demands demand for oxygen. However, in runningmammals this is that,in termsof energy expenditure, there be an optimalstride morecomplex than is generallyrecognized. As runningspeed frequency.Also, the ability of muscle to generateforce di- increases,the need for oxygenincreases rapidlyin a linear minishesas themuscle is stretchedbeyond or shortenedbelow manner(Taylor, Schmidt-Nielsen,and Raab 1970). For any itsso-called optimal length (Gordon, Huxley, and Julian1966). givenlevel ofaerobic exertion, the tissues' need foroxygen will Consequently,there must also be an optimalstride length with be metby a specificlung minutevolume, which is theproduct regardto muscle function.Because speed is the productof of the breathingfrequency and the tidal (lung)volume. How- stridelength and stridefrequency, the contractile properties of ever, as a consequenceof the elastic resistanceof the thorax, muscle can be expectedto limit animals to energeticallyop- airway resistance,and dead-space volume, thereis a specific timal speeds in all gaits. However, forrunning humans this rateand depthof breathing,for any minutevolume, that max- appears not to be the case. imizes ventilatoryefficiency (Otis, Fenn, and Rahn 1950, Crosfilland Widdicombe1961, Yamashiro and Grodins1973). A furtherlimitation results from the way in which speed is RUNNING variedwhile running.There appears to be a specificcombina- As is the case forwalking, the energeticcost of transportfor tionof stride length and stridefrequency that minimizes energy runningquadrupeds appears to change with speed, being consumptionfor any runningspeed (Knuttgen1961, Cavanagh minimalat intermediatespeeds withineach gait. By training and Williams1982). For sustainedeconomical transport a run- horsesto extendtheir gaits beyondnormal speeds, Hoyt and ning mammal must therefore(1) employan energeticallyap- Taylor (1981) have shown thatfor each gait thereis a specific propriateblend of stride length and stridefrequency, (2) match speed at which the amount of oxygenused to move a given themetabolic demand for oxygen via lungventilation, (3) ven- distanceis minimal(fig. 1). When the horseswere allowed to tilatethe lungs with an energeticallysuitable combination of selecttheir own speeds, theychose speeds thatcoincided with breathfrequency and volume, and (4) breathein synchrony theenergetic optimum within each gait. The optimalspeed for withthe locomotormotions of the body. each gait is also the preferredspeed. As a result,there are The tight1:1 couplingbetween breath and stridefrequency rangesof speed that the animals neveruse forany sustained of quadrupedsmay thereforeresult in a runningspeed, within period. Evidence thatother cursorial mammals have optimal each gait, that is energeticallyoptimal for breathing. As run- runningspeeds comes from the observationof Pennycuick ning speed divergesfrom a theoreticallyoptimal speed, the (1975) that migratingwildebeest and gazelle use only a re- motionsof the body necessary for breathing may begin to inter- strictedrange of speeds withineach gait. fere with the motionsrequired for running,decreasing the Given theseobservations on what mightbe expectedto be a efficiencyof the entiresystem. This would have the effectof generalpattern for vertebrates,it is somewhatsurprising to making the cost of transportdependent on runningspeed findthat Homo sapiens does not have a single energetically (withina singlegait), as it has been shownto be in thehorse. In optimalrunning speed. Over the rangeof speeds (8-20 km/hr) contrast,the capacityof humansto alterthe breathing pattern used byhumans when running long distances, the cost per unit while runningwould eliminate this problem. The striding distancedoes notvary significantly with speed (Margariaet al. bipedal gait of humans, by relaxingconstraints imposed on 1963, Cavagna and Kaneko 1977, Hagan et al. 1980). The lung ventilation,may broaden the range of speeds whichare recognitionof this apparent differencebetween humans and energeticallyviable. quadrupeds raises two immediatequestions. First, what is it The lack of an optimalrunning speed could be viewed as a about humans that detachesthe cost of runningfrom speed? disadvantage,because everyspeed withinthe aerobic scope of Second, what advantages or disadvantagesdoes thisunusual man is as costlyas any other.This is particularlysignificant in situationcreate for the runninghuman? Although the answers thatman is a relativelyinefficient runner compared with other to thesetwo questionsawait furtherexperimentation, several mammaliancursors. On the otherhand, giventhe physiology pointscan be made. necessaryto cope withhigh levels of energyconsumption and There is no evidenceto suggestthat there is anythingpartic- metabolicheat production,a constantcost of transportcould ularlyunusual about human skeletalmuscle. It seems to be providehumans with the option of running at a wide varietyof subject to the energeticand mechanicalconstraints typical of speeds. Quadrupeds,such as thehorse, that appear to be spe- othervertebrate skeletal muscle (see Thorstensson1976). Fur- cializedfor a narrowrange of speeds withineach gaitmay in a thermore,the marked ability of humansto make use of energy practicalsense be limitedto theseoptimal speeds. storedelastically in the tendonsand muscles while running (Cavagna and Kaneko 1977) is not unusual for mammalian cursors(Cavagna, Heglund,and Taylor 1977). Giventhe ordi- STORAGE AND UTILIZATION OF ENERGY narynature of human skeletal muscle, man would be expected to exhibitan optimalrunning speed. Depletionof muscleglycogen stores is one factorthat has been Man does differfrom quadrupeds, however,in the way in implicatedin the developmentof muscle fatigueduring pro-

486 CURRENT ANTHROPOLOGY This content downloaded from 155.97.178.73 on Fri, 27 Nov 2015 17:24:13 UTC All use subject to JSTOR Terms and Conditions longed exercise,forcing animals to stop or slow theirpace Carrier: HUMAN RUNNING AND HOMINID EVOLUTION (Ahlborget al. 1967, Bergstromet al. 1967). The rateat which muscleglycogen is depleteddepends on the level of blood glu- dissipatinglarge exerciseheat loads. Sweat glands that are cose (suppliedby liver glycogen)and the rate of fat oxidation controlledby synapsing,cholinergic neurons occur in Old (Holloszyand Booth 1976). Consequently,the highmetabolic World anthropoidsand appear to be confinedto this group rate of runninghumans combinedwith theirgreat stamina (Robertshaw 1975). These primatesare capable of greater leads to the predictionthat conditioned persons will have un- maximalrates of evaporativecooling during exercise than are usuallylarge reservoirs of (1) muscleglycogen and triglycerides certaincursorial mammals that depend on pantingfor ther- (whichcan be hydrolyzedto freefatty acids), (2) triglycerides moregulation(Taylor and Rowntree1974). Many of the great storedas adipose tissue,and (3) liverglycogen. At presentthe apes (Pongidae) have large bald areas (lack hair) on the face, literaturedoes notcontain the information necessary to address chest,and rump. thisissue. The body'sreservoir of glycogenand freefatty acids 2. The arborealmodes of locomotionof manyanthropoids variesdramatically depending on the diet and physicalcondi- necessitatemodifications of the limbs and trunkthat are transi- tion of the animal (Bergstromet al. 1967, Paul and Issekutz tional to uprightbipedal postureand allow limitedbipedal 1967). This combinedwith a relativelack of informationfrom locomotionin some modernforms (Tuttle 1975). This trend species otherthan man makes interspecificcomparisons im- towardsbipedality presents the possibility of enhanced transfer possibleat thistime. betweengravitational potential and kineticenergy while walk- A diet enrichedin carbohydrates,maintained for several ing. Bipedalityalso releases the mechanicalconstraints im- days,doubles muscleglycogen and enhancesendurance in hu- posed on the breathingcycle by locomotion,thereby making mans (Bergstromet al. 1967, Karlssonand Saltin 1971). Con- possiblea varietyof breathingpatterns. versely,a dietrich in proteinand fatdecreases muscle glycogen 3. The adrenal and thyroidglands of primatesare hyper- and prematurelydepletes glycogen during exercise (Gollnick et plastic compared with those of othermammals (see Spuhler al. 1972). Humans can adjust the concentrationof glycogenin 1979). This hyperplasticitymay increase the levels of those the muscles, and thus theirphysical performance, by short- hormonescritical to the mobilizationand utilizationof fatty termchanges in diet. It is unknownwhether this allows hu- acids and glucoseby muscles. mans to concentrateglycogen at higher levels than those 4. The omnivorousdiet of most anthropoidsopens up the reachedby othermammals. Presumably the optionof "carbo- possibilityof increased glycogen storage in themuscles through loading"is notavailable to thosepredators that are strictcarni- carbo-loading. vores(e.g., canids and felids). Hence, in these respects hominids may have been pre- During exercisethe mobilizationand rate of utilizationof adapted to endurancerunning. However, in orderto become carbohydratesand fattyacids by musclesis controlledlargely an endurancerunner man has had to overcomethe handicap by the circulatingconcentrations of fivehormones: epineph- imposedby a relativelyhigh energetic cost of transport.Given rine,norepinephrine, adrenocorticotrophic hormone (ACTH), thisconstraint, the fact that humans have exceptionalstamina glucagon,and thyroxine(Stryer 1975). Because onlylow levels suggeststhat at some pointin the evolutionof hominidsthere of thesehormones are storedin the body,a freshsupply must was strongselective pressure for endurance running. be synthesizedas the need arises. Withthe exception of gluca- Mammals runfor a limitednumber of purposes.Running is gon and ACTH, all are producedby the thyroidand adrenal oftena formof play, especiallyamong young cursorial mam- glands. As has been notedby Spuhler(1979), theseglands are mals. This is likelyto be of value mainlyfor the conditioning relativelylarge in humans. Spuhler suggeststhat relatively and trainingit provides for runningunder other circum- largegland size may resultin higherlevels of hormone produc- stances.In someinstances running is used formigration. How- tion and, in turn,could be associatedwith the highenergetic ever, mostspecies migrate at a walk, and runningis reported demandsof human endurancerunning. to be rare in thiscontext (Pennycuick 1975). Preyanimals de- pend heavily upon runningspeed and endurance to avoid predators.Because of the greatspeed of the large predators, ENDURANCE RUNNING AND runningis unlikelyto have been of muchvalue to man's early ancestorsas a meansof escape. Runningis also used by preda- There are importantdifferences in locomotionbetween man torsto captureprey. Predation is a behaviorin whichrunning and typicalquadrupeds (fig. 2). In mostquadrupeds, heat dis- ability,particularly endurance running, might have been use- sipationis coupled to the respiratorycycle. This in itselfis ful to early hominids.Although most mammalianpredators likelyto decreasethe capacityto dissipateheat whilerunning. relyon speed and accelerationto overtakeprey animals, a few Added to it is the limitationthat energy-efficient lung ventila- groups(e.g., Lycaon) make use of exceptionalendurance. The tion requiresa specificcombination of breathfrequency and physiologyand morphologyof modernman, combinedwith volumefor any minutevolume. The breathingcycle is in turn what is knownfrom hominid fossils, suggest that long before largely controlledby the locomotorcycle, which is ener- the developmentof complex cultureand huntingweapons, geticallylimited to a specificcombination of stridefrequency earlyhominids may have been endurancepredators equipped and lengthfor any givenrunning speed. These suggestedcon- withbiological weapons forhunting very different from those straintsmay combineto forcea mammal to run at a narrow of othermammalian predators. rangeof speeds in each gaitand limitits maximum rate of heat If, as is thecase forrunning humans, the cost of transportof dissipation.In contrast,in man heat dissipationis not tied to early bipedal hominidsdid not change with runningspeed, respiration,and lung ventilationis largely independentof thenthey would have been freeto pursue preyat any speed locomotion.Therefore, running humans should display greater withintheir aerobic range. They could thereforehave picked plasticityin the criticalfunctions of respirationand heat dissi- the speed least economical for a particularprey type. This pationthan runningquadrupeds. would have forcedthe preyto run inefficiently,expediting its Comparedto thatof other mammals, man's energeticcost of eventualfatigue. For example,a man in runningpursuit of a transportis relativelyhigh. Nevertheless,humans possess ex- horsewould do best to proceedat roughly16-17 km/hr.This ceptional locomotorstamina. Several of the charactersbe- is thespeed midwaybetween the optimal speed of thetrot and lievedto contributeto man's endurancecapacity may be primi- the optimalspeed of the gallop (fig.1) and is a speed at which tive charactersfor Old World Anthropoidea: the animal prefersnot to run (Hoyt and Taylor 1981). 1. The combinationof cholinergic sweat glandsand general An animal pursued at its least economicalrunning speed absence of bodyhair providesman withan effectivemeans for would he faced with two ontions.It could maintaindistance

Vol. 25 * No. 4 * August-October1984 487 This content downloaded from 155.97.178.73 on Fri, 27 Nov 2015 17:24:13 UTC All use subject to JSTOR Terms and Conditions CONSTRAINTS ON SUSTAINED RUNNING

QUADRUPED MAN

Stride Frequency X Stride Length Stride Frequency X Stride Length

Locomotor - RespiratoryCoupling

Breath Freq. X Breath Vol. B. F. X B. V.

I Heat Heat Respiration Dissipation Dissipation

FIG. 2. Constraintson sustainedrunning in typicalquadrupedal mammals and in man. Boxesrepresent possible constraints on thecircled functionsof respiration and heatdissipation.

fromthe predatorby runningat the nonoptimalspeed, or, transportcould give a predatora distinctenergetic advantage morelikely, it could race ahead at a fasterand moreefficient if the preyhad specificoptimal running speeds. speed. The latterof thesetwo escape strategieswould lead to Anotheraspect of human biology that would be usefulfor an intermittentrunning and resting.The preyanimal would out- endurancepredator is man's exceptionalability to dissipate distancethe predatorand, upon stoppingto catch its breath, heat whilerunning. It is truethat the greater energy consump- would findthat the predatorwas stillin pursuit,forcing it to tion of runninghumans generatesa relativelylarge exercise chargeoff once again. It would be forcedinto an intermittent heat load. However, the well-developedsweat glandsof man runningpattern by thecontrasting needs to avoid thepursuing make the whole body surfaceavailable forevaporative cool- predatorand to avoid unnecessaryfatigue and heat stressif the ing. Since evaporativecooling in humansis notlimited, as it is predatorhas given up the chase. This seems, frommy own in pantingmammals, by the rate and volumeof lung ventila- observation,to be what happens when pronghornantelope tion,it representsa meansof thermoregulationthat is compat- (Antelocapra)are pursuedby a runninghuman. ible with running.In addition,one fortunateconsequence of Althoughintermittent running provides brief rest periods, it the lack of body hair in humans is an increase in thermal is probablyless economicalthan continuous running. Tests on conductancewith increasingrunning speed (apparent wind humansshow thatthe workefficiency of intermittentexercise speed). Higher rates of convectionwith increasingrunning on cycleergometers can be as muchas 26% lowerthan that of speed will be muchless prevalentin mammalsequipped with a continuousexercise at the same average power output(Ed- moretypical complement of body hair because of the stagnate wards et al. 1973). Comparedwith continuous exercise, inter- layer of air maintainedby the fur. These thermoregulatory mittentexercise has also been shownto elevatecore body tem- characteristicsof man would certainlybenefit an endurance peratureand decrease evaporative heat loss as a result of predator. reducedsweating (Ekblom et al. 1971). Therefore,whether the There is some anecdotal evidence which suggeststhat the preyran at the pace set by the theoreticalpredator or chose to way in whichhumans dissipate heat whilerunning does play a run intermittently,the end resultwould be inefficienttrans- significantrole in human .Dawson, Robertshaw,and port.In a contestof endurance, a predatorwhose cost of trans- Taylor (1974) found that in spite of sweatingand increased port did not vary with runningspeed would likelyhave a respiratorycooling, red kangaroos are unable to dissipateall of substantialadvantage over a preyanimal that possessed re- the heat producedwhile runningat speeds between4 and 22 stricted,energetically optimal speeds in each gait. km/hr.They calculatedthat, hopping at speedsin thisrange, a In theexample of a man attemptingto rundown a horse,the kangaroo would reach a lethal temperaturein one to two muchgreater efficiency of thehorse would likelyoutweigh any hours.Consequently, it comesas no surprisethat Aborigines of benefitthat the constant cost of transport provided the man. In the warmdesert of northwesternAustralia are reportedto run all probabilitythe man would become exhaustedlong before down kangaroos(Sollas 1924, McCarthy 1957). On veryhot the horse. However, part of the reason that horsesare much summerdays it is a relativelysimple matter for a man to chase more efficientthan humans is the differencein body size be- down the hare, Lepus californicus(Schmidt-Nielsen 1964), tween the two species. The cost of transportscales to the thoughin thecool of earlymorning or duringthe winter this is -0.40 power of body mass (Taylor, Schmidt-Nielsen,and a seeminglyimpossible task. Hottentotsare reportedto run Raab 1970). In general,large mammals consume less energyin swiftprey animals to exhaustionin the heat of the sun (Scha- locomotionthan do small mammals.Where predator and prey pera 1930). Furthermore,Bushmen are known to run down are equal in bodysize or the preyis smaller,a constantcost of wildebeestand zebra duringthe hot dry season butuse alterna-

488 CURRENT ANTHROPOLOGY This content downloaded from 155.97.178.73 on Fri, 27 Nov 2015 17:24:13 UTC All use subject to JSTOR Terms and Conditions tivemethods when hunting these animals during other seasons Carrier:HUMAN RUNNING AND HOMINID EVOLUTION (Schapera 1930). This analysisof the morphologyand physiologyof human Comments locomotion,although incomplete and largelyspeculative, sug- geststhat man is a primatethat has become specialized for by A. K. KAPOOR (among other things)endurance running.This points to a Departmentof Anthropology, University of Delhi, Delhi 110 scenarioconcerning the originof hominidsthat has been pro- 007, India. 12 iv 84 posed in one formor anotherby several authors(Dart and This enlighteningarticle on various aspects of bipedal and Craig 1959,Ardrey 1961, Morris 1967, Krantz 1968). Exercis- not for ex- ing anthropoidprimates can dissipateheat morerapidly than quadrupedal locomotiondoes call much comment cept to link mode of locomotionwith brain size and human certain cursorial mammals. This suggeststhat the earliest Man a of hominidsmay have been moreeffective at heat loss thanmany evolution. can exhaust preyanimal duringthe heat the day, not in the cool of the morning.This phenomenon othercontemporary mammals. Furthermore,early australo- requiresa sense of timing,i.e., of when to hunt,which means pithecineswere fullybipedal. As a result,they were probably thinkingand hence the brain. When did the brain grow notconstrained to the typical1:1 breathingpattern of running large-at the beginningof bipedal locomotionor huntingby quadrupeds.Consequently, it is possiblethat one ofthe impor- hominids?This and the tant factorswhich differentiatedhominids from other an- early question consequencesshould have been discussed thropoids,and ultimatelyled to the evolutionof H. sapiens, here. was the occupationof a new predatoryniche. This hypothet- ical nichewas thatof a diurnalpredator which depended upon exceptionalendurance in hot (midday)temperatures to disable swifterprey animals. by TASUKU KIMURA These hypotheticalearly hominidswere endowed with a Research Institute,Kyoto University,Inuyama, physiologyand morphologythat (1) allowed runningspeeds Aichi 484, Japan. 13 Iv 84 which forcedprey to escape in an inefficientmanner and (2) Carrierproposes the new hypothesisthat ancestral man could provided rates of maximum heat dissipationthat were far pursue a preyof a large body size at the speed energetically above ratesobtainable by theprey. Exploiting this broad range least economicalfor the animal. The hypothesisis veryattrac- of runningspeeds and superiorability to thermoregulate,the tive,but he does notdemonstrate it. An energeticallyoptimum early hominidswere able to capture swiftprey animals by speedin quadrupedalterrestrial mammals has beenexperi- pursuingthem under conditions of high environmental temper- mentallyproven to exist only in horses (Hoyt and Taylor 1981). atureand at speeds differentfrom those for which the animals Horseschange gait pattern (walk, trot, or gallop)and select were physiologicallyspecialized. Initially the prey animals speeds in a mannerthat minimizesenergy consumption. would have been not the large ungulatesbut the less cursorial Whetherthis finding applies generally to terrestrialmammals hares and small artiodactyls(such as Serengetilagusand as Hoytand Taylorassume has notyet been determined. Pre- Raphicerus,which occur in theLaetolil Beds [Leakeyand Hay ciseexperimental analyses on manykinds of animals are called 1979]) and the relativelyhelpless infantsof the largerherd for.On theother hand, this finding does contradict the linear animals. relationshipbetween energy cost of transport and bodymass Alternatively,it has been argued on the basis of limb mor- fordifferent mammals shown by Taylor,Schmidt-Nielsen, phologythat earlyaustralopithecines may not have been par- and Raab (1970). That relationshipwas simplyobtained from ticularlyskilled runners(Jungers 1982, Stern and Susman theenergy cost of moving one unit of body mass over one unit 1983). Also, analysisof the tools and animal bones fromex- ofdistance at infinitespeed. Since the cost of moving one unit cavated Oldowan campsites(Leakey 1971),along withwhat is ofbody mass over one unit of distance depends on the speed of knownof dental morphology,suggests that huntingmay not theanimal, it is notcalculated from the slope of the regression have been an importanthominid activity until the earlyPleis- linebetween the energy cost per unit body mass and perunit tocene(Wolpoff 1980). In thiscase, thisscenario would better timeand speed as Schmidt-Nielsen(1975:248) proposed. applyto the evolutionof locomotionin Homo and mightserve Man'slack of an energeticallyoptimal running speed is ex- to distinguishHomo fromthe australopithecines.Whether the plainedby Carrier in connectionwith the capacity of humans Hominoidea arose as a consequenceof a shiftto a predatory toalter their breathing patterns relative to stride frequency. He life-styleor a divergingsubgroup became huntersat a much andhis coworker (Bramble and Carrier 1983) found that quad- laterpoint, the predatory niche is themost obvious explanation rupedalmammals (hares, dogs, and horses)normally syn- for many of the unique charactersof the primateknown as chronizetheir locomotor and respiratorycycles at a constant man. ratioof stride per breadth. Their original data showedthat a The modelof early hominids as diurnalendurance predators 2:1 ratioappeared to be favouredin humanrunning, though leads to severaltestable predictions. It would be worthwhileto severalbreathing patterns were available. It is difficultto ex- evaluatethe endurance performances of man and modernprey plainthe continuously regular energy cost of human running animals under a variety of temperatureregimens. If this relativeto speedin connectionwith a ratiothat is discontinu- scenariohas any validity,the enduranceperformance of man ous in character. relativeto that of preyanimals should increasewith ambient It is reasonablethat the human mechanisms of thermoregu- temperature.In addition,the speeds at whichmodern primi- lation,sweating and hairlessness,in runningare more advan- tivehunters run down preyshould vary from species to species tageousthan the panting used by many mammals, though this and shouldcorrespond to the preyanimal's nonoptimal speed. is nota newviewpoint. Readers should be awarethat cutane- The questionof whetherthe constantcost of transportof hu- ous evaporationis importantfor thermoregulation notonly in man runnersresults from the wide varietyof breathingratios thethree groups mentioned by Carrier but also in many ungu- used by runninghumans is also relevantto thisscenario. This lates,such as donkeys,llamas, and cattle (Whittow 1971). This could be testedby measuringoxygen consumption in human doesnot, however, influence the fact that human sweat glands runnerswho have been trainedto extendthe range of speed at maybe themost effective. which the differentbreathing ratios are normallyused. The Sakura(1983) has proposedthe hypothesisthat ancestral scenarioalso predictsthat early hominids were scantlyhaired. man occupieda new nicheof diurnalpredator. Most carni- Unfortunately,the fossil record is unlikelyto yieldevidence on voresin thetropics are activeduring times of low temperature this point. and not at midday. Early humans,as newcomers,may have

Vol. 25 * No. 4 * August-October1984 489 This content downloaded from 155.97.178.73 on Fri, 27 Nov 2015 17:24:13 UTC All use subject to JSTOR Terms and Conditions adopted the hot daytimefor theirhunting activity. This hy- WhileCarrier's model does accountfor the enhanced human pothesisexplains man's highlydeveloped mechanisms of ther- physiologicalability to dissipate heat by sweating,it is not moregulation,though it is insusceptibleto directproof. necessaryto postulateendurance running as the cause of the The bipedal walking of living nonhumanprimates is not increased heat load in early hominids.Activities related to energeticallyeconomical compared with that of humans short-rangehunting and scavengingin the open duringthe (Yamazaki et al. 1979). In human erectwalking, the center of hottestpart of the day seem to me sufficient.Consequently, in gravityof the body risesin the stance phase (Cavagna, Heg- myjudgment, Carrier's hypothesis, while interesting, is simply lund, and Taylor 1977). In nonhumanprimates, on the con- unnecessary;the short-rangehunting and scavengingexplana- trary,the centerof gravityof the body drops in the stance tion is simpler and more compatible with the available phase of walking because the knee joint continuesto flex evidence. (Yamazaki et al. 1979; Kimura et al. 1983). Nonhumanpri- One finalquestion: What "biologicalweapons forhunting matesdo not "run"bipedally in the senseof constantlyhaving verydifferent from those of othermammalian predators" did a phase of freetransit (Kimura et al. 1983). The locomotionof earlyhominids possess? Since such predatorspresumably pos- man's ancestorscould not have differedentirely from that of sess weapons of speed, power, and strength,what is leftfor living nonhumanprimates. On the other hand, when man earlyhominids if not intelligence, cunning, and employmentof regularlyhunted relativelylarge animals on the groundhe technology?But employmentof just such "weapons" seems must already have practisederect bipedal walkingand run- more than sufficientto explain the archaeologicalevidence ning.Man's acquisitionof bipedal walkingand runningcannot withoutany need foran explanationbased on theenhancement be explainedin termsof energycost alone. of aerobic physiology.

by MARTIN K. NICKELS by SATWANTI Departmentof Anthropology, Illinois State University,Nor- Departmentof Anthropology, University of Delhi, Delhi 110 mal, Ill. 61761, U.S.A. 29 III 84 007, India. 12 Iv 84 That persistencehunting based on endurancerunning is em- In discussinglocomotor stamina, the authorhas describedthe ployedby somehunters today is notnecessarily germane to the mode of locomotion,respiratory efficiency, and capacity to issue of whetherit was an aspect of the initialexploitation of dissipateheat, but thesystem which plays an importantrole in the hominids'diurnal huntingniche. How prevalentis such endurancerunning, i.e., the heartand circulatorysystem, has endurancerunning in these modernhunting groups? Is it the not been mentioned. primarytactic employed?Just how energy-efficientis it in termsof optimalforaging theory (Hill 1982)?Is thereevidence that endurancehunters engage in "carbo-loading,"or is this merely a trainingpractice employed by competitivelong- by EUGENIE C. SCOTT distancerunners for sporting events? Medical Anthropology,University of California at San Despite thesequestions, I am in basic agreementwith Car- Francisco, San Francisco, Calif. 94143, U.S.A. 11 Iv 84 rier's (and others') conclusionthat occupation of a diurnal The relationshipbetween human energetics,locomotion, and hunting(and I wouldadd scavenging)niche is a majorfeature of evolutionis well summarizedhere. I like theidea ofthe capac- the hominid evolutionarypattern. The question is whether ityof humans to vary theirspeed of pursuitaccording to the endurance runningis necessaryto explain what we know least efficientspeed of the prey animal. This may well be a about early hominidsubsistence patterns; I thinknot. The pursuitstrategy specific to persistencehunters and could per- archaeologicalevidence of deliberatebutchering of animal car- haps be testedby lookingat the speeds at whichhuman hunt- casses at australopithecine-grade(including Homo habilis)sites ers pursueprey with different optimal speeds (or by lookingat in East Africabeginning at about two millionyears ago does nonhumanpersistence hunters?). not indicatehow these animals died (Isaac 1983). As Carrier No one has fullyaddressed the question of the primate origin himselfadmits, the evidencecould equally supporteither de- of the human coolingsystem. Newman (1970), cited by Car- liberatehunting or scavenging.Wolpoff (1980:151) pointsout rier,has pointed out that human thermoregulationrequires thatthe natureof the skeletalremains from the larger animals considerablewater forevaporative cooling. Man can "sweat is consistentwith their having been scavengedfrom carnivore like a horse" but not drinklike one; we are not capable of kills. Additionalsupport of scavengingis the reportof Ship- "tankingup" largeamounts of waterat one timeas are equids man (1984) that some cut marks directlyoverlie carnivore and camelids. As a result,in hot, dryenvironments we must tooth marks on some early Olduvai Gorge faunal remains. drinkmore frequently than other savannah dwellers.As New- Furthermore,that chimpanzeesand baboons are capable of man has pointedout, thishuman cooling system was movedto occasionalsmall-game cooperative hunting based on suchtech- the savannah; it did not evolve there.The humaninability to niques as seizing,brief chasing, stalking (Teleki 1973:168),or consumelarge amounts of waterat one timeis a definitehand- even synchronouspersistence hunting (Harding and Strum icap to a savannahhunter and likelyrequired cultural compen- 1976)without endurance running suggests to me thataustralo- sationbefore the species was able to engagein lengthypersis- pithecinesand earlyHomo were capable of engagingin such tencehunting. behavior. Combined with organized regular scavengingof Carrierstates that the efficientcooling system of humansis larger game animals and enhanced technologicaland com- paralleled in Old World anthropoids,which are assumed to municativeskills, cooperative short-range persistence hunting have originatedin moist,forest habitats. The imageof frugivo- seemssufficient to explainthe archaeologicaland paleontolog- rous,herbaceous, or folivorousprimates moseying around cool, ical evidencefrom as earlyas two millionyears ago. I see no shady forestsdoes not encourage the expectationof strong need to introduceendurance running as a necessaryingredient selectionfor superefficient thermoregulation. What are nonhu- in this earlyadaptive pattern.Persistence in pursuitdoes not man primatesdoing with their efficient heat dissipation mecha- requirethe continuous physical exertion involved in running;it nism?Cursorial primates are rare. may involve perseverancein stalkingor scavenging,patience I would like to know (1) how efficientnonhuman primate while lyingin ambush, or completionof a preplannedcoor- thermoregulationis comparedwith that of humans(I predict dinatedencirclement of prey. Such strategieswould be based thatthe humanform is moreefficient, being an elaborationof principallyon neurologicalchanges in the brains of early the anthropoidpattern selected for improvedcooling during hominidsrather than in theiraerobic physiology. persistencehunting) and (2) how much "use" nonhumanpri-

490 CURRENT ANTHROPOLOGY This content downloaded from 155.97.178.73 on Fri, 27 Nov 2015 17:24:13 UTC All use subject to JSTOR Terms and Conditions matesmake oftheir enhanced sweating capacity (I predictthat Carrier:HUMAN RUNNING AND HOMINID EVOLUTION extensiveperiods of intensephysical activity are rare except perhapsfor Patas). If I am correctin thesepredictions, I would endurancerunning is an excellentexample of the type of activ- like to know if some otherfunction exists for the cholinergic itythat would promoteand maintainthis hypertrophy. Their enervationof primatesweat glands, accountingnot only for associatedenergetic cost duringthis endurance running would the large amountof sweat productionbut also forsome other have been accentuatedby theirrelatively small staturesand factor.Perhaps the efficientthermoregulatory abilities of pri- hence stridelengths (stature estimates: H. habilis, 150-159 matesare a pleiotropiceffect of selectionfor another function, cm, N = 3; H. erectus,158-172 cm, N = 4; Neandertals,166 such as pheromone production,likewise effectedthrough + 6 cm, N = 18), mostof whichare towardthe lower limits of sweat. recenthuman rangesof variation. Recent analyses of the archeologicalrecord (e.g., Binford 1981, 1982, 1984;Camps-Fabrer 1974; Clark 1983;Klein 1978; byJOSEPH K. So Oakley et al. 1977; Potts 1982; Straus 1982) suggesta similar Department of Anthropology,Trent University,Peter- pattern.They indicate the absence of effectivehunting pro- borough,Ont., Canada K9J 7B8. 7 Iv 84 jectileswith hafted points prior to the terminalMiddle Paleo- lithic(Aterian) and Upper Paleolithicand only fire-hardened Carrieris to be commendedfor his thought-provokingtheory. wooden thrustingspears (e.g., Clacton and Lehringenspears) Citingphysiological data, he arguesconvincingly that the hu- man speciespossesses an efficientmechanism for heat dissipa- fromearlier in thePleistocene. In conjunctionwith this, Lower faunal assemblages tionand endurancerunning. It is safe to say thatthese biolog- and Middle Paleolithichominid-derived mammals and ical attributesare uniquely human and may have played a appear to be dominated by small probably of medium-sizedto largemammals. There significantrole at some pointin our evolution.I am less com- scavengedportions is littleto indicatethat archaic humans were routinely hunting fortablewith his assertionthat the success of hominidsas en- animals than themselves.This interpretationof the ar- durancepredators and the abilityto outlastgame animalswas larger cheologicalrecord clearly fitswith both the paleontological theprimary selective force. This modelis based on theassump- evidencefrom archaic humansand Carrier'smodel of endur- tion that huntingwas the dominantmode of subsistence.As ance-runningpredation on smallermammals. Carrierhimself points out, the paleontologicalevidence indi- It is also interestingthat the earliestappearance in the ar- cates the contrary(Jungers 1982, Stern and Susman 1983). recordof hafted thatwould removethe There also existsa body of data thatquestions the validityof cheological projectiles need forhabitual endurance running to captureprey is associ- the "man-the-hunter"school of thoughtrepresented by Wash- ated with the appearance of early anatomicallymodern hu- burn and Lancaster (1968). Cross-culturaldata indicate mans,who show a markedreduction in postcranialrobusticity gatheringas the primarymode of subsistencein 58% of the 90 (Trinkaus 1983) and an increase in locomotorefficiency (as societiessurveyed compared with only 25% forhunting (Mar- indicated by an increase in statureand hence stridelength tinand Voorhies1975). Observationson huntingby chimpan- [European and Near Eastern early anatomicallymodern hu- zees and commonbaboons indicatethat meat is a minorpart of man statureestimates: 178 + 9 cm, N = 27], relativelylonger theirdiets. More importantly,primate hunting does not re- distal limb segments[Trinkaus 1981], and narrowerpelves quire greatskill, strength, or physiologicalendurance as Car- [Trinkausn.d.b]). These are combinedwith evidence of more riersuggests. There is a tendencyto overemphasizethe import- of a diversityof fauna and of more ance of the predominantlymale activityof huntingas a systematicexploitation routine monitoringof available environmentalresources. selectiveforce in hominidevolution at theexpense of the role of These considerationssuggest, therefore, that the predatory en- food gathering(Fedigan 1982, Slocum 1975). A model that durance Carrier have been veryim- accounts for only half of the human species is in my view runningproposed by may of the incomplete. portantamong archaic members genusHomo, permit- their into with Even acceptingthe premisethat endurance was important, ting (among other things) expansion regions markedseasonal variationin plant-foodavailability, but that cooperativehunting ought to be considered.It seems that it decreasedin importanceas logisticallyorganized and essen- whilehumans can chase preyanimals at speeds uneconomical modernhuman duringthe Up- forthe animals,success is possibleonly when severalhunters tially hunter-gatherersemerged Pleistocene. trailthe animal fromdifferent directions. Physiological expla- per nations,while valid and significant,are but one of manyap- proachesto theunderstanding of the evolution of humansocial life. Reply

by DAVID CARRIER by ERIK TRINKAUS Ann Arbor,Mich., U.S.A. 14 v 84 Departmentof Anthropology,University of New Mexico, In recentyears therehas been a tendencyto emphasizethe Albuquerque,NM. 87131, U.S.A. 20 III 84 evolutionarysignificance of scavenging and gatheringforms of Carrier'smodel of hominids as bipedalendurance runners who subsistenceof early hominids.This view is reflectedin the wereable to becomepredators without great strength or elabo- commentsof Nickels and So. Althoughthe available ar- rate technologyis well conceivedand convincing.Most inter- chaeologicaland paleontologicalevidence of earlyhominids is estingly,its implicationsfit with current interpretations of the ofteninterpreted as consistentwith gathering, scavenging, and Pleistocenearcheological and human paleontologicalrecords. short-rangeopportunistic forms of hunting,the possibilityof Archaicmembers of the genus Homo (H. habilis,H. erectus, persistencehunting cannot be excluded.A scavengingand op- and archaic H. sapiens) exhibitpronounced and consistent portunistichunting niche would imposefew selective pressures postcranialhypertrophy (Day 1971; Susman and Stern 1982; and could be filledby manygeneralized large mammals. How- Susman, Stern,and Rose 1983; Trinkaus 1983, n.d.a). This ever, humans are not generalizedmammals. Man's unique impliesconsiderable strength for these hominids. However, it physiologyand morphologycannot be easilyexplained by such primarilyindicates an adaptationfor habitually high levels of an unspecializedsubsistence pattern. If, for instance,man's activity,since osteological hypertrophy is essentially a response exceptionalcapacity to dissipateheat were simply a responseto to fatiguestress (Lanyon 1982).They musttherefore have been generaldiurnal activity, as Nickels suggests,then one might exertingconsiderable effort on a regularbasis, and predatory expectto see similaradaptations in otherlarge savannah main-

Vol. 25 * No. 4 * August-October1984 491 This content downloaded from 155.97.178.73 on Fri, 27 Nov 2015 17:24:13 UTC All use subject to JSTOR Terms and Conditions mals (e.g., heavilysweating and hairlessantelope). Hairless- to be veryimportant in the day-to-daylives of many nonhu- ness,transport cost independent of speed, and thecapacity for man primates. superiorendurance in an energeticallyinferior runner are fea- Nickels and So raise the issue of thesignificance of foraging turesso unique that any explanationdemands extreme selec- practicesof modernhunter-gatherers to the subsistencepat- tion. This selection,I believe, could best be providedby a ternsof man's ancestors.That some modernhunters run prey diurnalendurance form of predation. to exhaustion demonstratesthat modern humans possess Scott'sreference to Newman's (1970) thoughtfulpaper war- greaterstamina than the animals pursued,not thatman's an- rants some discussion.Newman's thesis is based on the as- cestorshunted this way. Moreover,the observationthat this sumptionthat man's exceptionalthermoregulatory capacity re- methodis not the primaryhunting tactic employed by extant sultedfrom an adaptive responseto environmentalheat loads. hominids,with their poison arrowsand rifles,is irrelevantto He speculatesthat hominids lost theirhair in an ancientforest the questionof how earlyhominids acquired protein. There is habitat beforethe move to open savannah. The change in furtherreason to questionthe value of extrapolatingthe prac- habitat fromshady forestto sunnysavannah would greatly tices of modern hunter-gatherersback in time to early increasethe radiant-heatload, particularlyif the animals in hominids.Before the recent invention of cooking fires, much of questionlacked hair. Man's enhanced abilityto sweat is ar- thecaloric and proteincontent of many plant foods used today gued to be a responseto thisincreased impact of radiant energy may not have been digestible(Stahl 1984). This suggeststhat on his naked ancestors.There are two problemswith this animalprotein in some formmay have been moreimportant in scenario.First, Newman does not providea functionalreason the past in meetingnutritional requirements than it is at pres- for the loss of hair. If the forest-dwellingpredecessors of ent. The presumablyrecent advent of greatlyincreased intelli- hominidslost theirfur coats simplyfrom a lack of need, why genceand culturemakes theextrapolation of modern behavior have otherforest primates retained a fullcomplement of hair? backwardin timemore tenuous than is thecase fornonhuman Second, man's exceptionalcapacity for heat dissipationis un- paleontology. likelyto have resultedfrom the impositionof the relatively The questionposed by Nickels of the costs and benefitsof minorenvironmental heat loads to which all large savannah persistencehunting is critical.Running prey for extended pe- mammalsare subjected.It is moreprobable that it is a reaction riodsin hot temperaturesis an energeticallyexpensive under- to the much largerthermal loads producedduring sustained taking. If diurnal endurance predation had a significant exercise.Newman's paper providesmany insights, but I dis- influenceon the course of hominidevolution, it must be an agreewith the basic premisethat hairlessness in man is largely energeticallyviable strategy.The occasionaluse of endurance disadvantageousand thatthe human capacityfor sweating is predationby modernhunters suggests that at least forHomo an adaptive responseto environmentalsources of heat. sapiens it is cost-effective,but thishas yetto be measured.In Scott raises a difficultissue for the persistence-hunting additionto the caloricexpenditure, this type of huntingcould modelin the seeminglylarge discrepancy between man's great have been exceptionallyhazardous because of the prolonged need forwater in thermoregulationand his limitedability to exposureto the sun's radiation,potential for dehydration, and carrya substantialreservoir in his gut (Newman 1970). As increasedexposure to the larger savannah predators.These Scottsuggests, before the inventionof water-carryingdevices, would have representedsignificant obstacles to a primateem- hominids'inability to drinklarge quantitiesof water at any ployingthe run-downtechnique and could have provided one timewould have placed limitson theduration of hunts and strongselection for increased intelligence, group cooperation, the distance covered. This in turn would have limitedthe and precisecommunication. species of preythat could have been acquired throughpersis- Several of the commentators(Kapoor, Nickels, So) address tence running.Certain typesof preywould have been more the issue of the relationshipbetween a huntinglife-style and vulnerablethan others.Hares (Leporidae), for example, are neurologicalfunctions such as intelligenceand social behavior. cursorialopen-country runners that are severelylimited by Groupcooperation plays a significantrole in the huntingof all theirinability to dissipate exerciseheat loads. To facilitate thesocial carnivoresand modernman. Withanimals as intelli- passive heat loss and to conservewater, on hot days hares gentand social as mostof the anthropoid primates, it would be allow theirbody temperatureto rise. This leave littlemargin ridiculousto suggestthat group cooperationwould not have for the additional heat that must be storedduring exercise. been importantin increasedhunting activity. What is really Storageof metabolicheat while runningin theseanimals can moreinteresting is the role thatpersistence hunting may have proceedat rates more than fivetimes the standardmetabolic playedin the evolutionof humanintelligence and way of life. rate. Consequently,the core temperatureof a hare pursuedin A numberof authors(Schaller and Lowther 1969, Laughlin theheat can reach a lethallevel in a fewminutes (Shoemaker, 1968,Washburn and Lancaster 1968,Wolpoff 1980) have con- Nagy, and Costa 1976). Hares of the genera Lepus and sideredthe probable influence of a shiftto a predatoryniche on Serengetilagus(Leakey 1965) were likelyto have been easily the developmentof hominidintelligence and social structure. accessibleto earlyaustralopithecines on shortexcursions away These authorsand othershave stressedthat the shift involved fromsources of water. muchmore than a changein diet. Huntingis suggestedto be a I am somewhatsurprised by Scott'ssuggestion that nonhu- way oflife that has dominatedthe course of hominid evolution man primatesdo not need effectivemechanisms of heat dissi- producingmodern man's intelligence,interest, emotions, com- pation.The dynamiclocomotor performance of primatessuch munication,and basic social life. as spider monkeys,langurs, and gibbonssuggests that these At no point have I suggested,as So states, that primate animals commonlyplace very large demands on theirther- huntingrequires great endurance,skill, or strength;I have moregulatorysystem. Because of the large accelerations arguedonly that endurance running may have providedearly againstgravity, climbing and leaping frombranch to branch hominidswith a reliablemechanism for increasing their intake will always requiremore energythan movingan equivalent of animal protein.Nor can I agree with So's assertionthat distanceon a continuoushorizontal surface. Indeed, brachia- huntingby earlyhominids would necessarilyhave been a pre- tion,the form of arboreallocomotion that could be expectedto dominantlymale activity.Excluding the osteologicalevidence be mosteconomical because of the possibilityof passive sup- of sexual dimorphismin body size (Wolpoff1976), I see no port and the storageand recoveryof energyin the pendular reasonto suppose thatfemales would have been completelyor motionof each swing,has been shownto be less efficientthan partiallyexcluded from hunting. Female membersof the social walkingin spidermonkeys (Parsons and Taylor 1977). Vigor- carnivoresregularly take an active and sometimesdominant ous arboreallocomotion will clearlygenerate substantial meta- rolein hunting.Often young are leftat a den sitein thecare of bolic heat loads, and dissipationof thismetabolic heat is likely a singleadult while the restof the adults engage in hunting.

492 CURRENT ANTHROPOLOGY This content downloaded from 155.97.178.73 on Fri, 27 Nov 2015 17:24:13 UTC All use subject to JSTOR Terms and Conditions Several of the pointsraised by Kimura requireclarification: Carrier: HUMAN RUNNING AND HOMINID EVOLUTION (1) It is unlikelythat ancestral man could have forcedprey to run at theirleast efficientspeed. It is moreprobable that prey Indian tribe of northernMexico. Chicago: Universityof Chicago could have been driven to run intermittentlyand therefore Press. inefficiently.In addition to the relevantdata fromhumans, BERGSTROM,J., L. HERMANSEN, E. HULTMAN, and B. SALTIN. 1967. Diet, muscleglycogen, and physicalperformance. Acta Phys- intermittentrunning has been shown to producefatigue more iologica Scandinavica 71:140-50. rapidlythan continuousrunning in rats (Gaesser and Brooks BINFORD,L. R. 1981. Bones. New York: AcademicPress. [ET] 1980). Intermittentrunning is reportedto be the escape strat- . 1982. Commenton: Rethinkingthe Middle/UpperPaleolithic egy used by prey animals fleeingBushman runners(Bjerre transition,by R. White.CURRENT ANTHROPOLOGY23:17 7-81. [ET] 1960). (2) The breathingof a runningquadruped is tightly . 1984. Faunal remainsfrom Klasies River Mouth. New York: coupled to the locomotorcycle, usually at a rateof one breath Academic Press. [ET] BJERRE, J. 1960. Kalahari. New York: Hill and Wang. per stride(Bramble 1984). The breathingof conditionedhu- BOJE, 0. 1944. Energyproduction, pulmonary ventilation, and length man runnersis typicallyalso synchronizedto the locomotor of steps in well-trainedrunners working on a treadmill.Acta Phy- cycle. The differenceis that in humans the integerratio of siologica Scandinavica 7:362-75. strideper breath varies dramatically depending on theindivid- BRAMBLE, D. M. 1984. "Locomotor-respiratoryintegration in running ual and conditions.This abilityto shiftratios is exactlythe mammals." Proceedings of the Association of Equine Sports mechanismsuggested here to providea costof transport that is Medicine, pp. 42-53. BRAMBLE, D. M., and D. R. CARRIER. 1983. Running and breathing independentof speed in runninghumans. (3) The reader in mammals.Science 219:251-56. shouldbe aware thatdonkeys are membersof the horsegenus CAMPs-FABRER, H. Editor. 1974. L'industrie de l'os dans la pre- Equus, llamas are a species of South Americancamel, and histoire. Aix-en-Provence:Editions de l'Universitede Provence. cattleare membersof the familyBovidae. [ET] I am intriguedby Trinkaus's alternative interpretation of the CAVAGNA, G. A., N. C. HEGLUND, and C. R. TAYLOR. 1977. Me- early chanical workin terrestriallocomotion: Two basic mechanismsfor functionalsignificance of the relativelyrobust bones of minimizingenergy expenditure. American Journal of Physiology hominids.If osteologicalhypertrophy is primarily a responseto 233:R243-61. fatiguestress and hence to habituallyhigh levels of activity, CAVAGNA, G. A., and M. KANEKO. 1977 Mechanical work and thenthis should be readilyapparent in allometriccomparisons efficiencyin level walking and running.Journal of Physiology of the bones of species thathave differentactivity patterns. A 268:467-81. comparative interspeciesanalysis of bone dimensionsand CAVAGNA,G. A., F. P. SAIBENE, and R. MARGARIA. 1963. External work in walking.Journal of Applied Physiology 18:1-9. locomotorperformance would help clarifythe extentto which CAVAGNA, G. A., H. THYS, and A. ZAMBONI. 1976. The sources of thisrelationship can be used to estimatelocomotor behavior of externalwork in level walkingand running.Journal of Physiology extinctspecies. 262:639-57. A view thatseems to be held by manyanthropologists is that CAVANAGH, P. R., and K. R. WILLIAMS. 1982. The effect of stride huntingcould not have been an importanthominid activity length variation on oxygen uptake during distance running. until the early or mid-Pleistocene.Given the available ar- Medicine and Science in Sportsand Exercise 14:30-35. CENA, K., and J. L. MONTEITH. 1975. Transfer processes in animal chaeologicaland paleontologicalevidence, this is a reasonable coats. 2. Conductionand convection.Proceedings, Royal Society of position.However, I would like to emphasizethat persistence London,Series B, 188:395. huntingcould have played a significantrole in the acquisition CLARK, J. D. 1983. "The significanceof culturechange in the early of meat long beforethe firstclear evidenceof hominidpreda- later Pleistocenein northernand southernAfrica," in The Mouste- tion. We know that the early australopithecineswere fully rian legacy.Edited by E. Trinkaus,pp. 1-12. BritishArchaeolog- their runningis likelyto have been less ical ReportsS164. [ET] bipedal. Although CROSFILL, M. L., and J. G. WIDDICOMBE. 1961. Physical characteris- efficientthan that of Homo, it was probablyno more costly tics of chestand lungsand the workof breathingin differentmam- than the quadrupedal runningof theirprehominid ancestors. malian species.Journal of Physiology 158:1-14. Over the range of speeds at which measurementshave been DART, R. A., and D. CRAIG. 1959. Adventureswith the missinglink. made, thecost of bipedal runningis notdifferent from the cost New York: Viking. of quadrupedal runningin chimpanzeesand capuchin mon- DAWSON, T. J., D. ROBERTSHAW, and C. R. TAYLOR. 1974. Sweating in the kangaroo:A coolingmechanism during exercise, but not in keys (Taylor and Rowntree 1973b). Instead of imposingan the heat. AmericanJournal of Physiology 22 7:494-98. energetichandicap on theinitial bipeds, the shift to runningon DAY, M. H. 1971. Postcranialremains of Homoerectus from Bed IV, two legs may have significantlyincreased the range of avail- Olduvai Gorge,Tanzania. 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Wanted public-policy-relatedworks on biomedicaltechnologies, hu- man ecology,health and environment,aging, food, popula- tion,and reproductivetechnologies; (2) theinfluence of biolog- * Correspondenceand suitable bibliographicreferences from ical factors on political behavior; (3) the relationshipof anthropologistsinterested in the ethnographyof blindness,in ethologyand sociobiologyto the concernsof traditionalpolit- connectionwith fieldworkamong the blind in Israel. Please ical scienceand ethics;and (4) therelationship of biopoliticsto write: Shlomo Deshen, Department of Sociology and An- otherperspectives in the social and naturalsciences, for the thropology,Bar-Ilan University,Ramat-Gan, 52100 Israel. journal Politics and the Life Sciences. Data-based empirical studies are especially welcome. Please write: Thomas C. * Papers dealingwith the lives, careers,and achievementsof Wiegele, Editor, NorthernIllinois University,DeKalb, Ill. eminentanthropologists from any countryof the world,for a 60115, U.S.A. volumein preparationentitled Eminent Anthropologists: Bio- graphicalPortraits. Papers shouldbe no longerthan 20 pages, * In connectionwith a dissertationon incipientcultivation typeddouble-spaced, using the footnotingrules of theAmeri- among Negrito hunter-gatherers,quantitative data on rice can Anthropologist.Three clean copies plus brief resumes swiddensin SoutheastAsia fora literaturereview and cross- should be sent beforeSeptember 1985 to Mario D. Zamora, culturalcomparative study. Information is requestedon pub- Departmentof Anthropology,College of William and Mary, lishedreferences on riceyields, swidden sizes, numberof rice Williamsburg,Va. 23185, U.S.A. varieties per swidden, and percentageof burned area left uncropped. Please write: Thomas N. Headland, Bagabag, * Manuscriptson a varietyof biopoliticaltopics, including (1) Nueva Vizcaya Province,Philippines 1505.

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