Juvenile Subsistence Effort, Activity Levels,and Growth PatternsMiddle Childhood among Pumé Foragers

Karen L. Kramer & Russell D. Greaves

Published online: 15 September 2011#

Abstract Attention has been given to cross-cultural differences in adolescentgrowth, but far less is known about developmental variability during juvenility(ages 3–10). Previous research among the Pumé, a group of South Americanforagers, found that girls achieve a greater proportion of their adult stature duringjuvenility compared with normative growth expectations. To explain rapid juvenilegrowth, in this paper we consider girls’ activity levels and energy expended insubsistence effort. Results show that Pumé girls spend far less time in subsistencetasks in proportion to their body size compared with adults, and they have lowerphysical activity levels compared with many juveniles cross-culturally. Low activitylevels help to explain where the extra energy comes from to support rapid growth ina challenging environment. We suggest that activity levels are important to accountfor the variation of resource and labor transfers in mediating energy availability.

Keywords Juvenility . Life history . Human growth . Physical activity levels (PAL) .

Hunter-gatherers (Foragers) . South American Indians . Pumé

Human juveniles are remarkable in several ways. Juveniles grow more slowly, andthe duration of immaturity is longer, than would be expected for an ape of our size(Kaplan et al. 2000; Walker et al. 2006a). Whereas nonhuman primate juveniles areindependent feeders, the metabolic cost of human juvenile growth is partiallysubsidized by others (Lancaster et al. 2000). Human juveniles also have an improvedchance of surviving. The probability of death is two to three times greater for anonhuman primate than for a human juvenile (Hill et al. 2001). Although juvenilityis a dangerous time for a nonhuman primate juvenile (Janson and van Schaik 1993),

Hum Nat (2011) 22:303–326DOI 10.1007/s12110-011-9122-8

K. L. Kramer (*)Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138, USAe-mail: kkramer@fas.harvard.edu

R. D. GreavesPeabody Museum of Archaeology and Ethnology, Harvard University, Cambridge, MA 02138, USA

Springer Science+Business Media, LLC 2011

for a human the lowest probabilities of death occur between ages 5 and 10–15 (Earlyand Peters 1990; Gurven and Kaplan 2007; Hill and Hurtado 1996; Howell 2000).These three features—slow growth, subsidized growth, and survival advantage—canbe related through energy budgets. The fact that human juveniles are subsidizedintroduces an important source of variation in the energy available for growth andmaintenance, not only through caloric input from others but, importantly, throughenergy expended in subsistence effort.

Juvenility refers to a specific period in offspring development, although it has beendefined in several ways. As a sharedmammalian trait, the juvenile period is bracketed byweaning and sexual maturity. Juveniles are independent of their mothers, but not yetfully grown. Human juvenility is often defined more narrowly because additionaldevelopmental stages are inserted after weaning (childhood) and before sexual maturity(adolescence). In preindustrial societies, weaning and the end of infancy occur onaverage at 29.0 (±10.0) months (Sellen 2006:189). The uniquely human stage ofchildhood (sensu Bogin 1999), which follows weaning, is characterized by rapid braingrowth and development of the digestive tract, and it ends with the eruption of the firstpermanent molar and the ability to consume adult foods (approximately ages 3–7).During juvenility, children in many preindustrial societies become economicallyengaged, provisioning some of their own calories but remaining dependant on othersfor some portion of their resource needs. Adolescence, which is not particular tohumans (Leigh 1996), is identified by a sharp rise in growth rates that coincides withhormonal changes and the initiation of pubertal events. Following its treatment in therest of this special issue on middle childhood, we define juvenility as the period ofslow growth from ages 3 to 10. Where applicable, we distinguish age groups 3–6 and7–10. In this context we use the terms middle childhood and juvenility interchangeably(see Campbell 2011 for full discussion).

Various perspectives have been forwarded to explain the long, slow juvenile period inprimates generally (Charnov and Berrigan 1993; Janson and van Schaik 1993) andspecifically in humans (Blurton Jones and Marlowe 2002; Bock 2002a; Dunbar 2003;Gurven and Walker 2006; Hawkes et al. 1998; Hill and Kaplan 1999; Hrdy 2009;Kaplan et al. 2000; Walker et al. 2006a). Although the prolonged human juvenileperiod contributes to the relatively late age of sexual maturity, growth during middlechildhood is an issue distinct from age at first birth and body size trade-offs. Our focusin this paper is on variation in female juvenile growth. Because humans subsidizejuveniles, provisioning affects energy expended in activity in ways not applicable tononhuman primate juveniles who are independent foragers. This also introducespotential cross-cultural variation in energy available for growth. Juvenile activity levelshave been discussed in terms of reduced expenditure and obesity in developed societies(Popkin and Gordon-Larsen 2004), but few activity data are available for preindustrialpopulations, particularly for foragers. We use the ethnographic example of the Pumé, agroup of South American foragers indigenous to the savannas of Venezuela, to evaluateactivity levels in relationship to the Pumé pattern of rapid growth during juvenility.

Pumé girls grow up in a savanna environment with distinct seasonal and annualfluctuations in food supply, and under harsh epidemiological conditions. Previousresearch has shown that Pumé girls invest in early skeletal growth (Kramer and Greaves2010; Kramer et al. 2009). When height is expressed as the proportion of mean adultbody size to standardize for populational body size differences, Pumé girls reach 88%

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of mean adult stature by age 10 (Table 1). In comparison with other traditional foragersand horticulturalists (Walker et al. 2006b), Pumé girls are at the upper end of the rangeof variation in height. Compared with Centers for Disease Control (CDC) standardsfor industrialized children, Pumé girls are taller relative to adult size during juvenilityand may not experience a distinct adolescent growth spurt. Trends are similar for bodyweight. We focus on height because skeletal maturity is the developmental hurdle girlsmust pass to reach menarche, the gateway to sexual maturity (Ellison 1981, 2001).Although Pumé girls deviate from normative growth expectations during develop-ment, their adult height is normal with respect to other native South Americans (DíazUngría 1966: cuadro 2; Salzano and Callegari-Jacques 1988:156). Pumé adult statureis slightly taller than that of the Hiwi, an unrelated group of foragers who live 50 kmto the northwest in a similar environment (Hurtado and Hill 1990; Walker et al.2006b), but their growth during juvenility is similar.

In this paper we expand on this pattern of rapid juvenile growth to investigate theassociation between early investment in growth and energy expended in activity.Before presenting the data, we first outline key biological mechanisms that affectvariability in juvenile growth patterns and energy allocated to growth, maintenance,and activity. We then briefly describe an allocation framework that provides amechanism to account for variability in energy expenditure. Following the analysis ofPumé girls’ activity patterns, we compare these results with available cross-cultural dataand with the Maya, a group of subsistence agriculturalists from Yucatan, Mexico, forwhom we also have detailed individual-level juvenile time-allocation data, to comparephysical activity levels (PAL).

Variability in Juvenile Growth Patterns

The human normative growth curve (Bock and Thissen 1980; Bogin 1999) shows thatvelocities decline sharply during infancy, remain low and flat during early childhood,and rise slightly in a mid-growth spurt at the end of childhood. During juvenility,growth rates decline again, and from about ages 7 to 10 children grow at their slowest

Table 1 Height, weight and BMI for Pumé females girls at age 10 based on cross-sectional growth curves(n=50; Kramer et al. 2009). Adult mean given for females ages 21–40 (n=25)

At age 10 Adult mean

Height

Average cm 133.1 151.5

Percent of adult mean 88%

Weight

Average kg 29.2 51.5

Percent of adult mean 57%

BMI

Average BMI 16.5 22.4

Percent of adult mean 74%

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rates since birth. Children pass through adolescence quickly, with a sharp inflection ingrowth rates (Bogin 1999; Tanner and Cameron 1980). During this sinuous path tomaturity some aspects of growth are canalized, such as rates of cellular proliferationand the sequence of developmental events (Ellison 2001; West et al. 2001). However,other aspects, such as the timing and magnitude of growth rate inflections, may vary.For children growing up in fluctuating or challenging nutritional and epidemiologicalenvironments, the adolescent growth spurt may be delayed, diminished, and/orprotracted (Blurton Jones 2006; Bogin et al. 1992; Cameron 1991; Cameron et al.1994; Sellen 1999). Although explicit attention has been given to cross-culturaldifferences in adolescent growth and pubertal events, far less is known aboutdevelopmental variation during juvenility.

The expectation of a slow juvenile period followed by a quick adolescent growthspurt is based largely on growth models developed from anthropometric surveysamong industrialized populations. These populations have access to health care,calorically dense market foods, fertility control, initiate childbearing in theirtwenties, and have infant mortality levels of less than 1%. To a growing child theserepresent evolutionarily recent and novel conditions. Children living in foragingsocieties face very different challenges. Many grow up in environments withfluctuations in food supply (Bailey and Peacock 1988; Draper and Howell 2005; Hillet al. 1984; Hurtado and Hill 1990), under harsh epidemiological conditions(Froment 2001; Sugiyama and Chacon 2000), with little or no access to marketfoods, health care, immunization, or birth control (Biesele and Hitchcock 2000;Draper and Howell 2005). They are likely to initiate reproduction before the age of20 (Blurton Jones et al. 1999; Early and Peters 1990; Hawkes et al. 1998; Kaplanand Lancaster 2000). Although their probability of survival is improved comparedwith that of a nonhuman primate juvenile, forager juveniles have about a 10%chance of not surviving to age 15 (Gurven and Kaplan 2007). Given thesedifferences and the known impact that background conditions have on adolescentgrowth, juvenile growth also should be expected to vary.

In a cross-cultural comparison of children 3 to 10 years old living in preindustrialsocieties, growth rates vary between 1.1 and 2.9 kg/year for weight and between 4.2and 7.1 cm/year for height (see Tables 2 and 3 in Walker et al. 2006b). Growthpatterns are affected by complex interactions between genetic, environmental, andhormonal factors. Adolescent growth appears to be under tighter genetic control thanjuvenile growth. In contrast, environmental influences on height-for-age are greaterduring childhood and decrease from juvenility through the teens (Beunen et al. 2000;Hauspie and Susanne 1998). In terms of environmental influences, juveniles areparticularly sensitive to infection and nutritional conditions (Ulijaszek 2006).

Energy Allocated to Growth vs. Maintenance

In life history approaches to maturational pace, high juvenile mortality is associated withrapid development (Charnov and Schaffer 1973; Cole 1954; Jones et al. 2008; Olsen etal. 2004; but see Stearns and Koella 1986; Williams 1966). In humans, gains in heightand weight from ages 3 to 10 are relatively faster in populations with high juvenilemortality, when population differences in body size are considered as an assay fornutrition (Walker et al. 2006b). Other studies more generally relate high-mortality

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regimes with fast life histories (Chisholm et al. 2005; Geronimus 1992; Migliano et al.2007; Promislow and Harvey 1990; Wilson and Daly 1997). The association of highmortality with rapid growth is a compelling life history pattern that is empiricallysupported in human populations. It is also consistent with Pumé high mortality and afast growth and early reproductive schedule (Kramer 2008). However, several energyallocation points remain unexplained.

First, as originally specified (Charnov and Schaffer 1973), the sensitivity of age atmaturity to juvenile mortality is specifically a sensitivity to extrinsic mortality rates(mortality rates that are not a consequence of energy available to an individual or ofan individual’s allocation decisions). However, predictions made from this modelmay need some adjustment since human juvenile mortality is likely influenced byenergy inputs from others, especially during illness and disease. For provisionedjuveniles, energy available for maintenance and growth is not limited by their ownsubsistence efforts. If juvenile mortality is sensitive to energetic condition, foodtransfers should positively affect energy balance through not only calorie input butalso the reduction in energy that would otherwise be expended in subsistenceactivity.

Second, the biological mechanism to explain mortality-based pressure on rapiddevelopment is unspecified. Without health care, vaccination, or modern sanitation,many preindustrial environments are immunologically challenging to juvenile well-being. In these environments, we would expect a greater proportion of anindividual’s energy to be allocated to immune function. Immune activity is a centralcomponent of maintenance and has been shown to raise metabolic rates and energyexpenditure in a variety of animals (Martin et al. 2003; Ots et al. 2001). Immunecosts are greater when children are young and the immune system is developing, andthey decrease into adulthood. Mounting even a mild immune response, especiallyfever, is potentially costly (Derting and Compton 2003). For every 1° (C) increase inbody temperature, basal metabolic rate is estimated to rise approximately 12%(DuBois 1937; Stettler et al. 1992). Activation of immune function during aninfection costs a child an equivalent of 19 kcal/kg/day (McDade 2003). All elsebeing equal, upregulated immune function would leave less energy available forgrowth.

In a two-way trade-off between growth and maintenance the solution isconstrained. Children living in immunologically challenging environments shouldgrow more slowly. However, this appears contrary to the empirical observation offaster growth in epidemiologically harsh environments (Kramer and Greaves 2010;Walker et al. 2006b).1 We recognize that many factors affect growth rates, but herewe focus on the roles that activity level and expenditure in subsistence effort play asmechanisms in mediating energy availability.

1 One means to achieve early maturity is for an individual to stop growing at a younger age, at a smallerbody size (Migliano et al. 2007; Walker and Hamilton 2008). Early maturity has been associated with achange in extrinsic juvenile mortality in a number of animal species—either from disease, predation,culling, or fishing pressure (Jones et al. 2008; Olsen et al. 2004). The emphasis of these studies is on earlyreproductive age, not specifically juvenile growth.

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Energy Expended in Growth vs. Activity

Between the ages of 3 and 10 a juvenile consumes approximately 4 million calories.2

Juveniles in preindustrial societies have complex economic relationships with theircaretakers, who often provide some portion of what juveniles need (Bird and BliegeBird 2005; Bliege Bird and Bird 2002; Blurton Jones 1993; Blurton Jones et al.1989, 1994, 1997; Cain 1977; Kaplan 1996; Kasarda 1971; Kramer 2002; Lee andKramer 2002; Nag et al. 1978; Reynolds 1991; Sugiyama and Chacon 2005; Turke1988; Zeller 1987). Juveniles are able to produce some of what they need at the levelof their own consumption and other resources in excess of their consumption—fetching water, harvesting, fishing, foraging for fruit, and collecting shellfish aregood examples. Juveniles also depend on others for some of what they need. Foodtransfers have the obvious effect of raising overall energy availability and smoothingfluctuations in juvenile foraging returns.

Subsidies also importantly affect the time and effort a juvenile expends insubsistence activities. Depending on ecology, sharing patterns, and other wayschildren can spend their time, juveniles may expend more or less energy in activitiesthat contribute to their survival and growth. Variation in energy expended in activityis potentially significant because it is a relatively large proportion of total dailymetabolic cost. In a sample of rural subsistence populations, adults spend 35–58% oftheir total daily caloric budget in physical activity (Leonard 2003:484). Among theMaya, for whom we have age-specific data, adults expend about 45% of their dailycaloric budget in subsistence activities, and juveniles about 20%.

Cross-culturally, children commit different amounts of time to subsistence activities.Table 2 lists all known published sources on the time juvenile girls spend working inpreindustrial societies (studies that do not distinguish boys from girls, or that providepercentages without the duration of the observation day, are not included). Althoughthere are methodological differences among studies (data collection methods andreported age ranges may vary from study to study), values for all groups include timechildren spend in resource acquisition and domestic tasks and are generallycomparable (for more detail, see Kramer 2005a: Table 7.5). Although childcare is animportant children’s task, it is not consistently reported in relation to subsistence workacross studies and is not included in these time estimates. Time allocated tosubsistence activities crosscuts modes of subsistence. Notably, forager children showboth high and low participation in economic activities, suggesting that children’s workeffort varies with factors other than whether a child is a forager, agriculturalist, orpastoralist per se. This variation is of interest because it affects the extent to whichchildren expend energy to meet their own metabolic requirements.

A pooled energy model (Fig. 1) summarizes these points (Kramer and Ellison2010; Kramer et al. 2009). A given calorie can be expended in three ways: onmaintenance, production, or activity. Following from Gadgil and Bossert’s (1970)seminal formulation, most life history allocation models delimit two principal energyexpenditures—on maintenance and on production. Energy balance in excess ofmaintenance can be spent in production. In an immature individual this is allocated

2 Based on age, sex, height, and weight-specific resting daily BMR adjusted for activity level in Mayagirls. Activity levels are averaged from year-long time-allocation data (Kramer 2005b).

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Table 2 Cross-cultural comparison of the daily hours that girls allocate to subsistence activitiesa

Group Daily hours of work Source

Foragers Hadza 5.2 Hawkes et al. 1997:556

Kung 0.6 Draper and Cashdan 1988:349

Pumé 0.99 (data presented in this article)

Horticulturalists Machiguenga 1.9 Johnson 1975:305

Piro-Machiguenga 2.1b Gurven and Kaplan 2006:40

Mixed economy Mikea 2.7 Tucker and Young 2005:155

Agriculturalists Java 4.9 Nag et al. 1978:295

Nepal 7.5 Nag et al. 1978:296

Java 2.8 White 1975:141

India 5.2 Skoufias 1994:340

Bangladesh 6.7 Cain 1977:216

Maya, Yucatan 4.3 Kramer and Boone 2002:308

Mayo, Sonora 6.5 Erasmus 1955:330

Dominica 1.8 Quinlan et al. 2005:475

Pastoralists Ariaal 9.6 Fratkin 1989:434

Kipsigis 4.9 Borgerhoff Mulder 1997:43

a Subsistence activities include resource acquisition (foraging, hunting, fishing, and agricultural work) anddomestic tasks (food processing, preparation, cooking, raw material processing, tool manufacture, haulingwater, chopping firewood, washing, cleaning, building a fire, sewing, weaving, etc.)b Value at age 10

Age categories reported in published sources vary from group to group. Values given here include childrenca. ages 3–12

Fig. 1 The pooled energy model is a modification of the classic two-way trade-off model betweenmaintenance and production (Kramer and Ellison 2010). A given calorie can be allocated to maintenance,production, or activity (A). Energy available to a subsidized juvenile can vary through two main pathways:energy input, either from self provisioning or food transfers from others (B), or through energy expendedin activity (C). The double arrow shown between pooled energy and activity signifies that a juvenile bothdraws from and contributes to pooled energy budgets through activity. The arrow between energyavailability and activity is dotted (D) to indicate that energy expended in activity is not a necessaryfunction of metabolic requirements. The strength of the arrows varies depending on age, sex, subsistenceecology, the kinds of activities in which children engage, food sharing, and labor cooperation patterns

Hum Nat (2011) 22:303–326 309309

to growth and becomes available for reproduction at sexual maturity (Charnov 1991;Stearns 1992). Energy allocated to activity is usually unspecified because foragingeffort is assumed to be a function of body size for a self-provisioning individual.However, comparative primate studies indicate that humans have higher daily energyexpenditures than would be predicted from body size (Aiello and Key 2002; Leonardand Roberson 1997). Although these comparisons are for adults, they are relevant tojuveniles because they suggest that at least some of the higher energy expenditure ofadults is related to provisioning young and to other sharing. In the pooled energymodel, energy allocated to activity is specified to account for the effects of theseintergenerational transfers on activity levels.

We focus on activity to address how juveniles may shift the use of energy indifferent environments. The pooled energy model delineates activity as themechanism through which energy available for growth may vary. If maintenance,growth, and activity are competing expenditures, any downward adjustment inactivity levels should increase the energy available for alternate allocations.

Age Patterning in Children’s Labor

Discussions of age-patterned variation in subsistence effort have focused onconstraints of learning skills, strength, and the age-specific relationship betweentime allocation and return rates (Bock 1995, 2002a, 2005; Gurven and Kaplan 2006;Kramer 1998, 2002). How much time an individual spends at a task and howefficient he or she is at that task are linked through opportunity costs, or the forgonebenefit to an individual to invest in one activity and not another (Hames 1992;Winterhalder 1983). For example, previous research with Maya children showed thattask difficulty, whether juveniles learned by working, and age-specific return ratescorrelated with the amount of time allocated to subsistence effort (Kramer 1998,2005a). Emphasis also has been placed on the opportunity cost of spending time inwork vs. in noneconomic activities such as school and other learning (Bock 2002b;Gurven and Kaplan 2006). These studies further understanding of the division oflabor, age-specific production patterning, and cross-cultural variation in children’slabor and parental investment. Our goal in this paper is not to identify factors ortrade-offs that affect what kinds of tasks children perform, but to examine theproximate mechanisms of how allocations to activity may affect energy available forgrowth.

Pumé girls grow up in an environment with distinct seasonal undernutrition,annual fluctuations in food supply, very little access to market food, and nosupplemental food programs, access to health care, or modern sanitation. Previousresearch has shown that despite these conditions, Pumé girls are larger than expectedduring juvenility (Kramer and Greaves 2010; Kramer et al. 2009). In this paper weinvestigate how activity levels may help explain where the energy comes from forjuveniles to grow more quickly than expected compared with normative growthcurves. The Pumé are an ideal case to investigate the role that activity plays inaffecting residual energy balance because the Pumé are food-limited and caloriesupplementation or preferential feeding do not explain Pumé girls’ rapid development.However, the time girls allocate to subsistence activities is potentially adjustable. This isexpected to be an important mechanism affecting overall energy budgets.

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Study Population and Methods

Pumé Foragers

The Pumé of west-central Venezuela inhabit low-lying plains (llanos) drained bytributaries of the Orinoco River. The Pumé who live on the savannas between thesemajor rivers are mobile central-place foragers, moving camp five to six times a yearin response to the hyperseasonal variation in rainfall and the water table. During thesix-month dry season, subsistence centers on fish and wild mangos. When the llanosflood during the wet season, the Pumé move their camps to higher ground andaggregate into extended families (Gragson 1989; Greaves 1997a, 2006; Mitrani1988). Fish are dispersed and difficult to locate during the wet season, and theresource base shifts to small game, wild roots, and bitter manioc (Greaves 1997b).Food is most abundant during the dry season, and disease exposure is minimalcompared with the wet season. Nutritional stress, extreme in some years, is mostpronounced during the wet season. This is also the period of highest disease incidence.

None of the three savanna study communities has a school, health clinic, store,electricity, well water, nor can they be reached by permanent road. No savanna Puméchild in our sample has attended school, is literate, or speaks Spanish. The savannaPumé have access to a few nonlocal goods through trade with the river Pumé, theirhorticultural neighbors who live along the major rivers that are the transportationroutes into the region. In the past, vaccination teams sporadically visited the savannainterior. Some older individuals have been immunized, but these visits have notoccurred for some time, and very few children (n=3) in the study communities havebeen inoculated in the past 10 years.

Pumé male and female foraging activities focus on different food resources.Fishing and hunting are almost exclusively male activities, and root collection is afemale activity. Both men and women participate in collecting mangos, althoughabout 70% of mango returns (by weight) are from women. Males and femalesparticipate fairly equally in manioc garden work, which yields about 10% of the dietduring the wet season. Pumé girls sometimes accompany women on foodprocurement trips but more often stay in camp, caring for their younger siblings,collecting water, and performing other domestic tasks while their mothers forage.

Savanna Pumé girls reach menarche on average at age 12.96, a normal age withrespect to other native South Americans. Average age at first birth is 15.5, with 90% ofPumé women having their first child between ages 15 and 19 (Kramer 2008). AlthoughPumé girls initiate childbearing at a younger age than the few other groups of foragersfor whom data exist, first birth occurs at an age that is biologically predictable givenage at menarche, a normal period of subfecundity, and because girls are married andengage in sexual activity soon after menarche (Kramer and Greaves 2010).

Data Collection

A subset of females who took part in the 2005–2007 growth study participated in thetime-allocation study. This subset consists of girls and women from one of the studycommunities (n=32). Standard time-allocation methods were used to compile thescan sample and focal follow data base (Altmann 1974; Borgerhoff Mulder and Caro

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1985; Hames 1992; Johnson 1975; Kramer 2005a). Instantaneous scan samples (n=5,663) were collected for females ages 3 to 68 every hour on most days during the2006 dry season. Daylight hours (from 7AM to 6:30PM) were broken into threeblocks, two of which were sampled each day. During a block, a scan sample wasrecorded once an hour for each individual in camp. Variables recorded during a scansample included the individual, his or her activity, the object of the activity (a person,in the case of childcare), location, date, and time.

A focal follow documents a continuous sequence of one individual’s activities.Variables coded on a focal follow include the sequence of activities performed by anindividual, the start and stop times of those activities, and the weight of anyresources collected between the start and stop time. Focal follows are used tocalculate return rates and bout durations of in-camp activities.

Several ethnographic methods were used to verify ages (Hill and Hurtado 1996;Howell 2000). All household members old enough to respond were interviewed andasked to list their siblings and children in ranked birth order. Asking multiple relativesabout kin relations and birth orders provides a check for conflicting information andidentifies cases needing further clarification. Interviews were conducted in the Pumélanguage, reducing the possibility of translation and interpretative mistakes. Parentscan accurately report the ages of infants in moon counts (months), and young childrenup to 4 years in season counts (6-month units). Several methods are used to ascertainages of older children. The Pumé use specific kin terms to reference older and youngersiblings. These terms are used to corroborate relative ages within sib groups.Additionally, because parallel cousins are identified by these sibling terms, relativeages also can be linked across nuclear families. Importantly, detailed censuses werecollected in the study communities several times throughout the 1980s and 1990s andare invaluable to anchor the ages of most individuals currently in their adolescence andearly reproductive careers (Kramer 2008; Kramer and Greaves 2007). Many children’sbirth dates were recorded during Greaves’s fieldwork.

Data Analysis

To calculate the proportion of daily time spent in various activities, the number ofobservations for an activity (or suite of activities) is divided by the total number ofobservations for an age group. To calculate time spent in an activity, proportions maybe multiplied by an 11.5-hr or 690-min observation day. A return rate is expressed bythe amount an individual produces divided by the amount of time spent performing theactivity. Time includes travel from camp, collection of the food resource, and return tocamp. The weight of resources excludes tare weight of the basket, gourd, or othercontainer. The adult mean is set as a baseline to compare the subsistence effort of girlsrelative to their body size. The same data collection and analytic methods were usedfor the comparative Maya data and are fully described in Kramer 2005a.

Physical activity levels (PAL) are calculated from time-allocation data forPumé and Maya juvenile girls using the factorial method. PAL is a multiple ofbasal metabolic rate and is used to compare activity levels and energyexpenditure cross-culturally (Dufour and Piperata 2008; Jenike 2001; Leonardand Roberson 1992). Each Pumé and Maya scan observation is assigned an activitylevel based on standard categories of task-specific energetic cost. The scale of

312 Hum Nat (2011) 22:303–326

energy cost (kcal/min) is taken from experimental studies that measure energeticcost using respiratory exchange while a subject performs a specific task. Thesecalculations have been made for a variety of domestic, agricultural, andrecreational activities in both traditional and postindustrial societies (Durnin andPassmore 1967:47; Montgomery and Johnson 1977:100–102; National Academyof Sciences 1989:27; Ulijaszek 1995:35–39). Activity levels range from 1.0(resting, sleeping) to 5.0 (chopping firewood, transporting heavy loads). Activitylevels for each scan observation are summarized in an average value for each girl.To this observed individual activity level is added 8 hrs of sleep at an activity levelof 1.0 and the remaining unobserved hours at an activity level of 1.5. To calculate adaily 24-hr PAL, these values are summed, weighted by their proportionalduration in a 24-hr day. For example, PAL = observed activity level (0.479)+1.0(0.333)+1.5 (0.281). Although there are more precise ways to measure overalldaily energy expenditure, the factorial method used to calculate PAL is idealbecause we are interested in task-specific time allocations and comparative profilesof physical activity. All computations and descriptive and statistical analyses wereperformed in SAS version 9.1.3 (2002–2003 SAS Institute, Inc., Cary, NC).

Results

Pumé Juvenile Subsistence Effort and Body Size

Figure 2 shows the time that Pumé females allocate to subsistence effort. Thisincludes time spent in food acquisition (gathering, fishing, collecting roots, hunting)and domestic work (food processing, preparation, cooking, raw material processing,tool manufacture, hauling water, chopping firewood, washing, cleaning, building afire, sewing, weaving, etc.). The time females allocate to subsistence is alsoexpressed as a proportion of the adult mean. Adult women 15 years of age or older(n=20) spend on average 45.4% of daylight hours in work. Results show that younggirls ages 3–6 spend no time out of camp acquiring food but spend about 5% of

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3-6 7-10 11-14 Reproductive Postreproductive

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Fig. 2 Proportion of daily time (mean ± SD) Pumé females ages 3–68 allocate to subsistence work (n=38females, 6,616 scan observations). The line shows subsistence work as the proportion of the adult mean(women at least 15 years of age). Reproductive is defined as women ages 15–44, and postreproductive aswomen ages 45 and older

Hum Nat (2011) 22:303–326 313313

daylight hours (34.5 min) on average in domestic activities, which represents 12.5%of the adult mean. Girls ages 7–10 allocate on average 2% of daylight hours(13.8 min) per day to foraging activities and 12% of daylight hours (82.8 min) todomestic work. Their total subsistence effort represents 31% of the adult mean. Timeallocated to subsistence sharply increases in adolescence and plateaus in earlyadulthood.

Compared with older females, Pumé girls spend little time in subsistence tasksand are much less efficient. Wild roots constitute about 35% of the total Pumé diet,approximately 50% of the wet-season diet and are procured almost exclusively byfemales. Return rates (kg/h) are plotted by age group and expressed as a proportionof the adult mean (Fig. 3). Mean adult return rates (for women ages 20–45) are1.395 kg/h for small roots (n=31 foraging trips) and 2.69 kg/h for large roots (n=36 foraging trips). Too few girls under the age of 10 participate in root collection toconsider them separately, and girls ages 3–14 are lumped as one age group. Girls3–14 years of age are on average 29% and 30% as efficient as adult womencollecting small and large roots, respectively. In the same amount of time, juvenilesbring back a third the amount of roots compared with older adults. Girls areslightly more efficient in fruit collection. Wild mangos, not shown on this graph,constitute about 30% of the Pumé diet and are an important dry-season food. Girlsare 47% as efficient as adults (n=149 foraging trips), bringing approximately halfthe amount of food back to camp as adults for the same amount of time spentforaging and traveling.

To put juvenile subsistence effort into context, age-specific Pumé body size, time-allocation, and return rates are plotted as proportions of adult means (Fig. 4). Meanadult height for Pumé women is 151.5 cm. The mean adult time allocated tosubsistence is 338 min in an 11.5-hr observation day. Return rate proportions areshown for large roots, which have an adult mean of 2.69 kg/h. Individual body size,time-allocation, and return rate values are smoothed using a LOWESSprocedure. A low-resolution interpolation value (0.3) is used to retain individualvariation and avoid over-fitting the data. The graph illustrates that neither thetime girls allocate to subsistence nor their return rates are proportional to bodysize. At the end of juvenility, a 10-year-old girl is 88% of adult body size but

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

3-14 Reproductive Postreproductive

)rh/

gk(

eta

Rnr

ute

R

0.0

0.5

1.0

1.5

2.0 na

eM

tlu

dA

noit r

op

orP

Small Roots Large Roots

Fig. 3 Foraging return rates (mean ± SD) for Pumé females ages 3–68 (n=125 large root and 75 smallroot foraging trips). The lines show return rates in each age interval as the proportion of the adult mean(women ages 20–45, triangles = large roots, circles = small roots). Reproductive is defined as women ages15–44, and postreproductive as women ages 45 and older

314 Hum Nat (2011) 22:303–326

spends only 40% of the adult mean time in subsistence tasks and produces 25%the amount of roots per unit time as an adult. This relationship among age,body size, and foraging effort is not unexpected and has been noted for otherforagers (Bock 2005; Hawkes et al. 1997; Hurtado et al. 1992). Although food andespecially labor transfers are very difficult to quantify in societies in which foodsharing and labor cooperation are widespread, this graph suggests that girls fallwell below matching their own metabolic requirements and that others’overproduction subsidizes their energetic needs.

Cross-Cultural Differences in Subsistence Effort

Compared with juveniles growing up in other subsistence societies, Pumé girls spendrelatively little time in economic activities. Figure 5 transforms the time-allocation datain Table 1 into z-scores, which measure deviation from the mean relative to standarddeviation. Juveniles in this cross-cultural sample allocate a mean of 4.18 h tosubsistence effort (SD = 2.54; n=16 groups). These summary-level data suggest thatPumé girls invest in subsistence effort at the lower end of the range of variation.

To control for study differences, the work effort of Pumé girls is compared withMaya girls for whom we also have individual time-allocation data. The Maya aresubsistence agriculturalists. At the time of this study, girls rarely attended school andwere important contributors to household labor (Kramer 2002, 2004, 2005a).Although the Maya make their living in a different way than the Pumé, they serve asan ideal comparative baseline because Maya girls participate in subsistence anddomestic labor at an average level (with an SD of <0.01 for this cross-culturalsample), and because the same field and analytic methods were used to collect andanalyze the Pumé and Maya data.

In each age group, Pumé girls spend significantly less time in subsistence work thanMaya girls (Fig. 6). When the outcome variable time allocated to subsistence work ismodeled as a function of age and a dummy variable for Pumé/Maya, Pumé girls work

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

0 10 20 30 40 50

Age

Pro

port

ion

Adu

ltM

ean

Time allocation

Body size

Retun rates

Fig. 4 Proportion of Pumé adult body size, time allocated to subsistence effort, and large root return ratesfor Pumé females ages 0–50. Data points shown for individual time allocation values

Hum Nat (2011) 22:303–326 315315

significantly less than Maya girls of the same age (r2=0.8791, p<0.0001, n=44females 3–19).3 Maya girls ages 7–10 spend 23.5% of daylight hours insubsistence activities; Pumé girls, 14.2%, which represents about 42% less time.

Time-allocation data are then transformed into an estimate of physical activity level(PAL). PAL estimates the additional energy an individual expends each day aboveresting basal metabolic rate (BMR) as a multiple of BMR. This measure of the metaboliccost of physical activity is used to examine differences between Pumé and Maya girls,and it takes advantage of the detailed time-allocation data available for both groups.

When the proportional distributions of the time that Maya girls (2,283 scanobservations) and Pumé girls (650 scan observations) ages 3–10 spend at differentactivity levels are compared (Fig. 7), Pumé and Maya girls spend similar amounts oftime in light tasks (p=0.5337). However, Pumé girls spend significantly less time incalorically expensive activities (p=0.0037) and significantly more time in inactivityand tasks with low levels of energy expenditure (p=0.0016). Pumé girls also spendsignificantly less time in play (p=0.0001). Compared with Pumé girls, Maya girlsboth work harder and play harder.

A Pumé girl age 3–10 has an average observed activity level of 1.561, whereas aMaya girl has a value of 1.9544 (Table 3). This significant difference (p<0.0001)represents a 20% savings in energy expenditure during daylight hours. PAL estimates(24-hr energy expenditure) are also significantly lower for Pumé girls. The dailyenergy expenditure of an average Maya girl age 3–10 is 1,352 kcal. Adjusting for thedifference in total daily (24-hr) PAL, Pumé girls save approximately 162 kcal/day.

3 Accounting for age, the dummy variable is significant when added to the model (p<0.0001). Because ofthe strong age effect the data have a linear distribution, residuals are normally distributed, and noheteroskedasticity is evident. The model is powered at 99.9% at an alpha level of 0.05 and an n of 44. Themodel is sufficiently powered to detect the effect of group (Pumé/Maya) on work effort. There is a 0.1%chance of incorrectly accepting group affiliation as a significant predictor when added to the model.

Fig. 5 Cross-cultural variation in children’s subsistence work (values listed in Table 2 expressed as z-scores)

316 Hum Nat (2011) 22:303–326

This savings is sufficient, for example, to meet the added caloric demands ofjuvenile growth (Spear 2002).

In sum, Pumé girls allocate little time to subsistence, about half the time theirbrothers do, and far less than is proportional to their body size. Pumé girls also workless than children in many other preindustrial societies, and significantly less thanMaya girls, who represent a cross-cultural average in terms of the time they allocateto subsistence. If Pumé girls were not subsidized as much as they are, they wouldhave to substantially increase their activity levels and calories expended insubsistence effort. All else being equal, low activity levels leave more energyavailable for growth or maintenance and may help explain where the extra energycomes from for rapid Pumé juvenile growth.

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

3-6 7-10 11-14

Pro

port

ion

ofT

otal

Tim

e

p=.0486

p=.0098

p=.0131

Fig. 6 Mean proportion and standard deviation for the time Pumé girls (n=13; striped bars) and Mayagirls (n=21; solid bars) allocate to subsistence work. Subsistence work includes resource acquisition anddomestic work, and, in the case of the Maya, agricultural work. P values are given for the differencebetween Pumé and Maya girls within each age group

0.0 0.2 0.4 0.6 0.8 1.0

1.0

1.9

2.5

5.0

PA

L

Proportion Time

p=.0016

p=.5337

p=<.0001

p=.0037

Fig. 7 Proportion of time Pumé (striped bars) and Maya (solid bars) girls ages 3–10 spend in variousphysical activity levels during daylight hours. Task-specific activity levels: Resting and very light activities(1.0–1.5)=resting, sleeping, inactivity, childcare, sewing, personal maintenance, eating, drinking, socializing,religious activities. Play (1.9)=active play. Light activities (2.5)=domestic work, food processing, resourceacquisition, foraging, hunting, fishing, traveling, tending animals, construction, general productive work.Moderate activities (5.0)=chopping firewood, transporting heavy loads, field work, collecting water, sports

Hum Nat (2011) 22:303–326 317317

Discussion

Fast growth has conventionally been considered an indicator of good or improvednutritional conditions and/or immunological conditions (Bogin and Rios 2003;Bogin et al. 1992; Orr et al. 2001; Sellen 1999). However, recent evidence suggeststhat suboptimal childhoods also are associated with fast maturation (Cooper et al.1996; Kramer and Greaves 2010; Walker et al. 2006b). Although early maturity istheoretically and empirically correlated with high mortality, the biological mecha-nisms that advance maturity are unclear. Why and how suboptimal environmentalconditions have accelerating effects on the pace of growth poses new questionsabout energy allocations. One means available to juveniles growing up in harshenvironments is to lower their activity levels.

Energy available for growth can vary through two main pathways: energy input fromeither self-provisioning efforts or calorie transfers from others, and energy expenditure.Although life history models typically do not specify energy expended in activity, it isimportant to delineate in humans since activity levels vary independently of body sizeand are an important source of cross-cultural energy expenditure variation (Dufour andPiperata 2008; Jenike 2001; Leonard and Roberson 1996; Sackett 1996).

Although immune function and maintenance expenditures play important roles inlife history allocations, little is known about the priority interests of intrinsic energyallocations, especially under conditions of energy limitation. However, anydownward adjustment in activity levels should leave more energy available forgrowth and maintenance. The comparatively low levels of subsistence effort relativeto body size suggest that Pumé girls support higher than expected juvenile growthrates in part through decreased activity levels. Lower levels of subsistence effort maybe especially important in environments that are food-limited and where littleleverage is available to adjust energy balance through caloric supplementation.

A trade-off structure predicts negative correlations among alternate expenditures. Ifthe energy available for maintenance and growth is finite, an increase in one expenditureprecipitates a decrease in another. However at the population level, because conditionsare often heterogenous across individuals, alternate energy allocations (for example, togrowth or maintenance) may appear positively correlated. This problem of phenotypiccorrelation can obfuscate empirical demonstrations of life history (Hill and Hurtado1996; Smith and Fretwell 1974) and energetic (McDade 2003) trade-offs. Within-population phenotypic differences are usually less pronounced in more impoverished

Table 3 Physical activity levels for an average Pumé (650 scan observations) and Maya (2,283observations) girl age 3–10. Standard deviations given in parentheses

Daylight hoursa 24-hr PAL

Pumé 1.561 (0.1487) 1.359 (0.0712)

Maya 1.944 (0.1153) 1.537 (0.0528)

a Average physical activity level taken from time allocation observations during daylight hours (11.5 hrsfor the Pumé, 11 hrs for the Maya). The 24-hr PAL adds to this observed individual activity level 8 hrs ofsleep at an activity level of 1.0 and the remaining unobserved hours at an activity level of 1.5. Thesevalues are summed, weighted by their proportional duration in a 24-hr day

318 Hum Nat (2011) 22:303–326

environments. This appears to be the case with the Pumé, as it is for other preindustrialpopulations where options to adjust calorie inputs are fairly equally constrained acrossjuveniles. Metabolic trade-offs may also be difficult to identify unless differences inphysical activity levels are taken into account.

In addition to explaining the low levels of subsistence activity, Pumé diets mayalso explain why girls do not experience negative growth effects despite growing upin less than optimal conditions. Although Pumé diets are marginal for 6 months ofthe year, food is sufficient and especially high in protein during the six-month dryseason, when children and adults put on weight. Even when their diet is calorie-restricted, it includes a variety of macronutrients. Although the relationship betweennutrition and growth has been under-studied in foragers, this factor is expected to bean important influence on growth trajectories. High-carbohydrate, low-protein dietsappear to have more profound effects on growth delays and faltering than do thenutrient-diverse, but low-calorie, diets typical of foragers. For example, nutritionalstudies find that iodine and iron deficiencies are associated with delayed growth andcompromised stature (Brabin and Brabin 1992; Ryan 1997). These key nutrients arefound in fish and meat, which represent about 25% of the Pumé diet but are oftenlimited in carbohydrate-rich and agricultural diets. Such protein-rich foods may beespecially important to growth during childhood and juvenility (Bogin 1999).

Relatively little is known about the annual staging of growth in children andwhether growth rates normally fluctuate over the course of a year seasonally stressedpopulations. Recent study among the Tsimane from lowland Bolivia found thatamong children who become ill, immune activation is followed by reduced gains inheight over the subsequent three-month period (McDade et al. 2008). This raisesseveral questions for future research. Do children who mature in seasonally food-depressed environments have growth rates that are elevated during seasons of plentybut adjust to lower levels when food is less available? Does seasonal caloricinadequacy have different effects on growth compared with chronic nutritionalinadequacy? With regard to how humans may adjust to common periodic shortfallsin food or crucial nutrients, the Pumé data suggest that growth may occur in a step-wise pattern (Lampl et al. 1992), which may help explain why Pumé girls rarelyexperience stunting and reach adult stature comparable to that of their SouthAmerican neighbors (Kramer and Greaves 2007).

We have focused on girls’ activity levels because Pumé girls grow rapidly duringjuvenility and reproduce at an early age despite food constraints and growing up inan epidemiologically stressful environment. Low activity levels are an importantmeans by which girls can manipulate their energy budget. This does not mean thatgirls in all populations with low activity levels will grow rapidly as juveniles. Forexample, !Kung children expend little effort in subsistence but do not invest in earlygrowth. Nor are they early reproducers.4 Although there is a fitness advantage forPumé girls to initiate reproduction at a young age (Kramer 2008), this may not bethe case for !Kung girls, who may be balancing other energetic, social, and

4 !Kung females are similar in adult stature to the Pumé (150 cm for the !Kung, compared with 151.5 cmfor the Pumé) but smaller in body mass (41 kg, compared with 50.5 kg; Jenike 2001:223).

Hum Nat (2011) 22:303–326 319319

biological demands that affect the pace of growth. Many factors affect growth, andcontinued hormonal and genetic research will uncover a more precise understandingof biological mechanisms and how they respond to extrinsic influences (Thomis andTowne 2006). Our purpose here was to account for juvenile activity levels, whichvary substantially across subsistence societies.

Food transfers are the other means to raise overall energy availability. Our analysesfocused on activity for several reasons. Although quantifying offspring provisioning isproblematic in societies that extensively share food and eat from a common pot,children’s activity budgets are amenable to field measurement. These data exist forseveral populations, which lend themselves to ethnographic comparison. Because foodsubsidies decrease investment in subsistence effort, activity levels account for some ofeffects of food transfers. But importantly, they also account for the energetic effects oflabor transfers. Improved understanding of interactions between energy allocations andexpenditures, especially in traditional societies, will further appreciation of variation inhuman responses to different environments.

Conclusion

Energy expended in activity is potentially a substantial proportion of an individual’sdaily energy budget, and any downward adjustment during growth should have apositive effect on metabolic balance. Pumé juvenile girls no doubt have the skills andstrength to work harder, increase their activity level, supply more of their own energyrequirements, and contribute more to the pooled effort. The opportunity cost to doing soincludes the forgone energy that could be allocated to growth, immunological defense,and other somatic maintenance. The emphasis here has been on the role that subsidizedsubsistence has on minimizing energy allocated to activity. The low productivity ofPumé girls liberates more energy to support maintenance and growth than if they metmore of their resource needs through their own effort.

Acknowledgments Foremost we thank the people of Doro Aná, Yagurí, and Charakotó for their tirelesshours of interviews and measurements. We are grateful to Drs. Roberto Lizarralde (Universidad Central deVenezuela), Ted Gragson (University of Georgia, Athens), and Haydée Seijas (Universidad Central deVenezuela) for their previous census research among the Pumé, which is invaluable in establishing thePumé age estimates. Much appreciation to Dr. Daisy Barreto (Universidad Central de Venezuela) andKleismer Correa (Salud Indígena) for assisting with Venezuelan research logistics. We thank Oskar Burgerand Amanda Veile for their assistance in the data collection. The 2005–2007 research was funded by theNational Science Foundation (0349963) and the Milton Foundation. The 1992–1993 Pumé research wasfunded by the L.S.B. Leakey Foundation and an NSF dissertation improvement grant awarded to RussellGreaves and Lewis R. Binford (DBS-9123875).

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Karen Kramer is an associate professor in the Department of Human Evolutionary Biology, HarvardUniversity. Her research interests include cooperative breeding, the evolution of juvenility, householdeconomics, comparative demography, and life history. Current field research includes projects with theMaya, a group of Yucatec subsistence agriculturalists, and the Pumé, a group of South American foragers.

Russell Greaves is a research associate at the Peabody Museum of Archaeology and Ethnology. Hisinterests include the behavioral ecology of living hunter-gatherer subsistence, technology, and socialorganization, as well as ethnoarchaeology.

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