Diurnal cortisol rhythms in Tsimaneв€™ Amazonian foragers

13 Pages·2011·0.4 MB·English

by  Colleen H. Nyberg

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P NEC-2000;No.ofPages13

Psychoneuroendocrinology(2011)xxx,xxx—xxx

available at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/psyneuen

Diurnal cortisol rhythms in Tsimane’ Amazonian

foragers: New insights into ecological HPA axis

research
Colleen H. Nyberg*

UniversityofMassachusettsBoston,DepartmentofAnthropology,100MorrisseyBoulevard,Boston,MA02125,USA

Received24October2010;receivedinrevisedform12May2011;accepted1June2011

KEYWORDS Summary Althoughagrowingbodyofresearchhasdocumentedimportantpathwaysbywhich

Cortisol; theHPAaxismediatestheinterfacebetweenthepsychosocialworldandindividualhealth,there

Stress; is a paucity of data from nonwestern populations, particularly from those populations with

HPAaxis; distinctnutritionalandinfectiousdiseaseecologies.Thespecificobjectivesofthisstudyare:(1)
Hom eostasis; todocum entvariat ioni ndiurnalco rtisolrh ythmsamo ngt heTsima ne’,arem ote pop ulatio nin the

Allostasis; BolivianAmazon,(2)toexplorethisvariationbyageandbygender,and(3)tocomparediurnal

Developmental plasticity; rhythmsfromthisstudytootherpopulationbasedstudiesofcortisolconductedinindustrialized
Marketintegrat ion; nations. Saliv ary cortiso l sampl es were co llected twice da ily, imm ediately u po n waking and
Life his torytheory; beforeb ed,forth reecons ecutived aysfro m303par ticipan ts(age 1.6—82year s,1564 sample s)in
Boliv ia conjun ction wit hthe Tsimane’Am azoni anPa nel Study(TAPS). Cort isolrhyt hmssh owed stronga ge

effectsacrossthedevelopmentalspan,withbasallevelsandslopesincreasingintoadulthood,

although individuals older than 60 years demonstrated a precipitous flattening of the diurnal

slope. Cortisol profiles were elevated in adult females compared to their age-matched male

counterparts, anddiurnal slopes,aswellasmean cortisol concentrationsamongthe Tsimane’

werethelowestreportedinanypopulationbasedstudyofHPAaxisfunction.Althoughthewithin-

populationvariationincortisolprofileswasconsistentwiththeestablishedcorrelatesoftimeof

day,age,andsex,thebetween-populationcomparisonsrevealeddramaticallylowerlevelsofHPA

activityamongtheTsimane’.Thisstudyprovidesabenchmarkagainstwhichtoreferencecortisol

levelsfromindustrializedpopulations,andexpandstherangeofdocumentedvariationinHPAaxis

functioninanonwesterncontext.
#2011 Els ev ierLtd.All rightsreserved.

1. Introduction

A formidable body of research has identified stress as an
* Correspondingauthor.Tel.:[phone];fax:[phone].
important pathway linkingthe psychosocial world to indivi-
E-mailaddresses:[email protected],
colleennyb erg2009@u .northwestern.edu. dualhealth andwel lbeing, and manystudies havef ocu sedon

0306-4530/$—seefrontmatter#2011ElsevierLtd.Allrightsreserved.

doi:10.1016/j.psyneuen.2011.06.002
Pleasecitethisarticleinpressas:Nyberg,C.H.,DiurnalcortisolrhythmsinTsimane’Amazonianforagers:NewinsightsintoecologicalHPA

axisresearch.Psychoneuroendocrinology(2011),doi:10.1016/j.psyneuen.2011.06.002
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P NEC-2000;No.ofPages13

2 C.H. Nyberg

cortisol to provide a biomarker of psychoneuroendocrine Its role in coordinating circadian metabolic functions

activity (Adam and Kumari, 2009; Miller et al., 2009). Ele- coupled with its capacity for reactivity place the HPA axis

vatedcortisollevelshavebeenassociatedwithaconstella- atthedynamicinterfacemediatinginternalhomeostasis,the

tionofrelatedhealthoutcomes,includinganincreasedrisk localecology,andthebroaderpsychosocialandsociocultural

ofcentraladiposity,diabetes,cardiovasculardisease,hyper- environment (Romero et al., 2009; McEwen and Wingfield,

tension,andthemetabolicsyndrome(Bjorntorpetal.,2000; 2003;Milleretal.,2009;Schulkin,2003).Byextension,the

Bjorntorp and Rosmond, 2000; Chrousos, 2000; Epel et al., HPA axis also serves as a key mechanism of developmental

2000;Rosmond,2005;Walleriusetal.,2003).Ahigherriskfor plasticity, modulating competing life history domains of

depression,reducedhippocampalvolume,andPTSDvulner- growth (Sloboda et al., 2009; Tsigos and Chrousos, 2002),

ability also signal the burden of chronic stress on mental maintenance (i.e. immune function) (Cohen et al., 2007;

health, with dysregulation of the HPA negative feedback Cole, 2008), and reproduction (Nepomnaschy et al., 2006;

circuitry playing a central role (Burke et al., 2005; Cohen Worthman and Kuzara, 2005) across a diverse array of taxa

etal.,2007;Leeetal.,2002;Milleretal.,2007;McEwenand (CrespiandDenver,2005;PowerandSchulkin,2006;Romero

Magarinos, 2001; Sapolsky, 2001; Yehuda and Bierer, 2008). andWikelski,2010).DifferentialtrajectoriesofHPAfunction

Ratherthanbeinguniformlyassociatedwithelevatedcorti- may,overtime,recalibratethresholdsfordiseaseriskacross

sol, however, chronic stress may also promote hypocortiso- thelifespan(Belskyetal.,2010;Chrousos,2000;Gluckman

lismoradrenalexhaustion(GunnarandVazquez,2001;Heim etal.,2010;Kajantieetal.,2002;KuzawaandQuinn,2009;

etal.,2000;Milleretal.,2007;Yehuda,2004).Inparticular, McEwen and Wingfield, 2003; Miller et al., 2002; Phillips,

stressorsassociatedwithtrauma,physicalthreat,andthose 2007). With the growing consensus that context matters

ofahighlyuncontrollablenaturetendtoelicitanelevated, (Boyce and Ellis, 2005), and that early life experiences can

flattenedcortisolprofile(Milleretal.,2007).Cortisollevels play a critical role in the developmental programming of

may also decrease over time since the onset of a stressor, physiologicalsystems(deRooijetal.,2006;Kajantieetal.,

further underscoring the complexities between stress and 2002; Gluckman et al., 2009; Kuzawa and Quinn, 2009;

patterns ofHPAactivity (Miller et al., 2007). McDade et al., 2010), it is especially important to utilize a

Despitetheseimportantadvancesinourunderstandingof comparativelenstoinvestigatevariationinHPAaxisfunction

stressphysiology,however,thevastmajorityofthesestudies within and between populations (Boyce and Ellis, 2005;

have been conducted among relatively affluent, well-nour- Chisholm and Coall, 2008; Ellis et al., 2005; Worthman and

ished,sedentaryindustrializedpopulations—conditionsthat Kuzara, 2005).

are far from ubiquitous for most inhabitants of the world Beyond the utility of conducting a study of HPA axis

(Adam, 2006; Evans and Kim, 2007; Cohen et al., 2006; dynamics in a nonwestern population, this is the first study

Jonetz-Mentzel and Wiedemann, 1993; Lupien et al., to document cortisol rhythms in an indigenous hunting and

2000). In contrast, there is a paucity of comparative data foraging society, the Tsimane’ of the Bolivian Amazon

onHPAaxisfunctionfromnonwesternpopulations,particu- (Huanca,2006;Nyberg,2009).Withadevelopmentalmilieu

larly from those whose developmental ecologies are char- characterized by high levels of physical activity, marginal

acterized by high burdens of infectious and parasitic nutritional status, and high burdens of infectious and para-

diseases, and marginal nutrition. Though recent studies in sitic diseases, this remote setting provides a unique ecolo-

Botswana (Decker, 2000), Dominica (Flinn and England, gical context in which to explore the dynamics of HPA axis

1997), Jamaica (Fernald and Grantham-McGregor, 1998), function. Aswithmanyhistorically marginalized indigenous

Kenya (Pike and Williams, 2006), Mexico (Fernald et al., populations of lowland South America, the Tsimane’ are

2009), Guatemala (Nepomnaschy et al., 2004) and Nepal undergoing rapid lifestyle changes (Byron, 2003; Godoy

(Fernald et al., 2003; Hruschka et al., 2005; Worthman et al., 2005; Godoy et al., 2006; Reyes-Garcia et al.,

andPanter-Brick,2008),havebeeninvaluabletoourunder- 2003): the past 25 years have witnessed the opening of a

standing of differential cortisol release in nonwestern set- newroadandamarkedincreaseinloggingactivities,provid-

tings, the paucity of data on the diurnal rhythm precludes ingtwoofthemostdirectwaysfortheTsimane’toenterthe

population levelcomparisons of HPAfunction. regional marketeconomy.AmongtheTsimane’wholivefar

Thehypothalamic—pituitary—adrenalaxis(HPA)servesas frommarketcentershuntingandforagingsubsistenceprac-

a central anchor of the stress response (Sterling and Eyer, tices are prevalent, and overall, Tsimane’ social structure

1988). Hierarchically organized, the response is elicited in remainshighlyautarkic,withsocialnetworksjoinedbylines

thebrainuponthecognitiveappraisalofastressor,withCRH of blood and marriage forming the prevailing conduits of

cascading from the paraventricular nucleus in the hypotha- social andeconomicexchange (Godoy et al., 2005).

lamus, which then stimulates production of ACTH from the Recent research has demonstrated elevated levels of

anterior pituitary (Hellhammer et al., 2009; Miller et al., infection (via the inflammatory protein CRP) (McDade

2007).OncethecirculatingACTHsignalreachestheadrenal et al., 2005), high parasite loads (Tanner et al., 2009), and

cortex,cortisolisreleasedintothebloodstream,withnega- high mortality rates among the Tsimane’ (Gurven et al.,

tivefeedbackoperatingprimarilyinthehippocampusviathe 2007). Growth stunting is prevalent (Godoy et al.,

highdensityofglucocorticoidreceptors(GRs),whichdampen 2010a,b; Foster et al., 2005) and adults are also relatively

cortisollevelspost-challenge(Anackeretal.,2010;Galeeva lean,exhibithighlevelsofphysicalactivity,andhavemark-

etal.,2010).Cortisolexhibitsastrongdiurnalpattern,with edly lower blood lipids and leptin levels compared to U.S.

levelsreachingazenithshortlyafterawakeninganddipping populations (Gurven et al., 2009; Sharrock et al., 2008;

toitsnadirbeforesleep(Dallmanetal.,1993;deKloetand Vasunilashorn et al., 2010). Previous TAPS studies have

Sarabdjitsingh, 2008; Kirschbaum andHellhammer,1994). revealed that greater participation in market activities is

associated with higher self-reports of anger and fear, and

Pleasecitethisarticleinpressas:Nyberg,C.H.,DiurnalcortisolrhythmsinTsimane’Amazonianforagers:NewinsightsintoecologicalHPA

axisresearch.Psychoneuroendocrinology(2011),doi:10.1016/j.psyneuen.2011.06.002
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Diurnalcortisol rhythms in Tsimane’ Amazonian foragers 3

havereportedanassociationbetweenlowerwealthrankand to fill the collection vials immediately upon waking, ‘‘as

poorer subjective health (Godoy et al., 2005; Reyes-Garcia soon as you open your eyes and before your feet hit the

etal.,2008;Undurragaetal.,2010).Notably,theTsimane’ ground’’,andimmediatelybeforebedor‘‘rightbeforeyou

do not have a direct indigenous translation for the word close your eyes’’ (Adam and Kumari, 2009; Cohen et al.,

‘‘stress’’, underscoring the utility of salivary cortisol to 2006). The nature of this collection protocol allowed for

provide an objective measure of HPA activity in this cross theadjustmentofthemorningwakingandbedtimevalues

cultural setting (Dressler,1991; Nyberg,2009). to each individual’s circadian rhythm (Adam and Gunnar,

This setting provides a compelling backdrop for the 2001). Due to logistical difficulties in this remote field

explorationofHPAaxisdynamics,andpermitsafirstglimpse setting (i.e. Tsimane’ do not have time keeping devices,

into how the ‘‘typical’’ cortisol values derived from indus- thus hindering adequately capturing the 30min cortisol

trialized populations compare to those from a small-scale response to awakening), and in an effort to maximize

horticulturalist,hunting,andforagingsocietyintheBolivian participantcompliance,thisstudydidnotcollectasample

Amazon(N=303individuals,1564samples,ages1.6—82.2). representingthecortisolawakeningresponse(Adam,2006;

The specific objectives of this study are: (1) to document Clow et al., 2004).

variationinthediurnalcortisolrhythmsamongTsimane’,(2) Growthparametersandnutritionalstatuswereassessed

to explore this variation by age and by gender, and (3) to using standard anthropometric techniques utilized in pre-

comparediurnalrhythmsfromtheTsimane’tootherpopula- viousTAPSstudies(Fosteretal.,2005;Godoyetal.,2005;

tion based studies of cortisol conducted in industrialized Leonard and Godoy, 2008; Tanner et al., 2009; Lohman

nations. et al., 1988). A portable stadiometer was used to

measure stature (cm), and weight (to the nearest

0.1kg) was measured with a Tanita scale. These variables
2. Methods
were used to calculated body mass index (BMI) as (kg)/

(heig ht (m ))2.
2.1. Data collection

Participantsforthisstudywereenrolledinconjunctionwith 2.2. Cortisol analysis

the Tsimane’ Amazonian Panel Study (TAPS), a longitudinal

study collecting data on health, quality of life, and market Afterthecollectionofsalivasampleswascompletedineach

integration among (cid:2)1985 individuals since 2002 (Godoy study community, the vials were stored in the TAPS refrig-

et al., 2009; Leonard and Godoy, 2008). Thorough descrip- erationunitinSanBorja,Boliviawithinsevendaysofinitial

tions of TAPS are located at http://www.tsimane.org/ collection. Once manually transported back to the United

index.html, and excellent ethnographic overviews of the States, the samples were stored at (cid:3)308C at the North-

Tsimane’ are provided by Reyes-Garcia et al. (2003, 2008) western University Laboratory forHuman Biology Research.

andHuanca (2006). Subsequently,thesampleswereplacedondryiceandexpress

The TAPS survey on demographics and socioeconomic shipped to the University of Trier, Germany. Samples were

factorswasadministeredineachoftheparticipatinghouse- assayed in duplicate using a competitive solid phase time-

holds during the first phase of research. An inventory of resolved fluorescence immunoassay with fluorometric end-

traditional and modern assets, along with income was point detection (DELFIA), and exhibited a mean inter-assay

compiled, and items were assigned current market values coefficient ofvariation of6.7%.

to assess total household wealth, used as a gross proxy of Salivarycortisolisrelativelyrobusttodegradation,even

socioeconomicstatusinthisstudy.Duringthesecondphase, intropicalconditions,foratleasttwoweekswithoutrefrig-

the collection of cortisol and anthropometric data was eration (Hellhammer et al., 2009). Due to the extreme

accompaniedbyabriefsurveyonhealth.Adummyvariable temperaturefluctuationsandcollectiontimebetweensam-

was constructed to representwhether the participant had ples,however,variableswereconstructedtoassesspotential

experiencedillnessintheweekleadinguptocollection,an sources of sample degradation. No significant correlations

importantpotentialconfounderofcortisollevels.Thecol- were detected between cortisol concentrations and (a) the

lectionofsalivarycortisolfollowedacross-sectional wave duration(indays)betweentimeofcollectionandstoragein

acrossvillagesaspartofthehealthunit,andthecollection theprojectrefrigeratorinSanBorja(r=0.008,n.s.),or(b)

of anthropometric measurements to assess growth and thedurationbetweencollectiontimeandassaycompletion

nutritional status was performed on the third collection atthe University ofTrier, Germany (r=0.009, n.s.).

day. CortisolvaluesfromtheCARDIAstudy(Cohenetal.,2006)

Intotal,datafrom303individuals(175subadultsunder were used to illustrate population level comparisons

theage of16, 128adults)from fiveTsimane’communities between diurnal slopes in Fig. 3 for several reasons: the

are presented in this study, and comprise a total of 1564 study comprises a large multi-city sample; both morning

salivasamples.Toemphasizetheassessmentoftheperson- waking and bedtime cortisol values were available; and

specific basal diurnal rhythm, rather than a day-specific becauseassayswerealsoperformedusingDELFIA.Thecom-

pattern, cortisol samples were collected twice a day over parativecortisolvaluespresentedinTable3wereobtained

three days for a maximum of 6 samples per person. The from published studies of salivary cortisol if they provided

passivedrooltechniquewasdemonstratedtoparticipants, data on waking, evening, all times mean, or slopes. Addi-

who were given straws to help expel saliva into labeled tional values were adapted from Jessop and Turner-Cobb

2mL polypropylene vials. In an effort to capture the (2008, p. 3). Cortisol concentrations from the Tsimane’

maximumdiurnalcortisoldecline,participantswereasked sampleandthecomparativestudiesarereportedinnmol/L.

Pleasecitethisarticleinpressas:Nyberg,C.H.,DiurnalcortisolrhythmsinTsimane’Amazonianforagers:NewinsightsintoecologicalHPA

axisresearch.Psychoneuroendocrinology(2011),doi:10.1016/j.psyneuen.2011.06.002
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P NEC-2000;No.ofPages13

4 C.H. Nyberg

Table1 Descriptivecharacteristicsofsampleandmeancortisolparametersbysubgroup.

Females<16yrs Males<16yrs Adultfemales Adultmales

(N=91) (N=84) (N=68) (N=60)

Samplesperperson 5.3 4.8 5.4 5.2

Height(cm) 121.5(19.7)* 119.2(22.3) 152.6(4.7) 162.9(5.1)**

Weight(kg) 27.2(11.4) 26.1(11.9) 57.5(8.5) 62.3(8.0)**
BMI(kg /m2) 17.5 (2.0) 17.3 (1.7) 24.7 (3.5) ** 23.2 (2.4)

Morbidity(%reportingsymptoms) 34.60% 37.50%* 40.20%** 28.40%

Genderdifferencesbetweenage-matchedsubadultsandadultsareindicatedbysignificance*P<0.05;**P<0.01.

2.3. Statistical analysis primaryTsimane’governingbody,alsograntedpermissionto
the proj ect.

StatisticalanalyseswereperformedinStataversion10(Stata

Corp.,CollegeStation,TX).CortisolandBMIwerelogtrans- 3. Results

formedtoimprovethenormalityofthedistributionsforthe

multilevelanalyses.Allmorningwakingvaluesrepresent+0h
3.1. Descriptive statistics
postwaking, and the bedtime values represent +16h, and

valuesreportedforthehierarchicalmodelsarecenteredat
Table 1 reports general anthropometric and health charac-
+8hpostwaking.Slopesvalueswereobtainedbyestimating

teristics of the sample. For the 303 participants, mean
abestfitlinethoughthemultiplemeasuresofmorningand

morningwakinglevelswere5.83nmol/L(SD3.33)andbed-
eveningcortisolusinghierarchicallinearregression,withthe
timelevelswere1.94nmol/L(SD1.94).Theall-timesmean
coefficient for time of collection representing the diurnal

was4.44nmol/L(SD4.11)andthediurnalrhythmexhibiteda
rhythm (Adam and Kumari, 2009; Hruschka et al., 2005).

slope of(cid:3)0.076 (SE0.002).
Finally,eightpregnantwomenwereexcludedfromanalyses
While the vast majority of cortisol values in this sample
due to their dramatically elevated cortisol profiles (Obel

werelow,1.6%ofthesampleshadvaluesatleast3standard
etal., 2005).

deviations greater than the population mean, similar to
Descriptivestatisticsareprovidedfortheentiresamplein
reports from the Whitehall II and Rotterdam Studies (Adam
Table 1, and bivariate analyses were employed to evaluate

and Kumari, 2009; Steptoe et al., 2008). At the other
between group differences in cortisol parameters. Specifi-

extreme,lessthan10%oftheindividualshadaslopeofzero
cally,two-tailedt-testswereutilizedtoevaluatesexdiffer-
orgreater,withamaximumslopeof+8.89.Incomparison,a
encesinmultipleHPAparameters(AM,PM,mean,decline)in

recentstudyreportedthat14%ofadolescentparticipantsina
sub adults (under age 16) and adults. Finally, a series of

study of racial differences in cortisol rhythms exhibited a
multilevelmodelswereusedtoassessvariationatthewithin-

positiveslopeacrosstheday,withamaximumprofileof+18.9
and between-person levels, as well to assess the impact of
(DeSantis et al., 2007).
covariatesonslopeandbasalmeasuresofcortisol.Theuseof

multilevel modeling to analyze cortisol data represents a
significant improvem en t over r elying o n cru de averag es 3.2. Age and sex as determinants of HPA axis
(Adam and Gunnar, 2001 ; Hrus chka et al., 2005; Williams, activ ity

2008),byaugmentingthestatisticalpowerofthesemodels

while simultaneously adjusting for within-day correlations Althoughbothsubadultandadultfemaleshadhighermorning

(RaudenbushandBryk,2002).Inaddition,thisanalyticstrat- wakingandlowereveningcortisolconcentrationscompared

egy relaxes traditional assumptions of independence toage-matchedmales,thesevaluesdidnotreachstatistical

requiredforregressionmodeling,andprovidesahightoler- significance. However, the diurnal slope was significantly

ance for missing data and for unequal collection periods steeper in subadult females compared to males (t=(cid:3)2.48,

(Singer and Willett, 2003), issues that plague naturalistic P<0.01).Adultmalesexhibitedeveningcortisollevelsthat

studies of human health and pose challenges to the TAPS were on average 0.83nmol/L lower than adult females

collection protocol in this remotefield setting. (t=2.23, P<0.05),andadultfemaleshadaflatterdiurnal

Initially, an unconditional model with no predictors was rhythm compared to males (t=2.9, P<0.05). In addition,

usedtopredicttheintercept(meanmiddaycortisol)andto thealltimesmeanwassignificantlyloweramongadultmen

partition variance into within-person and between levels. (t=2.37, P<0.05). Thus, the gender gap widens signifi-

ThewithinpersonvariableswereaddedatLevel1(covariates cantly into adulthood, with adult women showing higher

such as time of collection, day of collection); while the overall mean levels, elevated evening levels, and a flatter

individuallevelcovariateswereenteredatLevel2(between diurnal cortisol rhythm compared to adult males. These

person attributes such as age, gender, morbidity, etc.), distinctions in cortisol profilesare illustrated in Fig.1.

linkedby theTAPSsubject identification number. Age-related changes in morning and evening cortisol

Allprotocolemployedinthisstudywereapprovedbythe acrossthelifespanareillustratedinFig.2,whichalsoreveals

Institutional Review Board for human subjects research at moresubtledistinctionsinthedevelopmentaltrajectoriesof

Northwestern University. In addition, in accordance with cortisolreleasebetweenmalesandfemales.Whereasthefull

established TAPS protocol, the Gran Consejo Tsimane’, the multilevelanalysisdemonstratingtheimpactofageondiur-

Pleasecitethisarticleinpressas:Nyberg,C.H.,DiurnalcortisolrhythmsinTsimane’Amazonianforagers:NewinsightsintoecologicalHPA

axisresearch.Psychoneuroendocrinology(2011),doi:10.1016/j.psyneuen.2011.06.002
+Models
P NEC-2000;No.ofPages13

Diurnalcortisol rhythms in Tsimane’ Amazonian foragers 5

8 2). Before controlling for the time of day, an unconditional
7 Women mo delreve alsnearly 75% oft heto tal varia nc eincortisolis
mol/L 56 MGiernls wbeitthwien e nindpievrisd ounasls,( thw eithin tjeur scte po tveorf L1e7v%e lof1 ,t chhe i 2v=a3ri8a4n.c 6e,
ol n 4 Boys P=0.000 ; random eff ect of the in tercep t1/ interc ept 2,
Cortis 23 tcoh it 2h=e 2t0w.o6 ,l ePv e<l m0.o0 d0e1l),. thWe hceon e ftfiimc iee notff ocrotllheecteifofne cits oafdtdi mede
1 of col lect ion o n the slop e is (cid:3)0.0 76 (t-r atio (cid:3) 27 .81,
0 P= 0.000). Th e a dditi on of tim e of co llection covariate
AM (+0 hrs) PM (+16 hrs)
reducedthevarianceby0.63(from1.44intheunconditional

Time since waking model to 0.87 in the unconditional growth model), and

therefore accounts for about 44% of the within person var-

Figure1 Diurnalrhythmsvarybysubgroup. iancein diurnal cortisol profiles.

ThreemultilevelmodelsarepresentedinTable2.Model1

presentstheunconditionalmodel,withtimeanddayasthe

nalslopesispresentedinTable2andinterpretedinSection only time-varying Level 1 predictors, Model 2 includes the

3.3,heremeancortisolconcentrationswithstandarddevia- covariatesageandsex,andModel3presentsthefullsuiteof

tions and hierarchical regression-based slope coefficients between-person covariates with the interpretation of sig-

with standard errors are provided for the age groups, nificantfindings.Tofacilitatetheinterpretationofthefixed

adjusted for gender. The interpretation of the slope coeffi- effects,coefficients(butnottheintercept),aretransformed

cientislistedasapercentagedeclineperhour.Areasonable using the following formula: (B =[exp(B )](cid:3)1)
%change raw

estimateoftheearlychildhoodpatternofHPAaxisfunctionis (Adam,2006;Hauneretal.,2008).InModel1,thecoefficient

represented by 20 children between one and four years of fortimeofcollectionindicatesthatcortisoldeclinesatarate

age, who display low mean cortisol levels (3.8nmol/L, SD of 7% per hour from waking until bedtime. Beyond time of

3.1) and a relatively shallow diurnal rhythm (b=(cid:3)0.05, SE collection, collection day is the only other time-varying

0.01, (cid:3)4.8%/h). Moderate increases in mean cortisol predictor, which displays a significant effect on both the

(4.2nmol/L, SD 3.7) and slopes (b=(cid:3)0.08, SE 0.01, intercept and slope. These findings may be, in part, the

(cid:3)7.6%/h) occur from ages five though nine, followed by an result of a large number of individuals missing the morning

upwardshiftinbasalconcentrations(4.7nmol/L,SD4.0)and collection period on day 1, thus arbitrarily reducing the

diurnalrhythms(b=(cid:3)0.09,SE0.005,(cid:3)8.6%/h)betweenthe averageconcentrations,butitmayalsoindicatetheimpor-

agesof10and12.Comparedtotheearlyadolescentrisein tance of factors such as mood and sleep schedule in con-

HPA activity, basal levels (4.6nmol/L, SD 3.1) and slopes tributingtoday-to-dayvariationwithinperson(Adam,2006).

(b=(cid:3)0.07,SE0.001,(cid:3)6.7%/h)plateaufromage13untilage Model2revealsthe expectedassociation withage,aseach

30,followedbysteadyincreasesinaveragelevels,exhibiting additional year of age is associated with a 0.6% increase in

apeakinmeanconcentrations(5.3nmol/L,SD4.2nmol/L), cortisol—aneffectthatbecomesconsiderablewhenextra-

andaslightelevationinslopes(b=(cid:3)0.08,SE0.00,(cid:3)7.6%/h) polatedacrossthelifespan.Whilethecoefficientforsexdoes

betweenages50and59.From60to82years,however,basal not reach statistical significance in the full hierarchical

levels are somewhat reduced (4.7nmol/L, SD 3.4), with model (P=0.09) presented in Model 3, the relationship is

morningcortisoldecreasingandbedtimecortisolincreasing in the direction expected, with males exhibiting a 4%

markedly,resultinginaprecipitousflatteningofthediurnal decrease in cortisol compared tofemales. The reductionin

rhythm (b=(cid:3)0.03, SE 0.01, (cid:3)2.9%/h). themagnitudeofthe relationship between sexandcortisol

comparedtothesubgroupdifferencesreportedinthebivari-
3.3. Variance and multilevel models of diurnal ateanalys es may bearesu ltofthelat enteffect so fag ethat

HPA activity emergeinthemultilevelmodel,whicharealsodepictedin

Fig.2.Thepresenceofinfectioussymptomswithinoneweek

Next,multilevelmodelswereusedtoapportionvarianceto ofsalivacollectionwassignificantlyassociatedwithanele-
thew ithin-(Leve l1)and betw een-p ers oncompon ents(Lev el va ted co rtisol profi le, w hile the co ntrol variab les B MI and

9
8
7
ol/L 6 AM cort
m 5 PM cort
n
sol 4 AM cort
Corti 3 PM cort
2
1
0
5 15 25 35 45 55 65+

Age
Figure2 PatternsofHPAactivityacrossthelifespan.

Pleasecitethisarticleinpressas:Nyberg,C.H.,DiurnalcortisolrhythmsinTsimane’Amazonianforagers:NewinsightsintoecologicalHPA

axisresearch.Psychoneuroendocrinology(2011),doi:10.1016/j.psyneuen.2011.06.002
+Models
P NEC-2000;No.ofPages13

6 C.H. Nyberg

householdwealthwerenotassociatedwithdifferentialcor-
g ollection P-value 0.0000.000 Ttmiasubolllte irl ee2vl eeaalr seem .so iFgdinenilafis lcltayo,n tte,h seut inmv daaertiraesncocdreiif nfcegor m ethnpetoi ans leanltitresan jcienecc tlooufrd ieeu dssi niinng
kin fc cortisolrel easeeve nin theabsen ceofasuite oftime-vary ing
wa ko covariat es.Like lihoo dr atio testsbe tw e enth et hreemodels
Interpretation 4.13nmol/Lat+8hpost7.8%declineperhour(cid:3)8%increaseafterday1+0.6%peryearolder4%ifmale(cid:3)n.s+23%ifsickwithin1ween.s. 2riance(SD)Chi 14(0.40)672.9001(0.03)531.055(0.74) Mds7(3pth2ea.oio.m4vrd4wia.eea, em ln, PPd 2ca eo e<agtpi en me0ub,d r. pe ls0Msaret0owotx0vid)eo)e e.(endDln 3 cfi d(Motae mo lvldai papenneald crr se 1ioas 6n o(2-sunl2iengs. vcn3 eooi,fil nf Pcc d Hao<itnvPi at0oA r.ni 0 raaae0ltxd)1e ui)s s a)ca nt(niDdod n dbM eeoovtdfiw aeentl ehcnee2
P-value 0.0000.0000.0000.0010.0950.2600.0450.460 Va 0.0.0. pFirgo.fi 3le sp raensde ntths ea vcaolmuepsa roibsotani nbeedt wfreoemn tthhee TCsAimRaDnIAe ’s tduiudryn, aal
large US based study on SES, lifestyle factors, and cardio-
t-Ratio 26.4(cid:3)27.6(cid:3)3.493.450.74(cid:3)1.95(cid:3)2.210.75 P-value 0.0000.000 davarreascmgu arlaetirac t:he etrhatelht ham ne(Cathnor hec eeonr ts ietsato nla dvl a.ar,ld u2ed0se0 vf6ri)oa .tm iTo hnthese a cCbo oAmvRpeDaI trAhi sesotnuT dsiiys-

covariates. Model3 Coefficient(SE) 1.9(0.070)(cid:3)0.072(0.003)(cid:3)0.083(0.024)0.006(0.001)0.045(0.060)(cid:3)0.29(0.250)0.20(0.075)0.001(0.00) 2Chi 662.1531.0 cpmastonauamdrdTna opeiome a’tsf ehru.aeterdedFrtur hosptlert oo ro mpe tffuha ealceHacah PnitTlAi,isopt ianamafntsruae,adn n m Tcceaateo’libs.tomolene pr ea3fxorr hifopsimrobHoni Pvtso Ai adtb hefeseustt rnewv ceaeptpleoiueonpern u std lchfaioouetrilr ol nTemnsaci lumt belstaaldiosnpepelideen’
d
cortisolrhythmsan t-RatioP-value 15.180.000(cid:3)24.3800.000(cid:3)1.500.1353.490.0001.040.100(cid:3) Variance(SD) 0.15(0.40)0.001(0.03)0.68(0.09) tttaPtshhioaavom eiennsa rt lp.nsaeo tl grTweua-eh dgBeoeeysrmf ti -Nc(o mocAkneroMa,nlpr yt,i2atc n i0lPshsget0oMesu8lwed, d)l a,esycs lkv hawowieimpnlhldiegsitpcr shrlev,hee an so pali ovauomvfegree itre4lreaao 8a1ldrf gl0 T eamv6—sdma.ie1m0 lo5ua4nan.en y9nmgs)e7e, oaa w ’tnlnr h/amcsyeL sh (o h .WiTdllusAd/romiLarlmrte wtahcanhnonon m u wmpefago’riphnt pohah muaart lenhav addeena-
diurnal nt(SE) .020)0.003)0.030)0.002)0.07) e cNthoeelplreaeclfetoisroe en mloocowcreunrrirnt eghd a sanafmtheaprd l ethtsh eew ayew rbaeek eetninmic neog-l slreteacsntpedodan rsidemi,zm eaednd,d i awt hteeerlieyr
sformed Model2 Coefficie 1.88(0(cid:3)0.074((cid:3)0.058(0.007(0.075((cid:3) P-valu 0.0000.000 ucootphnoednru wcsttauekdd iineigns (rBWeop otorsrtwthiamn ngaa nsi (mDa neildca krPley ar ,nlot2ew0r 0- vB6a)rliucaekns,d a2rt0eh0 e8fr)Po. hmTil hispetpu odinnieelyss
n
nlogtra P-value 0.0000.000 2 .40.0 (4K.uzDawisac,u p sesris oonnal comm unicatio n Nove mbe r, 20 09).
ee hi 5729
w o C 65
bet Rati 4327.4 This study is the first to present developmental changes in
delsofassociations Model1 Coefficient(SE)t- 1.68(0.038)(cid:3)(cid:3)0.076(0.002)(cid:3)(cid:3) Variance(SD) 0.16(0.41)0.001(0.03)0.69(0.03) HttchAaihonulPctendnAahs t lolilsiotsynuertw ggxael he,ojn e swatbtwc newetcidrtotio w thrlhrieiefetn vtoiess-her npoaela-olsg pce pvioorsnuaoftpgll asuau Hsbtle PaslisiotAotshnic hooea ienne cvd ttlarcy iicerfvo ieociamtsroitnyprrpie oadaalnn,atrm hittsieaoehonmsn en goscsBoe f onot rtrhgelfiitime vvins aeideoaT ai lsnnosl ie mmfgp dsdrAaa oameldnfilyxer-,alsap e’azc.masoga nAnealidess.-,
mo the docume ntedran geofp op ulationv ariatio nindiur nalHPA
el (h) acti vity.
Table2Multilev Fixedeffect Intercept(+8h)TimesincewakingDayAgeSex(male=1)logBMIMorbidityHouseholdwealth Randomeffect Level2interceptTimeslopeLevel1 Hfihmr2e0onPas0oAdeAl5dei ann; frc guR(cahsGnohbiculm rsdt(neeerKinpnoeouaocnn,drer i2 tb eii0oenenl0kft cg 5aotsa) hmit.gelhi .senSte, u i afiapb2emclot0.lalp,ep0en uvl9 2tidla)fi 0a,itpe0st irtoid9aoein ;nnnip ncd Kuott ubioifsaode arnHirecedstPo alobAknsllea iesmst ifseswuacitxnlneeea dcnendrt c ntiiKfe ot ffio nwerea srmniceptidnhhanr be laceaavedp diuasurou imnluoitldnstr-,

Pleasecitethisarticleinpressas:Nyberg,C.H.,DiurnalcortisolrhythmsinTsimane’Amazonianforagers:NewinsightsintoecologicalHPA

axisresearch.Psychoneuroendocrinology(2011),doi:10.1016/j.psyneuen.2011.06.002
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Diurnalcortisol rhythms in Tsimane’ Amazonian foragers 7

25 smallbutgrowingbodyofresearchontheearlyontogenyof
CARDIA

HPAfunction(Galeevaetal.,2010;JessopandTurner-Cobb,
20 Women 2008 ; Lupien et al., 2 009 ; Rosn er, 19 90). Age-related
L Men
mol/ 15 Girls minacrleesasaensd infe cmoarlteissoal rferoamls opucobnesritsyt eunnttiwl imthidsdelvee raaglep irne vbioouths
ol n Boys report s (A dam, 20 06; Gunn ar and Qu eved o, 2007 ; Lupien
Cortis 10 eretfl ael.c,t 2 a0d0a9p)t,i vyee ts hiti fitss uinnctlheears et to- pwoh inatt seoxftebnats a tlheHsPeA c ahcatnivgietys
5
that track biological development, versus the cumulative

burdenofstress exposures experienced overdecades.
0
AM (+0 hrs) PM (+16 hrs) The precipitous flattening of the cortisol rhythm in indi-

vidualsoverage 60iscontrary topriorfindingsin US-based
Figure3 ComparisonsbetweenTsimane’andUSdiurnalcor- elderly popu latio ns (I ce et al. , 2 004; Ice, 2005 ), although
tisolrh yt hms. age-rel ateddeclines ino the rend ocrine horm onesh avebeen

reportedamongsomenonwesternpopulations(Ellison,2010;

Ellisonetal.,2002;Campbelletal.,2006).Itispossiblethat

females (Darnall and Suarez, 2009; Hardie et al., 2002; thisfindingisrelatedtosenescenceamongtheTsimane’,or

Kudielka and Kirschbaum, 2005; Netherton et al., 2004; alternatively,couldrepresentacohort-effectamongindivi-

Rosner, 1990; Shansky et al., 2004). As evident from dualswhodidnotexperiencethesuiteofrapidsociocultural

Fig. 2, however, there is considerable variation in diurnal and lifestyle changes that present potential stressors for

rhythmwithineachsexthroughoutadulthood,andthesmal- younger generations. Given the high mortality rate in this

ler sample sizes within age categories coupled with an population (Gurven et al., 2007), a third possibility is that

absence of additional lifestyle variables challenges simple selectioneffectscontributetotheobserved‘convergence’of

interpretations of thegender gap incortisol release. cortisolrhythmsinthisagegroup.Withoutadditionaldatato

Fromadevelopmentalperspective,theflatteneddiurnal clarifyitscauses,theflattenedslopemayattheveryleastbe

slopes in children under age four are consistent with the considered amarkerof agingin this population.

hypothesized‘hyporesponsiveperiod’ofHPAactivityoccur- Fromacomparativestandpoint,thelowcortisolrhythms

ringduringinfancyandlastingthroughearlychildhood(Gun- from the Tsimane’ represent a departure from those docu-

nar and Donzella, 2002; Lupien et al., 2009). Although mentedfromindustrializedpopulations,andraisetheques-

measurementerrororissueswithcompliancemaycontribute tion of whether these findings indicate pathology, or

to some of this variation, these findings could indicate the alternatively, represent naturally occurring variation in

delayedestablishmentofthenegativefeedbackrhythmuntil HPA function among a population with a distinct suite of

thehippocampusismorefullydeveloped,andaugmentthe sociocultural,developmental,andecologicalexposures.The

Table3 Comparativecortisolvaluesindiversepopulations.

Study Age N Wakeup Bedtime Slope Mean Reference

Tsimane’ 1.6—15.9 222 5.27 1.94 (cid:3)0.07 4.16 Nyberg(thisstudy)

Tsimane’ 16—82 81 6.39 2.22 (cid:3)0.08 5.00 Nyberg(thisstudy)

Botswana >17 64 n.a n.a. n.a. 5.00 Decker(2006)

Nepal 11.8 107 6.11 n.a n.a. n.a. WorthmanandPanter-Brick(2008)

Philippines 15—16 245 7.44 2.19 (cid:3)0.10 n.a. Kuzawa(unpublished)

Dominica 2—18 256 15.8 n.a n.a n.a. FlinnandEngland(1997)

Romania 8.55 18 22.2 n.a n.a n.a. GunnarandVazquez(2001)

Canada 7.9 27 18.9 n.a. n.a. n.a. GunnarandVazquez(2001)

Chicago 13—19 257 15.6 3.61 (cid:3)0.15 n.a. Adam(2006)

US 6—7 34 19.7 n.a. n.a. n.a. Bruceetal.(2002)

CARDIAUS 18—30 769 20.3 7.76 (cid:3)0.78 n.a. Cohenetal.(2006)

US 5—6 28 10.0 2.22 n.a. n.a. DeCaroandWorthman(2008)

ChicagoandLA 16—18 255 12.2 2.78 (cid:3)0.55 n.a. DeSantisetal.(2007)

US 10—12 262 8.06 n.a n.a. n.a. Hardieetal.(2002)

US 7—9 68boys 6.94—13.1 n.a. n.a. n.a. Jonesetal.(2006)

US 7—9 72girls 8.06—13.9 n.a. n.a. n.a. Jonesetal.(2006)

US 11—17 71 11.1 n.a. n.a. n.a. Klimes-Douganetal.(2001)

US 5—14 1152 13.6 n.a. n.a. n.a. Koupiletal.(2005)

US 6—10 217 13.9—25.0 n.a. n.a. n.a. Lupienetal.(2000)

US 11 178 8.06 n.a. n.a. n.a. Mossetal.(1999)

US 8—16 126 9.17 n.a. n.a. n.a. Nethertonetal.(2004)

US 10—12 1768 15.3 n.a. n.a. n.a. Rosmalenetal.(2005)

US 7—15 210boys 8.88 n.a. n.a. n.a. Tornhage(2002)

US 7—15 176girls 8.61 n.a. n.a. n.a. Tornhage(2002)

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8 C.H. Nyberg

vast majority of studies on hypocortisolism have revealed (Curleyet al.,2009; Fishet al.,2004; Meaney,2010; Ober-

associationswithextremeadversity,chronicstress,abuse, lander et al., 2008; Weaver et al., 2004). Thus, behaviors

majorpsychologicaltrauma,orPTSD(GunnarandVazquez, such as exclusive breastfeeding, co-sleeping, and intensive

2001;Heimetal.,2000;Milleretal.,2007;Yehuda,2004). alloparental care should be explored as salient factors in

Lessisknownabouttheeffectsofprolongedinflammatory establishingthesensitivityoftheHPAaxisofTsimane’infants

stimulation on HPA function in a high pathogen environ- andinbufferingtheeffectsofadversityduringdevelopment

ment,andwhetherthiscouldrepresentanotherpathwayto (Champagne et al., 2003; Chen et al., 2010; Gunnar and

chronic adrenal exhaustion. In this scenario, it might be Donzella,2002;Levine,2005;Lupienetal.,2009;Tronickand

expected that cortisol levels (average output and slope) Reck,2009).

would decrease with age to reflect the cumulative infec- Though initial efforts have been made in tracing the

tious burden and emergent HPA dysregulation across the nuancedroleofglucocorticoidsinregulatinginflammatory

lifespan. A second hypothesis generated from the adrenal pathways (Chrousos, 1995; Dantzer et al., 2008; Elenkov

exhaustionmodelwouldpredictaninabilityoftheHPAaxis etal.,2000;GlaserandKiecolt-Glaser,2005;Milleretal.,

to respond to acute episodes of infectious morbidity, with 2002; Nadeau and Rivest, 2003; Raison and Miller, 2003;

dysregulationofthesystemresultinginimpairmenttothe Rivest, 2003; Sorrells and Sapolsky, 2007; Vedhara et al.,

HPA reactive scope. The findings from this study indicate 2007),especiallywithregardtotheetiologyofdepression,

theoppositepatternsinbothregards:first,ageispositively the intersection of HPA activity and immune function in a

associatedwithbothcortisoloutputanddiurnalrhythmin highpathogenenvironmenthasyettobeconsidered(Bese-

this population, and second, since the age- and sex- dovsky and del Rey, 1996; Blalock, 1989; Cole, 2008). In

adjustedcortisollevelsamongindividualsnotexperiencing contrast to the relatively sterile environments in most

acute morbidity are significantly lower compared to those industrialized nations, Tsimane’ experience high rates of

reporting illness, the inhibitory capacity of the system infectiousandparasiticdiseasesacrossthelifespan(McDade

appears to remain intact. These findings are inconsistent etal.,2005;McDadeetal.,2008;Tanneretal.,2009).These

with HPA axis dysfunction, adrenal exhaustion, or func- developmentalexposuresmayinducephenotypicvariation

tional resistance at a receptor level (Miller et al., 2002; in the immune repertoire (McDade et al., 2010), and

Raison and Miller, 2003), but longitudinal data are neces- although speculative, may also shape HPA function, which

sarytofurtherclarifythecomplexandreciprocalrelation- plays an integral role in dampening the inflammatory

ships between HPA activity and immune function in this responseduringinfection.Futureinvestigationsshouldthus

setting. explicitlyevaluatewhetherlowerbasalcortisollevelsper-

A broad body of anthropological studies have reported mit up-regulation of immune function in response to fre-

associations between various measures of acculturation quent microbial exposures, a major threat to mortality in

and ‘westernization’ experience and elevated catechola- thispopulation.

mines, blood pressure, cortisol, as well as stress induced Finally,themetabolicactionsofcortisol arenumerous,

immunosuppression (Baker et al., 1986; Dressler, 1999; and range from the mobilization of energy reserves via

Graves and Graves, 1979; James et al., 1987; McDade, gluconeogenesisandlipolysis,totheintracellularmodula-

2002; McDade and Nyberg, 2010; McGarvey and Baker, tionofATPproduction(Brillonetal.,1995;Duetal.,2009;

1979; Nyberg, 2009). In the absence of refined data on Dallmanetal.,1993;Hershbergeretal.,2004).Therefore,

self-perceivedstress,however,inhasyettobedetermined an evolved sensitivity of the HPA axis to energy status

whether lower cortisol levels among the Tsimane’ are emerges as another hypothetical pathway linking diverse

reflectiveofalowerpsychosocialburden.Moreover,while environmental conditions to variation in cortisol rhythms.

lifestyle factors and stress exposures are possible contri- Important international research in human reproductive

butorstotheobserveddifferencesincortisolprofiles,they ecology has documented the metabolic sensitivity of the

likelydonotaccountentirelyforthefactthatlessthan2% hypothalamic—pituitary—gonadal (HPG) axis, and has illu-

of the Tsimane’ cortisol values resemble the values minated how endocrine architecture is largely shaped by

reported in the CARDIA study conducted in the United theenvironmentinwhichitdevelops,andmayevenconvey

States (Cohen et al., 2006). It would also be inaccurate signalsofecologicalinformationacrossgenerations(Ellison

to assert that Tsimane’ lives are stress-free, as many et al., 1993; Kuzawa, 2005; Kuzawa and Quinn, 2009). For

communities are grappling with the emergence of income instance, rural nonwestern populations experiencing mar-

inequality, exploitative debt relationships with river tra- ginalnutritionandhighlevelsofphysicalactivitythrough-

ders, and the encroachment of logging activities (Godoy out development consistently demonstrate lower levels of

etal.,2005;Nyberg,2009;Undurragaetal.,2010).Beyond reproductive steroids compared to urbanized, sedentary,

acursoryconsiderationofthepsychosocialcontributorsto industrialized populations (Ellison, 2003; Ellison and Pan-

differential cortisol profiles, conceptualizing how the HPA ter-Brick, 1996; Jasienska et al., 2006; Nu´n˜ez-de la Mora

axis navigates allostasis in diverse ecologies may yield et al., 2007; Vitzthum, 2009). A recent study measuring

deeper insight into the broad range of factors influencing leptin (Sharrock et al., 2008), an endocrine hormone

HPAaxisplasticity(Bateson,2001;Barker,2004;Gluckman released from adipocytes that signals energy status,

et al., 2009). Though not exhaustive, this approach would revealed that levels among the Tsimane’ are also the low-

benefit from inquiry into the relative roles of early social est on record, and thus provides compelling impetus for

exposures, infectious disease loads, and nutritional and future analyses. Similar inquiry may help to determine if

energetic status as logical points of entry. thelowcortisollevelsamongtheTsimane’areinfluenced,

Forinstance,earlysocialinteractionsmayhaveimportant in part, by homeostatic calibration of the HPA axis to

implicationsfortheepigeneticprogrammingoftheHPAaxis energy scarcity.

Pleasecitethisarticleinpressas:Nyberg,C.H.,DiurnalcortisolrhythmsinTsimane’Amazonianforagers:NewinsightsintoecologicalHPA

axisresearch.Psychoneuroendocrinology(2011),doi:10.1016/j.psyneuen.2011.06.002
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Diurnalcortisol rhythms in Tsimane’ Amazonian foragers 9

5. Conclusions Laboratory for Human Biology Research for their helpful
comments and profess ional ex pertise, an d R icardo Godoy

for providing logistical support for TAPS. Kathryn Hicks and
The paucity of time-varying covariates on perceived stress,

two anonymous reviewers provided comments that greatly
mood, affect, and sleep quality preclude the evaluation of
improvedthequalityofthismanuscript.Thisstudywouldnot
themoment-to-momentdifferencesincortisolinthisstudy.

havebeenpossiblewithoutthesupportoftheGranConsejo
Alsoabsentaredataonthemenstrualcycle,birthweight,or

Tsimane’, TAPS participants, Tomas Huanca, Susan Tanner,
otherpre-orpostnatalfactorsthatmaycontributetodiffer-
and especially Roman Durvano, who served as the Spanish-
ential patterns of cortisol release. The cross-sectional ana-

Tsimane’ translatorin the field.
lyses presented here provide important preliminary insight

into HPA axis dynamics among the Tsimane’, but additional

longitudinaldatawillfacilitateamorecomprehensiveunder- References

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Research was supported by a National Science Foundation
lisminhumans.Am.J.Physiol.268,E501—E513.
DDIG (BCS-0622576), an American Association of University
Bruce,J.,Davis,E.P.,Gunnar,M.R.,2002.Individualdifferencesin
Wom en Dissertation Fel lowship, a Northweste rn University chil dre n’scor tisolr esponse tothe beginn ingofane wschoolye ar.
Graduat e Research Grant, and a Northwestern University Psychoneu roendoc rinology 27 ,63 5—650.
Fellowshi p andaNo rthwes tern Un iversity FAN Gr ant. Burke,H.M.,Davis,M.C.,Otte ,C., Mohr,D.C.,2005.Depressionand

cortisolresponsestopsychologicalstress:ameta-analysis.Psy-

choneuroendocrinology30,846—856.
Conflict of interest
Byron, E., 2003. Market integration and health: the impact of

marketsandacculturationontheself-perceivedmorbidity,diet,

Nonedeclared. and nutritional status of the Tsimane’ Amerindians of lowland
Boli via,Univers ityofF lor ida. Unpublish edDoctoralT he sis.

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axisresearch.Psychoneuroendocrinology(2011),doi:10.1016/j.psyneuen.2011.06.002
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Pleasecitethisarticleinpressas:Nyberg,C.H.,DiurnalcortisolrhythmsinTsimane’Amazonianforagers:NewinsightsintoecologicalHPA

axisresearch.Psychoneuroendocrinology(2011),doi:10.1016/j.psyneuen.2011.06.002