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The University of Chicago
Temperature, Activity, and Lizard Life Histories
Author(s): Stephen C. Adolph and Warren P. Porter
Source: The American Naturalist, Vol. 142, No. 2 (Aug., 1993), pp. 273-295
Published by: The University of Chicago Press for The American Society of Naturalists
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The AmericanNaturalist
Vol. 142, No. 2
August 1993
TEMPERATURE, ACTIVITY, AND LIZARD LIFE HISTORIES
STEPHEN
C.
ADOLPH AND WARREN P. PORTER
Departmentof Zoology, Universityof Wisconsin-Madison, Madison, Wisconsin53706
SubmittedDecember 23, 1991; Revised June 8, 1992; Accepted July10, 1992
characteristicsvarywidelyamongspecies and populations.Most
Abstract.-Lizard life-history
patterns,which are usually
authorsseek adaptive or phylogeneticexplanationsforlife-history
presumedto reflectgeneticdifferences.However, lizard lifehistoriesare oftenphenotypically
factors.
plastic, varyingin response to temperature,food availability,and otherenvironmental
Despite the importanceof temperatureto lizard ecology and physiology,its effectson life
historieshave received relativelylittleattention.We presenta theoreticalmodel predictingthe
proximateconsequences of the thermalenvironmentfor lizard life histories.Temperature,by
affectingactivitytimes, can cause variationin annual survivalrate and fecundity,leading to a
thermal
negativecorrelationbetween survivalrate and fecundityamongpopulationsin different
environments.Thus, physiologicaland evolutionarymodels predictthe same qualitativepattern
data from
variationin lizards. We tested our model with published life-history
of life-history
fieldstudies of the lizard Sceloporus undulatus,using climate and geographicaldata to reconstructestimatedannual activityseasons. Amongpopulations,annual activitytimeswere negatively correlated with annual survival rate and positively correlated with annual fecundity.
variaProximateeffectsof temperaturemay confoundcomparativeanalyses oflizardlife-history
tion and should be included in futureevolutionarymodels.
characteristics
varywidelyamonglizardspeciesand populations
Life-history
(Tinkle1967,1969;Fitch1970;Ballinger1983;Stearns1984;Dunhamand Miles
mostauthorssoughtadaptiveexplanations
1985;Dunhamet al. 1988).Initially,
on thebasis ofpredictions
fromlife-history
theory
forlizardlife-history
patterns
(Tinkle1969;Tinkleet al. 1970;TinkleandBallinger1972;Stearns1977;Ballinger
1979;Tinkleand Dunham1986;Dunhamet al. 1988).A second,morerecent
underlievariationin life
approachexamineshow body size and/orphylogeny
histories(Ballinger1983;Stearns1984;Dunhamand Miles 1985;Dunhamet al.
assumethat
1988;Miles and Dunham1992).These approachesoftenimplicitly
variation
based. However,commongardenexperiments
is genetically
life-history
onlya fewtimeswithlizards(Tinkle
(Clausenet al. 1940)have been performed
1970;Ballinger1979;Fergusonand Brockman1980;Sinervoand Adolph1989;
Sinervo1990;Fergusonand Talent 1993).Therefore,
we knowlittleaboutthe
eitheramongorwithinspecies(Stearns1977;
geneticbasisoflizardlifehistories,
Ballinger1979,1983;Fergusonet al. 1980;Bradshaw1986;Sinervoand Adolph
by a number
in naturalpopulationsare affected
phenotypes
1989).Life-history
of environmental
factors(Bervenet al. 1979;Ballinger1983;Bervenand Gill
and moistureare knownto
foodavailability,
temperature,
1983).In particular,
exertproximate
on lizardlifehistories(Tinkle1972;Ballinger1977,
influences
Am. Nat. 1993. Vol. 142, pp. 273-295.
? 1993 by The Universityof Chicago. 0003-0147/93/4202-0005$02.00.
All rightsreserved.
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THE AMERICAN NATURALIST
274
|
Tpreferred
....
.............
(inactive)
-a--
active
-
P
.
.....................
.W...
(inactive)
TIME OF DAY
FIG. 1.-Idealized daily body temperature(Tb) profileof a diurnal,heliothermiclizard.
Value of Tb is typicallyhighand relativelyconstant(around Tpreferred)
duringactivitybecause
The Tb value of active lizardsoftenvariesrelativelylittleover thecourse
ofthermoregulation.
environments.However, the
of the activityseason and among populationslivingin different
and therefore
amountof timelizards can attainTpreferred
depends on the thermalenvironment
can vary substantiallyboth seasonally and geographically.In addition,Tb of inactivelizards
is likelyto vary seasonally and geographically.
1983;Dunham1978,1981;Abts1987;JonesandBallinger1987;Joneset al. 1987;
Sinervoand Adolph1989;Sinervo1990).
to lizard ecology and physiology
Despite the importanceof temperature
(Cowles and Bogert1944; Bartlettand Gates 1967;Norris1967;Avery1979;
havereceivedlittleformalattention
until
Huey 1982),itseffectson lifehistories
recently(Huey and Stevenson1979; Ballinger1983;Nagy 1983;Beuchatand
Ellner1987;Jonesand Ballinger1987;Joneset al. 1987;Dunhamet al. 1989;
Porter1989;Sinervoand Adolph1989;Sinervo1990;Grantand Dunham1990;
can
Grantand Porter1992).In thisarticlewe discussthewaysthattemperature
lizardlifehistories.We presenta generalmechanistic
modelforthe
influence
oftemperature
on fecundity
and survivalrate,based on lizard
proximate
effects
thermalphysiology.Specifically,
we addressthe question:Whatkindof lifethermalenvironments
historyvariationwould we expect to see among different
due simplyto proximate
effectsin theabsenceof geneticdifferentiation
among
feaOur modelpredictsthe same associationbetweenlife-history
populations?
turesthatis predicted
different
by evolutionary
theories,butbecauseofentirely
causes. We thenprovidea testof our modelusingpublisheddata frompopulationsof theeasternfencelizard,Sceloporusundulatus.Finally,we discussthe
limitations
ofourmodel,itsimplications
forlife-history
evolution,
anditsimplicawillrespondto climatechange.
tionsforhowpopulations
TEMPERATURE AND LIZARD LIFE HISTORIES: POSSIBLE MECHANISMS
on lizardlifehistories
oftemperature
is complicated
The effect
bythefactthat
Diurnallizardsoftenmaintaina relatively
high,
manylizardsthermoregulate.
constantbody temperature(Tb) duringdaytimeactivity(fig. 1) throughvarious
behavioraland physiologicalmechanisms(Cowles and Bogert 1944; Avery 1979,
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AND LIZARDLIFE HISTORIES
TEMPERATURE
275
1982;Huey 1982;Bradshaw1986).As a result,themeanTbofactivelizardsoften
littledespitedaily,seasonal,andgeographical
variesrelatively
variation
inthermal
environments
(Bogert1949;Avery1982).However,twoaspectsoflizardTbare
environments
and seasonallyin thesameenvironlikelyto varyamongdifferent
is largelydetermined
ment(fig.1). First,Tbduringinactivity
bysubstrate
andair
whichrestricts
temperatures,
thermoregulatory
options(butsee Cowlesand Bogert1944;Porteret al. 1973;Huey 1982;Huey et al. 1989).Second,and more
theamountoftimeperdaythata lizardcan be activeat itspreferred
important,
environment
and Gates 1967;Porteret
Tbis constrained
by thethermal
(Bartlett
et al. 1983;Porterand Tracy
al. 1973;Huey et al. 1977;Avery1979;Christian
1983;Grantand Dunham1988,1990;Sinervoand Adolph1989;Van Dammeet
timeof activityis one of theprimary
al. 1989).Indeed,modifying
mechanisms
by whichlizardsthermoregulate
(Huey et al. 1977;Grantand Dunham1988).
environments
Thus, althoughlizardsin two different
mightmaintainthe same
meanTbduringactivity,thecumulativeamountof timespentat highTbcould
Annualactivitytimeis thenroughly
differ
substantially.
equivalentto thetotal
amountoftimespentat highTbandcan be considereda measureofphysiological
timeforlizards.
Lizards are foundin a wide varietyof thermalenvironments,
hot
including
tropicallowlands,temperate
deserts,and cool, highlyseasonalhabitatsat high
in thermal
elevationor highlatitude(Pearsonand Bradford1976).Thisvariation
inactivity
variation
andconcomitant
season(Huey 1982),is likely
environments,
inlifehistories
tocause someoftheobservedvariation
amongspeciesandamong
widespreadpopulationsof singlespecies (Grantand Dunham1990).Here, we
can directlyinfluence
describesome of the ways thattemperature
life-history
characteristics.
Many of theseeffectsare mediatedthrough
activitytimesand
energybudgets.
ActivityTime and Energetics
Energyallocatedto reproduction
ultimately
dependson thedailyenergybudget,whichin turndependson activitytimein severalways.Energyacquisition
and by therate
bothby therateat whichresourcesare harvested
is determined
at whichtheyare processed(Congdon1989).Daily preycapturerate should
thatlizardsare foraging
increasewithdailyactivitytime,undertheassumption
whileactive(Avery1971,1978,1984;Averyet al. 1982;Karasovand Anderson
et al. 1986).In addition,highTbmayincreasepreycapture
1984;Waldschmidt
ratesand handling
efficiency
(Averyet al. 1982;Van Dammeet al. 1991).Daily
shouldincreasewithactivity
energyassimilation
time,becauseratesofdigestion
are temperature
at ornearactivity
andassimilation
andaremaximized
dependent
and Louw
Tb's(Avery1973,1984;Skoczylas1978;Harwood1979;Buffenstein
1982;Huey1982;Waldschmidt
etal. 1986,1987;Dunhametal. 1989;Zimmerman
andTracy1989;Van Dammeet al. 1991).On thedebitsideoftheenergybudget,
shouldalso increasewithactivitytime,bothbecause
dailyenergyexpenditure
resting
metabolicratesare higherat activityTb's(BennettandDawson 1976)and
because activelizardsoftenincuradditionalmetaboliccosts in pursuingprey,
and the like (Bennett1982;Karasov and Anderson1984;
defending
territories,
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276
THE AMERICANNATURALIST
Marlerand Moore 1989).The difference
betweenenergyassimilated
and energy
expendedrepresents
discretionary
energythatcan be allocatedto reproduction,
growth,
or storage(Porter1989).Thus,energyallocatedto reproduction
depends
on activity
timevia dailyandannualenergybudgets(Congdonetal. 1982;Anderson and Karasov 1988;Dunhamet al. 1989;Porter1989;Grantand Porter1992).
Potential
timeis likelyto be correlated
activity
withthesize oftheannualenergy
budgetand consequently
withthe amountof energythatcan be allocatedto
reproduction.
Growth,ActivityTime, and Age at Maturity
distorts
therelationship
betweenphysiological
In ectotherms,
and
temperature
time(Taylor1981;Sinervoand Doyle 1990).For example,lizards
chronological
seasonsspendmoretimeathighTbandtherefore
withlongeractivity
areexpected
at a youngerage (Pianka1970;
to growfasterand reachreproductive
maturity
are supported
Jamesand Shine1988).Thesepredictions
byfieldstudiesshowing
ratesoflizardsincreasewithannualactivity
time(Davis 1967;
thatannualgrowth
Tinkle1972;Ballinger1983;GrantandDunham1990)andbydirectobservations
underlongergrowingseasons (Tinkleand Ballinger1972;
of earliermaturation
Goldberg1974;Grantand Dunham1990).In addition,severallaboratory
studies
ofactivity
timeon growth
effects
havedemonstrated
rates.GrowthratesofjuvenileLacerta vivipara,Sceloporus occidentalis,and Sceloporus graciosus increase
withdailyactivitytime(i.e., access to highTb via radiantheat; Avery1984;
Sinervoand Adolph1989;Sinervo1990;B. Sinervoand S. C. Adolph,unpubis frequently
observedin animalsmaintained
lisheddata). Acceleratedmaturity
underoptimalthermalconditionsin thelaboratory
(e.g., A. Muth,unpublished
data,citedin Porterand Tracy1983;Fergusonand Talent1993).The observed
effects
oftemperature
and activity
timeon growth
fromtheenerfollowdirectly
outlinedabove.
geticconsiderations
ReproductiveCycles
Temperature
typicallyservesas a proximatecue forinitiating
reproductive
cycles in temperate-zone
lizards,eitherdirectlyor by entraining
endogenous
circannualrhythms
(Duvall et al. 1982;Marion1982;Licht 1984;Mooreet al.
1984; Underwood1992). Correspondingly,
populationsin warmenvironments
ofteninitiate
at an earlierdate(Fitch
oraltitudes)
(e.g.,lowlatitudes
reproduction
can often
1970;Goldberg1974;Duvall et al. 1982;Licht1984)and consequently
reproducemorethanonce per year,whereascool environments
usuallylimit
to one clutchor broodper year(McCoy and Hoddenbach1966;
reproduction
Tinkle1969;Goldberg1974;Parkerand Pianka 1975;Gregory1982;Ballinger
1983;Joneset al. 1987;Jamesand Shine1988).
ActivitySeason and SurvivalRate
orlatitudes
oftenhavehigher
at highaltitudes
annualsurvivalrates
Populations
at
to
those
low
altitudes/latitudes
compared
(Tinkle1969;Pianka 1970;Tinkle
andBallinger1972;Smithand Hall 1974;Turner1977;Ballinger1979;Jamesand
risk(notablyriskofpredation)
is higher
Shine1988).Thisimpliesthatmortality
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TEMPERATURE AND LIZARD LIFE HISTORIES
277
foractivelizardsthanforinactiveones (Rose 1981).Severalstudieswithin
populationssupportthisconclusion.Wilson(1991; B. Wilson,personalcommunication)foundthatdailymortality
ratesin Uta stansburianaare highestin spring,
intermediate
in summer,
and lowestduringthewinter;dailyactivity
timesfollow
thesamerankorder.Marlerand Moore(1988,1989)experimentally
manipulated
testosteronelevels in male Sceloporus jarrovi and found that individualswith
testosterone
implants
hadlongerdailyactivity
periodsandsuffered
higher
mortalityrelativeto controls.
Acute Effectsof Temperatureon SurvivalRates
All lizards have upper and lower criticalthermallimitsbeyond which the animals perish (Cowles and Bogert 1944; Dawson 1967; Spellerberg 1973). How
oftentheselimitsare approachedin natureis unknown.Deaths due to winter
coldhavebeenreported
(Tinkle1967;Vitt1974;reviewinGregory1982);deaths
are probablyless common(Dawson 1967).Acuteeffectsof
due to overheating
temperature
may also influencesurvivalrates indirectly,
throughthe thermal
andTracy1981;Huey 1982;
dependenceoflocomotion(Bennett1980;Christian
vanBerkum1986,1988).In somecases lizardsareactiveat Tb'sthatsignificantly
impairsprintspeed, which could lead to greaterriskof predation(Christianand
Tracy 1981;Huey 1982; Crowley1985;van Berkum1986;Van Dammeet al.
thatlead to lowersprintspeeds
1989,1990).However,the cool environments
theoveralleffect
mayalso reduceactivity
times,whichwouldtendto ameliorate
on annualsurvivalrates.Temperature
mayalso affectresistanceto disease. For
example, the abilityof desertiguanas (Dipsosaurus dorsalis) to survivebacterial
infectionimproveswithincreasingTb(Kluger 1979).
Energetics of Hibernation
Lizards can be inactive more than halfthe year, particularlyat highlatitudes
or highaltitudes(Gregory1982; Tsuji 1988a). Duringthistimetheyrelyon stored
energy,
particularly
lipids(Derickson1976;Gregory1982).Because temperature
conditions
affectmetabolicrates(Bennettand Dawson 1976;
duringhibernation
Tsuji 1988a,1988b),energystoresmustbe adequateforboththedurationand
theTb'sexperienced
duringhibernation.
Temperatureand EmbryonicDevelopment
affects
In lizards,temperature
and(insome
eggincubation
time,eggmortality,
species)sexualdifferentiation
(Bull 1980;Muth1980;PackardandPackard1988).
shorter
In warmerenvironments,
incubation
timesmaylengthen
theactivity
seathemto reacha largersize priorto
son experiencedby hatchlings,
permitting
hibernation.Laying several clutches of eggs in a single activityseason is more
incubation
times.The significance
oftemperafeasibleifaccompaniedby shorter
forlizardlifehistories
sex determination
is notwellunderstood.
ture-dependent
inducedcorrelation
One possibleeffectis an environmentally
betweenhatching
dateand sex, whichcouldlead to a correlation
betweenjuvenilesize and sex by
theend of theactivityseason. Because mostlizardsreachmaturity
within1-2
couldpersistintoadulthood.
yr,thissexualsize difference
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DAY OF ACTIVITYSEASON, j
a
24
.
-150
-50
-100
50
0
100
150
18
O 120
b
J
F
M
A
J
FMAMJ
J
F M
M
J
J
A
S O
N
D
24
a
24
~18
0
6_
0
JASMN
D
24
c
~18
0
0
A M
J J A SON
MONTH
D
FIG. 2.-Seasonal variationin potentialactivitytimeof diurnallizards, as determinedby
thethermalenvironmentand thermalphysiologyof thelizard. NorthernHemisphereseasons
are illustrated.Unshaded region indicates times when thermalconditionspermitactivity;
shaded region indicates periods of inactivity.Individuallizards may not be active as often
as the thermalenvironmentpermits(see, e.g., Nagy 1973; Porteret al. 1973; Simon and
Middendorf1976; Rose 1981; Beuchat 1989). a, Elliptical activityseason characteristicof
manydiurnaltemperate-zonelizards. b, Activitypatternoftenobserved in lizards livingin
desertsor otherseasonally hot environments,where highsummertemperaturescause midday inactivity(hence bimodal activity;Porteret al. 1973; Grant 1990; Grant and Dunham
1990). c, Rectangularactivityseason characteristicof some lowland tropicallizards (see,
e.g., Heatwole et al. 1969; Porterand James 1979).
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AND LIZARDLIFE HISTORIES
TEMPERATURE
279
Thus,temperature
potentially
affects
lizardlifehistories
through
variousmechanisms.However,thereis no generaltheoryincorporating
theseproximate
influences.A fewstudieshaveexaminedtheeffect
oftemperature
on lifehistories
of
individual
detailedphysiological
speciesthrough
modelstailoredtothelifehistory
of the species in question(Beuchatand Ellner 1987;Grantand Porter1992).
Here,we presenta generalmodeloftheeffect
oftemperature
on annualfecundity
and annualsurvivalrates.Othertraits,suchas age and size at maturity,
could
be modeledsimilarly.
A GENERAL
MODEL
Annual and Daily ActivityTime
For mostdiurnaltemperate-zone
lizards,potentialdailyactivitytimevaries
timesare typically
shortin thespringandfallandlong
seasonally.Daily activity
insummer,
becauseofseasonalchangesintemperature
(Porteret al. 1973;Porter
theannualactivity
andTracy1983}.Here, we approximate
patternas an ellipse
(fig.2a), wherethe lengthof the activityseason is 2y d and the lengthof the
maximumactivityday is 2d h. For an ellipticalactivityseason the potential
numberofhoursofactivity
perdayis givenby
h = 2d/ 1-_(j2/y2),
(1)
wherej represents
day of theyear;j = 0 at themiddleof theactivityseason,
whenh is maximal.The area of theellipseTryd
equals thecumulative
potential
hoursofactivity
peryear.
effectson potentialactivitytimeare reflected
Temperature
in thevaluesofy
and d. These valuesare affected
in air
primarily
by dailyand seasonalvariation
and solarradiation.Warmlow-latitude
temperature
environments
usuallypermit
inlargey,whereaslizardsat highlatitudes
formuchoftheyear,resulting
activity
or altitudescan have activityseasonsas shortas 4-5 mo (Tsuji 1988a).Factors
and cloud cover can also affectthesevalues; heavy
such as habitatstructure
wouldtendto decreased becauseoftheshadowscastinearlymorning
vegetation
Thermalphysiological
andlateafternoon.
characteristics
ofthelizardalso influencey andd. For example,somespeciesrequirerelatively
hightemperatures
for
theirpotentialactivitytime(reducingbothy and
whichwouldrestrict
activity,
thermal
allowslongeractivity
d). Conversely,
relaxing
requirements
periods(PorterandTracy1983;Grant1990).
fordifferent
Shapes otherthanellipsesmightbe moreappropriate
thermal
For example,desertlizardsoftenhavebimodaldailyactivity
environments.
patternsduringthesummer,to avoid hotmiddaytemperatures
(Porteret al. 1973;
Grant1990;Grantand Dunham1990;fig.2b). Lizardsin tropicallowlandsmay
be activeyear-round
duringdaylighthours(Heatwoleet al. 1969;Porterand
we willrestrict
James1979;Huey 1982;fig.2c). For simplicity,
ouranalysisto
elliptical
activity
seasons,butourmodelcan be extendedto anyseasonalactivity
pattern.
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THE AMERICAN NATURALIST
280
b
a
ma:
1.0
0.8:
1.0
0.0001
0.60
ir
0
0.8
0.4
0
activity
0.2'
cn
0.0003
0OU
0.3
0.6
0.6
e.(.uvartce0.0005s
saneg(uutehroatiyafr
_1
m
z
[lotte on
z 0.1030006
FIG.
1000
0.0
~~~~~~~~~~~~~~~~~~~~
0m00vm6
00i00o3aeSa
nulautsria
La,3.Mdlpeitosfrepce
0.05
0.4
2000
0.2
3000
10~00
2000
uciono
0.00009
3000
ANNUALACTIVITYTIME(HOURS)
ANNUALACTIVITYTIME(HOURS)
of
FIG. 3.-Model predictions
forexpectedannualadultsurvivalrateS as a function
seasonlength(cumulative
hoursof activity,
a), fromeq. (3). Survivalratecurves
activity
are plottedon a logarithmic
scale forseveraldifferent
values Of Ma and mi (thehourly
and inactivity,
valuesof
risksduringactivity
a, Effectofdifferent
mortality
respectively),
valuesofini, setting
ofdifferent
Ma equal to 0.0003.
in'al setting
miequal to 0; b, effect
SurvivalRates
We assumethateach individual
has constantprobabilities
ofmortalityMaper
oftimeofyearortime
andmiperhourofinactivity,
independent
hourofactivity
amongindividuofday.Undertheassumption
thatmortality
riskis independent
is givenby
als, expectedannualsurvivalrate(S) forthepopulation
S
= (1 - ma)a (1 - mi)i,
(2)
andinactivity
fortheyear,
wherea andi are thetotalnumberofhoursofactivity
Thisis closelyapproximated
by
respectively.
S = exp(-ama
- im )
(3)
risksless than0.01 perhour;typicalvaluesare less than
forper-hour
mortality
data). Because
0.002 (see below; S. C. Adolphand B. S. Wilson,unpublished
=
in
can
as
a
+
i
number
of
hours
this
a
year), expression be rewritten
8,766(the
S = exp[a(mi
-
ma) -
8,766mi].
(4)
(e.g., becauseof
In thespecialcase in whichall mortality
occursduringactivity
avianpredation),
S = exp(-ama).
(5)
withdifferent
risks
activityseasonsbutthesamehourlymortality
Populations
seasons
willdiffer
inexpectedannualsurvivalrates.In particular,
longeractivity
willresultin lowerS ifma > mi; theempiricalstudiesdiscussedabove suggest
thatthismayoftenbe true.The degreeofvariationin S dependson thevalues
twofold
overa typical
ofmaandmi(fig.3). For example,S variesapproximately
rangeofactivityseasonsif ma = 0.0005and mi = 0.0. However,S variesrelaover the same rangeif ma = 0.0001and mi = 0.0. Similarly,
tivelyslightly
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TEMPERATURE AND LIZARD LIFE HISTORIES
b
a
0
0
03
--~~~~~~~
-
00
ir
.1~~~0
-
UJ~~~~~~~~~~~~~~~~
z
281
-zM
HOURS OF ACTIVITYPER DAY, h
ENERGY ASSIMILATED PER DAY, Ea
FIG. 4.-Model assumptionsfordaily energyassimilationand allocationtowardreproduction by individuallizards. a, Daily energyassimilationEa (in arbitraryunitsof energy)as a
functionof activitytimeh. Dashed line illustratesthe special case where c2 = 0. b, Amount
of energyallocated per day to reproduction,Er, as a functionof Ea. Above a daily energy
thresholdEt (daily maintenancerequirements),a constantfractionfofeach day's assimilated
energyis allocated to reproduction.
of deathsoccur
variationin S is reducedas mi increases;as a greaterfraction
in
variation
season
will
have
a
smallereffect.Figure3
duringinactivity,
activity
in survivalrate(i.e., greaterthantwofold)
thatlargedifferences
also illustrates
amonglizardpopulationsor betweenyearsin a singlepopulationare likelyto
in mortality
differences
risksin additionto differences
in activity.
reflect
Thisis
the
between
S
and
to
due
a; doublinga reducesS by
exponentialrelationship
less thana factoroftwo.
Ourmodelforsurvivalrateassumesthatvaluesformaandmiare independent
ofactivity
wouldbe violatedby
patterns
(thevaluesofa and i). Thisassumption
that
are
either
to
animals
activetoo infrequently obtainenoughfoodor are so
activethattheycannotmaintaina positiveenergybalance(Marlerand Moore
to estimatea priori;however,they
1988,1989).Valuesformaandmiare difficult
can be estimated
fromsurvivalratedata.In ourtestofthemodel(see below)we
givean example.We knowof no otherpublishedestimatesforhourlymortality
risksin reptiles.
EnergyAssimilationand Allocation to Reproduction
We model energyintake and allocation to reproductionon a daily basis. An
individual'sdaily energyassimilation(Ea) may be limitedby eitherpreycapture
rate or by digestionand absorptionrates(Congdon1989). In eithercase, Ea
shouldvarypositivelywithhoursof activity:morepreycan be captured,and
will be fasterwhena lizardspendsmoretimeat a
digestionand assimilation
higherTb.We assumethatEa increaseswithdailyactivitytimeh accordingto
therelationship
Ea=
clh-C2h2,
(6)
unitsof energy(fig.4a) and cl and c2 are
whereEa is expressedin arbitrary
as h variesfrom0 to 12 h
constantschosenso thatEa increasesmonotonically
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THE AMERICAN NATURALIST
282
and is maximizedat h = 12 h. Thatis, energyassimilatedper hourdecreases
Theformofthisrelationtime(diminishing
withincreasing
dailyactivity
returns).
due to gut size, foodpassage rate,
limitations
shipcould reflectphysiological
satiation,and the like. Variationin preycaptureprobability
(amongdifferent
reform.Finally,diminishing
timesof day) wouldlikewiseyieldthisfunctional
turnscouldresultfrombehavior,iflizardsdo notuse all ofthepotential
activity
timeavailableto them(Sinervoand Adolph1989;Sinervo1990;see also Simon
and Middendorf
1976;Rose 1981).
is supported
forEa (diminishing
Thisgeneralrelationship
returns)
bythelaboraabove (Avery1984;Sinervoand
torystudieson lizardgrowthratesmentioned
Adolph1989;Sinervo1990).Dependingon thepopulationand species,growth
to c2 = 0) to curvilinear
linear(corresponding
curvesvariedfromapproximately
withpeaks near 12 h (C2 = 0.04 cl). This suggeststhatenergyintakein these
form.
juvenilelizardshad a similarfunctional
each day duringthe
We assumethatfemalesallocateenergyto reproduction
reproductive
season, iftheirintakeexceeds a minimum
dailyenergythreshold
Abovethisthreshold,
maintenance
allocationto
requirements).
Et (representing
ofenergyassimilated.
reproduction
(Er) is assumedto be a linearfunction
Thus,
,
E = t?for
r
f(E -Et),
Ea<Et
forE >2Et,
(7)
wheref is a fractionless thanone (fig.4b). The difference
Ea - Er includes
and growth.For simplicity
metaboliccostssuchas locomotion
we assumef and
oftimeofyear.
Et to be independent
We assumethatlizardsallocateenergyto reproduction
throughout
thereproductiveseason,whoselengthis 2y - n d, where2yis thelengthoftheactivity
season(as above) and n is thelengthin daysofthenonreproductive
season.The
minimum
valueofn is set by theamountoftimenecessaryforeggsto hatch(in
to acquiresufficient
oviparousspecies) and forhatchlings
energyreservesfor
We also assumethatn does not varyamongdifferent
overwintering.
environments.In reality,n couldbe shorterin warmenvironments
becauseeggswould
lizardsin warmenvironments
incubatein less time;alternatively,
mightcurtail
in longern.
reproduction
earlier,resulting
Totalannualenergyassimilatedis then
=
Eannual
(8)
Ea aij
where
Ea
2cd
1 -7ly2
-
4C2d2(1
_ j2/y2).
(9)
Thisyields
Eannual = dy[c Tr - (16dC2/3)],
(10)
whichshows thatthe annualenergybudgetincreaseswiththe lengthsof the
season2yand themaximum
activity
activity
day 2d.
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TEMPERATURE AND LIZARD LIFE HISTORIES
283
annualreproductive
Similarly,
investment
is givenby
=
Rannual
f_y
rY
Erai
=
f
V- 1
-itf(Ea
-
()
Et)ai,
where
It=
-
I
c-
4C2Et
(16d2C2)
(12)
limit(y - n) is thefinalday
andEa[h(j)] is givenabove; theupperintegration
limit-ji is necessaryto
of thereproductive
season, and thelowerintegration
avoid havingnegativevalues forEr earlyin the activityseason whenEa < Et
season
(-jt is thevalueofj forwhichEa = Et). We assumethatthereproductive
endsbeforeEa againfallsbelowEt (i.e., that[y - n] < jt). The solutionto this
is
integral
= fc, d/yx {(y
Rannual
-
n) Vy2
-
(y
-
n)2 +jt
y2 _
+ y2sin-1[(y- n)/y]+ y2sin-l(it/y)}
- 4fd2c2/3y2[2y3 + 3y2jt - 3yn2 + n3 - j3]
-
fEt(Y
(13)
-
n + it)
Because thisexpressioninvolvesmanyterms,the effectsof activityseason
and energeticparametersare not immediately
apparent.In the simplestcase
(setting
c2, n, and Et equal to zero) thissolutionreducestofdyclr, showingthe
on the area of the activityellipseand the energy
lineardependenceof Rannual
We assumethatRannual
intakeandallocationparameters.
is proportional
to annual
thisincludestheassumption
thattheenergetic
costperoffspring
fecundity;
does
notvaryamongenvironments.
We exploredthegeneralsolution(eq. [13]) by evaluating
fordifferent
Rannual
valuesanddifferent
parameter
activity
ellipsesizes. We choseseasons(2y)rangand maximum
ingfrom120to 300 d (30-dincrements)
day lengths(2d) ranging
from8 to 12 h (1-hincrements),
thevarietyof thermalenvironapproximating
lizardsat different
mentsencountered
bytemperate-zone
latitudesandaltitudes.
5a. Note thattherelationship
An exampleis shownin figure
betweenRannual
and
linearovera widerangeof
ellipsearea (= annualactivity
time)is approximately
termsin theintegral
solutionabove. Also
activityseasonsdespitethenonlinear
involvessome variationin Rannual
fora givenellipse
notethattherelationship
area. This is because of thecurvilinear
betweenenergyintakeand
relationship
time(fig.4a). For activityellipseswiththesamearea, an ellipsewitha
activity
highervalueofy (longerseason)buta lowervalueofd (shorter
days)willresult
in a largerannualenergybudgetand a largerallocationto reproduction.
While
values (forf, Et, and n) affectthequantitative
different
parameter
relationship
and annualactivity
betweenRannual
does notchange.
time,thequalitative
pattern
In general,a twofoldincreasein annualactivity
timeincreasesRannual
bya factor
of 1.4-3.5.
Underourmodelbothpredictedannualsurvivalrate(fig.3) and annualreproductiveinvestment
(fig.5a) varywiththe lengthof the activityseason. This
suggeststhatlizardlifehistoriescould differsubstantially
amongpopulations
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THE AMERICAN NATURALIST
284
a
b
1.0-
1.0
0:8 |
0.8
0~~~~~~~~~~~~~~~~~~~
E 0.6-
Eo
~
C:
500
.
0.6-
1*.
~ ~
0
0400
0.2
0.0
0
0.6-~~~00.
0.6-
E
**
0.0
0.2
1000
1500
2000
2500
Annual ActivityTime (hours)
3000
0.0
0.3
0.
0.4
0.5
0.6
0.7
Annual Adult Survivorship
FIG. 5.-Model predictionsof annual reproductiveallocation(Rannual)
evaluatedforactivity
seasons rangingfrom=750 to =3,000 h yr-'. Values ofRannual
are normalizedto themaximum
as a functionof activityseason length.In thisexample,
value of 404.6 energyunits.a, Rannual
cl = 1.0, c2 = 0.042, f = 0.3, n = 60, and Et = 0.0. Otherparametervalues yield similar
graphsthatdiffermainlyin overall slope. Connected points representactivityseasons with
the same numberof days (2y) but different
maximumday lengths(2d); nonlinearitiesresult
fromthediminishing-returns
assumptionforenergyassimilation(fig.4b). b, Predictedpattern
and annual adult survivalrateamongpopulationsfromdifferent
ofcovariationbetweenRannual
thermalenvironments,combiningreproductiveoutputfromfig.5a and survivalrate curves
fromfig. 3b (with ma = 0.0003 and mi = 0.00003). This negative relationshipbetween
survival rate and reproductiveoutput is a proximateconsequence of variationin activity
season length.Similarly,data presentedby Tinkle (1969) show a negativerelationship(r =
-0.88, P < .001) between annual adult survivalrate and annual fecundityon the basis of
empiricalstudies of 14 lizard populations(13 species). These data matchpredictionsof both
our mechanisticmodel and evolutionarymodels.
ofdifferent
simplybecauseoftheproximate
effects
thermal
environments,
without any geneticdifferences.
This possibility
has been givenless attention
than
evolutionary
explanations
(Tinkleand Ballinger1972;Stearns1977,1980,1984;
Ballinger1983;Joneset al. 1987;Dunhamet al. 1988;Jamesand Shine 1988),
almostnothing
is knownaboutthegeneticbasis of lizardlifehistories
although
(Ballinger1983;Sinervoand Adolph1989;Fergusonand Talent1993).
Evolutionary
life-history
theorypredictsthathighannualreproductive
investmentwill evolve whenannualadultsurvivalrateis low (Tinkle1969;Stearns
1977;Pianka 1988). Underthistheory,comparisonsof speciesor populations
betweensurvivalrateand fecundity
shouldshowa negativecorrelation
(Tinkle
based model offersthe same prediction,
1969). Our physiologically
without
betweenpopulations
evolveddifferences
(fig.5b). Thus,thenegativecorrelation
betweenannualfecundity
and annualsurvivalrateobservedby Tinkle(1969)
couldreflecttheproximate
influence
of temperature
ratherthan(or in addition
to) adaptiveevolutionof reproductive
investment
to compensateformortality.
Ourmodelsuggeststhatthermal
effects
on reproductive
outputwillautomatically
compensate(at least partially)forthermaleffectson survivalrate,if foodresourcesare not limiting.
Because bothevolutionary
and physiological
models
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TEMPERATURE AND LIZARD LIFE HISTORIES
285
predictthe same phenotypic
patterns,simplecomparisons
of wildpopulations
willnotdistinguish
betweenthem.
TESTING
THE MODEL:
DATA FROM SCELOPORUS
UNDULATUS
and annualadultsurvivalratewill
Our modelpredictsthatannualfecundity
We testedthesepredictions
co-varywithannualhoursofactivity.
usingpublished
datafrom11populations
oftheeasternfencelizard(Sceloporusundulife-history
in montane,
latus).This species is widespreadin the UnitedStates,occurring
woodland,prairie,and deserthabitats(Smith1946).These data werecollected
by severaldifferent
researchers
and weresummarized
in Dunhamet al. (1988).
EstimatingActivitySeasons
We calculatedpotentialactivityseasonsforeach populationusingcomputer
and animalTbon thebasis of heattransfer
modelsthatestimatemicroclimates
principles
(Porteret al. 1973;Porterand Tracy1983).For each population,
we
andmaximum
obtainedclimatedata(monthly
airtemperatures)
averageminimum
fromthenearestavailablelocationforeach yearofthefieldstudy(U.S. Weather
wereadjustedfordifferences
in altitudebetweenstudy
Bureau).Temperatures
sitesand climatestationsat the theoretical
adiabaticcoolingrateof 9.9?C per
kilometer
ofaltitude(Sutton1977).Detaileddiscussionofthismodelis presented
in Porteret al. (1973).Solarradiation
was calculatedon thebasis ofMcCullough
andPorter(1971;software
SOLRAD [developedbyW. P. Porter]availprogram
ablethrough
WISCWARE,University
ofWisconsinAcademicComputer
Center,
alti1210WestDaytonStreet,Madison,Wis. 53706).Exceptfortemperatures,
tudes,andlatitudes,
we assumedall studysiteswereequivalentintheirmeteorologicalcharacteristics
(e.g., windspeed,cloudcover,soil thermal
conductivity)
becauselocallyspecificinformation
was unavailable.Table 1 liststhevaluesof
we used in thesesimulations.
parameters
and
simulations
estimatedair and soil temperature
The microclimate
profiles
forthefifteenth
at ?1-h intervals
radiation
conditions
dayofeach month.These
modelthatcalculatedtheequilibrium
datawerethenused as inputto a computer
and
Lizardmorphological
Tbattainable
bya lizardwithgiventhermal
properties.
1.
We
assumed
in
table
used in thisanalysisare given
thermalcharacteristics
a typicaladultbody size forS. undulatus(Dunhamet al. 1988)and obtained
forabsorptivity
measurements
and Gates
(Norris1967)and emissivity
(Bartlett
assumed
that
lizards
We
could
be
of
radiation.
active
whenever
1967)
potentially
in
them
to
reach
a
their
microclimates
permitted
Tb
preferred
bodytemperature
rangeof32?-37?C(Bogert1949;Avery1982;Crowley1985).Themodelcalculated
at <5-minintervalsthroughout
Tbestimatesforvariouspossiblemicrohabitats
fromfullsunlight
theday. Lizardswere"allowed" to chooseperchesranging
to
fullshadeand at anyheightfromthegroundto 2.0 m offtheground.Sceloporus
use (Smith1946),and Sceloporus
undulatusare flexiblein theirmicrohabitat
andperchheight
lizardsareknowntouse baskingfrequency
choiceas thermoregulatorymechanisms
(Adolph1990a).
The computerprogramdetermined
how muchtimelizardscould have been
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286
THE AMERICAN NATURALIST
TABLE 1
PARAMETER
ANDANIMALENERGETICS
VALUESUSED IN MICROCLIMATE
MODELS
Value
Parameter
Environment:
Soil solar absorptance
Soil density x specificheat
Soil thermalconductivity
Substrateroughnessheight
Cloud cover
Wind speed at heightof 2.0 m
Humidity
Slope
Lizard:
Body mass
Snout-ventlength
Solar absorptivity
Infraredemissivity
Surface area, silhouetteareas, and shape factors
PreferredTb range
.70
2.096 x 106m-3 K-l
2.5 W m-1 K-'
.001 rn
None (clear skies)
Varies daily from.5 to 2.5 m s
Varies daily from20% to 50%
100 north-facing
10 g
65 mm
.95
1.0
See Porterand Tracy (1983)
320-370C
NOTE.-Models and parametersare describedin detail in Porteret al. (1973) and Porterand Tracy
(1983). Values were assumed to be equal forall studysites.
activeduringan averageday of each month,multiplied
thisby thenumberof
daysin thatmonth,and summedthesevaluesfortheyear.For empirical
studies
lastingmorethan 1 yr,we used climatedata foreach year of the studyand
estimatesofannualactivity
time.Calculatedpotential
averagedtheresulting
annualactivityseasons rangedfrom1,707h foran Ohio population
to 3,012h for
in Texas.
a population
Survival Rate
Populationswithlongerpotentialactivityseasonshad lowerobservedannual
survival
rateofadultfemales(fig.6a). Thissuggests
thatmortality
riskwas higher
foractivethanforinactivefencelizards.The relationship
betweensurvivalrate
and activity
timeallowsus to estimatetheserisks.Fromequation(4),
ln(S) = (mi - ma)a - 8,766mi.
(14)
Withthisequationand theassumptionof equal risksforall populations,
leastof thedata in figure
6a yieldsestimates
of0.0 to 5.8 x 10-5
squaresregression
per hourformi (95% confidenceintervalforthe intercept,
omitting
negative
values formi). The slope of the regression
[undefined]
(whichestimatesmi ma) is -1.97 x 10' (confidence
interval,+8.3 x 10-), suggesting
thatma is
x
2.0 10' perhour.However,thisestimateofmais impossibly
approximately
high;even ifall mortality
occurredduringactivity,
themaximum
value forma
wouldbe lower,as follows.We obtainedmaximum
estimates
formabyassuming
mi = 0 and usingequation(5) separatelyforeach population.Estimatedmaximumma averaged
5.5 x 10-i perhourandrangedfrom3.0 x 10-4 to 9.3 x
10-4. The discrepancy
betweentheregression
estimateformaandtheindividual
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287
TEMPERATURE AND LIZARD LIFE HISTORIES
a
0.6
1
0.40
1500
b
>- 40
20
500
0.2-
,U.
S
0.~1
z
.
0.05
1500
0
2000
c
01%
~
3000
2500
~
~
~ ~ ~
CD,1
z
z
.4
0
1500
2000
2500
3000
d
~~~2.10
2.0
42
1500
UJ
~~~-1.0. *
2000
2500
3000
ANNUALACTIVITYTIME (HOURS)
0
~~~~~~~~~~~~~~-2.0
1500
2000
2500
3000
ANNUALACTIVITYTIME (HOURS)
features(publisheddata fromfieldstudies,
FIG. 6.-Relationshipsbetweenlife-history
microcliinDunhametal. 1988)andlength
ofactivity
season(calculated
through
summarized
forNorthAmerican
oftheiguanidlizardSceloporusundulamatesimulations)
populations
seasonand annualsurvivalrateof
tus.a, Negativerelationship
betweenlengthofactivity
adultfemales,plottedon a logarithmic
scale (see eq. [4]) (r = -0.76 fornatural-logbetweenannualfecundity
transformed
(mean
data,N = 10,P < .01).b, Positiverelationship
season
ofactivity
ofeggsperclutchx meannumber
ofclutchesperyear)andlength
number
(r = 0.55, N = 11, P < .05). c, Positive relationshipbetweentotal annual egg mass (annual
x meanmassperegg)andlengthofactivity
season(r = 0.36,N = 10,P > .1).
fecundity
seasonandresidualtotalannualeggmass,
betweenlengthofactivity
d, Positiverelationship
femalesineachpopulation
ofmature
aftercorrecting
forbodysize (meansnout-vent
length)
(r = 0.82, N = 10, P < .005). Lines show least-squaresregressions;P values forcorrelation
based on ourmodel.
testsof a priorihypotheses
one-tailedsignificance
coefficients
reflect
estimatesindicatesthatthereducedsurvivalrateofS. undulatus
poppopulation
risk
an increasein hourlymortality
ulationswithlongeractivityseasonsreflects
times.Thisconclusion
oflongeractivity
(eitherma or mi)inadditionto theeffect
is higherat low
is consistentwiththe commonbeliefthatpredationintensity
latitudesand at low altitudes(butsee Wilson1991).In eithercase, ouranalysis
riskaveragedat least 10 timeshigherforactive
indicatesthathourlymortality
fencelizardsthanforinactivelizards.
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288
THE AMERICAN NATURALIST
Annual ReproductiveOutput
Dunhamet al. (1988) estimatedannualfecundity
foreach populationof S.
meannumberofclutches
undulatusas themeanclutchsize timestheestimated
laidperyear.Theyalso provideinformation
on averageeggmass.We usedthese
data to comparetwo measuresof annualreproductive
output,annualfecundity
andtotalannualeggmass,totheestimated
lengthofactivity
seasons.Bothannual
fecundity
(fig.6b) and totalannualegg mass (fig.6c) werepositively
correlated
seasonlength,
as predicted
withactivity
byourmodel.However,therelationship
fortotalannualeggmasswas notstatistically
andinbothrelationships
significant,
for.Although
muchof thevariationwas unaccounted
ourmodelpredictssome
scatterintheserelationships
(fig.5a), additional
factorsarelikelyto be involved.
and bodysize are potential
Food availability
complicating
factors,as bothare
knownto influence
reproductive
outputin lizards(Ballinger1977,1983;Stearns
1984;Dunhamand Miles 1985;Dunhamet al. 1988;MilesandDunham1992).To
whether
inbodysize ofS. undulatus
variation
determine
intraspecific
was related
to variation
in reproductive
a regression
outputwe performed
oftotalannualegg
massagainstthemeansnout-vent
length(SVL) ofadultfemalesin each population(Dunhamet al. 1988).We founda strongpositiverelationship
(totalannual
egg mass [g] = - 10.51 + 0.26 SVL [mm]; r = 0.76, N = 10, P < .05). Thus,
variation
in SVL amongpopulationsaccountedfor58% ofthevariation
in total
annualeggmass. We used residualsfromthisregression
as size-corrected
measuresof annualegg mass production.
Residualtotalannualegg mass was posiwithlengthofactivityseason(fig.6d). Together,
tivelycorrelated
bodysize and
lengthofactivityseasonaccountedfor87% ofthevariationin annualeggmass.
Thisleavesrelatively
littleresidualvariation
tobe explainedbyamong-population
in factorssuchas reproductive
variation
investment
or foodavailability.
and
size
season
to
influence
annualreproduction
in
Bothactivity
body
appear
size
can
be
into
model
our
the
S. undulatus.Body
incorporated
general
through
of metabolism,
energyintakeand allocationfunctions
(fig.4); the allometries
forlizards
allocationare well characterized
energyintake,and reproductive
Bennett
Bennett
and
Dawson
Dunham
et al.
(Fitch1970;
1976;
1982;Nagy1983;
food
could
alter
the
of
the
intake
curves
1988).Similarly, availability
shape
energy
(fig.4a) and perhapstheformof the allocationfunction
(fig.4b). Overalllifediffered
wouldthendependon howfoodavailability
history
patterns
amongtherand
Dunham
showed
thattheexGrant
For
malenvironments. example,
(1990)
traitsin Sceloporus merriamidepends on the interaction
pression of life-history
constraints.
betweenresourcelevelsand thermal
relatedto seasonality.For example,
Body size is also likelyto be intimately
lizardsbornin a longactivityseasonmaybe able to growsufficiently
hatchling
so thatthey reach minimumreproductivesize in time to reproducein the next
year. These lizards would be relativelysmall at maturityand consequentlywould
have small clutch sizes. In contrast,lizards born in a shorteractivityseason
mightnot reach reproductivematurityuntiltheirsecond year, when theywould
be large, and would consequentlyhave large clutches. This potentialnegative
effectof activityseason lengthon clutch size would counterthe positive effect
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TEMPERATURE AND LIZARD LIFE HISTORIES
289
betweenactivityseason
of season lengthon clutchfrequency.The interplay
on the
maybe an important
influence
length,body size, and clutchfrequency
evolutionofeggsize and clutchsize in lizards.
DISCUSSION
low
Evolutionary
life-history
theorypredictsthatpopulationsexperiencing
and highfecundity,
adultsurvivalrateswillevolveearlymaturity
comparedto
considerations
suggest
populations
withhighadultsurvivalrates.Physiological
can resultfroma whollydifferent
oflife-history
thatthesamepattern
phenotypes
inducedvariationdue to theeffects
oftemperature
mechanism:
environmentally
fortheinterpretation
Thisresulthas implications
on activity
timeand energetics.
andforthephenotypic
forlife-history
response
oflife-history
evolution,
patterns,
to climatechange.
ofpopulations
theneedformoreinformation
on thegeneticbasis ofintraFirst,it highlights
in lizardlifehistories.Comparisons
variation
oflifehistories
as
andinterspecific
are imperfect
testsofevolutionary
theorybecause
measuredin wildpopulations
whether
determining
nonevolutionary
processesmaybe involved.In principle,
are genetically
based is straightforward,
via common-garden
life-history
patterns
eitherin the fieldor in the laboratory
(Ballinger1979;Bervenet
experiments
studiesare rarely
al. 1979;Bervenand Gill 1983).In practice,common-garden
butalso forphysiowithreptiles;thisis truenotonlyforlifehistories
performed
logical and behavioral traits(Adolph 1990b; Garland and Adolph 1991). Several
studiesofgrowth
and life-history
traitsinSceloporushavebeen
common-garden
and Adolph1989;Sinervo
experiments:
Sinervo
completedrecently(laboratory
data;
1990;FergusonandTalent1993;B. Sinervoand S. C. Adolph,unpublished
P. H. Niewiarowski
fieldtransplant
and W. M. Roosenberg,perexperiments:
sonalcommunication).
Each of thesestudiesfoundevidenceof interpopulation
as well as evidenceof strong
differences
thatmayreflectgeneticdifferences,
environmental
effects.These findings
variationamong
indicatethatphenotypic
naturalpopulations
is likelyto havebothenvironmental
andgeneticcomponents.
is thatlife-history
can
One consequenceofphenotypic
plasticity
optimization
if the reaction
be achievedwithoutgeneticdifferentiation
amongpopulations,
traitsare appropriately
normsoflife-history
shaped.However,decidingwhether
reactionnormis problematic.
The trounaturalselectionhas shapeda particular
must
norm
have
some
if
is
that
reaction
because
of
ble
shape(even flat)
every
nature
of
For
most
thefundamental
organisms
(Stearns1989).
physicochemical
we do notknowenoughabouttheunderlying
todetermine
physiology
organisms,
in
the
a
would
be
absence
of
selective
that
what
agent.
presumed
exactly
shape
truein thecase oftemperature,
whichcauses a widevariety
Thisis particularly
and life-history
offunctional
traits;thepreciseform
responsesin physiological
is rarelypredictable
fromlowerlevelsofintegration
ofa responseto temperature
null model
(e.g., enzymekinetics).Consequently,we have no physiological
be gaugedfora singlepopulation.
ofadaptation
might
againstwhicha hypothesis
based differences
in reactionnormsamongpopulationsin
Findinggenetically
different
environmentsoffersmuch betterevidence foradaptive evolution(Ber-
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290
THE AMERICAN NATURALIST
venet al. 1979;Conoverand Present1990;B. Sinervoand S. C. Adolph,unpublisheddata).
Our modelpredictsthatthe proximateeffectsof temperature
on lizardlifetraitswillbe at leastpartially
withlowsurvival
history
compensatory:
populations
rates will also have highfecundity.In addition,these populations are likelyto
reachreproductive
maturity
earlier,althoughour modeldoes not includethis
trait.Thissuggeststhattheimpactofdirectional
climatechangeon lizardpopulaas longas factorssuchas foodavailtiondynamicswillbe partially
ameliorated,
riskare notalteredsubstantially.
abilityand mortality
However,thesefactors
dependon thephysiological
responsesofotherspecies,bothpreyandpredators.
For example,food availability
mightbe largelydetermined
by the overlapbetweenlizardand preyactivitytimes(Porteret al. 1973).If theseactivitytimes
to a givenchangeinthethermal
responddifferently
environment,
expecteddaily
ratesmaychange,whichwouldchangetherelationship
encounter
betweenentime(fig.4a). Similarly,
lizardmortality
ergyintakeandactivity
ratesmaydepend
on overlapbetweenactivitytimesof lizardsand theirpredators.Thus,thereto climatechangeis likelyto dependon thephysiolsponseoflizardpopulations
ogyofotherspeciesas wellas theirownphysiology.
is an important
linkbetweenthethermal
Activity
environment
and lizardlife
histories.Therefore,
are a likelytargetofnaturalselection.Inactivitypatterns
deed, Fox (1978)foundthatsurvivalratesof individualUta stansburiana
were
withtheirtemporal
andspatialactivity
correlated
In manycases,lizards
patterns.
mayuse less thanthemaximum
potentialactivitytimeafforded
by thethermal
environment
(Simonand Middendorf
1976;Sinervoand Adolph1989;Sinervo
1990),whichsuggestsa compromise
betweenthebenefits
and costs of activity
(Rose 1981).The difference
betweenpotential
andrealizedactivity
timesinvolves
behavioraldecisionsby thelizardthatmaybe shapedin partby local selective
regimes.The functional
relationships
betweenactivityand life-history
traitsare
likelyto playa keyrole in theevolutionof activitypatterns.Grantand Porter
(1992)presenta preliminary
analysisof a behavioraloptimization
modelformulatedin theseterms.
inlife-history
traitscomplicates
Phenotypic
plasticity
theformulation
ofevoluofpatterns
observedin nature.Idetionarymodelsas well as theinterpretation
theoriesshouldincorporate
bothproximateand evolutionary
ally,life-history
responses(Ballinger1983;Siblyand Calow 1986;Stearnsand Koella 1986;Beuchatand Ellner1987).The modelpresentedhereoffers
a generalframework
for
lizardlifehistoriesfroma physiological
Futureefforts
modeling
standpoint.
can
be tailoredto particularspecies or environments
detailedmechanistic
through
modelsofprocessessuchas digestionand metabolism
(e.g., Beuchatand Ellner
on resourceabundance(Joneset
1987;Grantand Porter1992)and information
al. 1987).
ACKNOWLEDGMENTS
We thankD. Bauwens, T. Garland, Jr.,J. Jaeger,R. M. Lee III, G. Mayer,
P. S. Reynolds,B. Sinervo, B. Wilson,and two anonymousreviewersforhelpful
This content downloaded from 128.114.163.7 on Thu, 5 Sep 2013 17:33:27 PM
All use subject to JSTOR Terms and Conditions
TEMPERATURE AND LIZARD LIFE HISTORIES
291
discussion or commentson the manuscript.This researchwas supportedby the
Officeof Health and EnvironmentalResearch, U.S. Departmentof Energy,
throughcontractDE-FG02-88ER60633 to W.P.P., and by a Guyer Fellowship
(Departmentof Zoology, Universityof Wisconsin) to S.C.A.
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