Nordic Society Oikos
Age at Maturity Influences Adult Sex Ratio in the Turtle Malaclemys terrapin
Author(s): Jeffrey E. Lovich and J. Whitfield Gibbons
Reviewed work(s):
Source: Oikos, Vol. 59, No. 1 (Sep., 1990), pp. 126-134
Published by: Wiley-Blackwell on behalf of Nordic Society Oikos
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1990
OIKOS 59: 126-134.Copenhagen
adultsexratioin theturtle
influences
Ageat maturity
Malaclemys
terrapin
E. Lovich and J. WhitfieldGibbons
Jeffrey
adultsexratioin
influences
Lovich,J.E. andGibbons,J.W. 1990.Age at maturity
- Oikos59: 126-134.
theturtle
Malaclemys
terrapin.
forbiasedsex ratiosincluding
havebeenoffered
sampling
explanations
Numerous
differential
and
immigration
sexratios,differential
mortality,
bias,skewedprimary
of thesexes.We observeda strongly
maleand differential
maturity
emigration,
in SouthCarolina,USA. The
of theturtleMalaclemys
terrapin
biasedpopulation
sex ratiowas 1.78: 1. Althoughmalespredominated
overalladultmale:female
of recapturing
individuals
of eithersex was thesame
theprobability
numerically,
malebiasedwhen
(0.44 formales,0.38 forfemales).Sex ratioswereconsistently
andyearly
samples.Thisbiaswasnotalteredbytheuseofdifferent
basedonmonthly
or restriction
ofthesampleto majorhabitats
within
thestudy
collecting
techniques
adultsexratiosforotherpopulations
rangefromstrongly
reported
area.Previously
femalebiased.Reports
offemale-biased
samplesappeartobe
malebiasedtostrongly
a resultofsampling
biasortheartificial
conditions
underwhichterrapins
havebeen
inthepast.Theexcessofmalesinourpopulation
cultivated
appearstobe a resultof
of maturity
mature
in thetiming
betweenthesexes.Male Malaclemys
differences
a minimal
effect
aftertheirthirdyearandfemalesaftertheirsixthyear.Assuming
andregular
weexpectthatmale
from
factors
juvenilerecruitment,
theotherpotential
Weproposethat
Malaclemys
willmaintain
numerical
superiority
inmostpopulations.
inthe
adultsexratiovariation
inturtles,
andotherorganisms
withsexualdifferences
can be explainedwitha simplemodel:theearliermaturing
sex
ofmaturity,
timing
willpredominate
numerically.
J.E. LovichandJ.W.Gibbons,
SavannahRiverEcologyLab., DrawerE, Aiken,SC
29801,USA.
Fisher(1930) originally
envisioneda 1:1 sex ratioas
evolutionarily
stable,predicting
thatparentalinvesthave mentshouldbe equallydividedbetweenmaleand feImbalancedadultsex ratiosin turtlepopulations
been reportedfordecades (Hildebrand1929,Cagle maleoffspring.
He arguedthatifa majority
ofoffspring
1952,Bury1979), althoughsamplingbias has often beingproducedwerefemale,thena parentwho probeen indictedas the explanation
forthesedeviations ducesmostly
maleswill,on average,havemoregrandfrom1:1(ReamandReam1966,Gibbons1970).In this children
thanone thatdoes notproducemostly
males.
paper,wepresent
evidencefora significant
male-biased Underthesecircumstances
thesexratioina population
sex ratioin a population
of thediamondback
terrapin willbe restoredto unity.The same argument
would
(Malaclemysterrapin).This bias is not a resultof sam- applyshouldan excessofmalesbe produced.
Hamilton
plingerrorbutinsteadresultsfroma biologicalcause. (1967)laterpointedoutthatFisher'sargument
didnot
Sex ratiosthatdiffer
fromthe1:1 ratiopredicted
by applyin extreme
situations
wheretherewas localmate
Fisher(1930) havebeen of greatinterest
to biologists competition.
Hamiltonlisted26 speciesof insectsand
andnumerous
explanations
havebeenoffered
fortheir miteswithhabitualsib matingand an arrhenotokous
existence(see reviewsin Hamilton1967, Maynard breedingsystemthatexhibited
strongly
female-biased
Smith1978,Armitage1987,Chapmanet al. 1989a). offspring
sex ratios.Thisstrongfemalebias wouldbe
Introduction
Accepted 17 June1990
(
OLKOS
126
OIKOS 59:1 (1990)
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All use subject to JSTOR Terms and Conditions
ourconclusions.
Each excanmatewithall his Cousens1985)to formulate
expectedifa singlemaleoffspring
to
a parentthatpro- planationwas testedas an alternative
hypothesis
sisters.Underthesecircumstances
is based on
itsutility.
Our finalconclusion
duces only one male per clutchwill producemore determine
ofcompeting
hypotheses.
thanone thatproducesmorethanone elimination
grandchildren
Triversand Willard(1973) sugmale. More recently,
gestedthatnaturalselectionfavorsdeviationsaway
thandeviations
in thesexesrather
from1:1 investment
in sex ratiosperse. Theirmodel,validatedbydatafor Materialsand methods
statesthatif
severalpolygynous
speciesof mammals,
Defining sex ratio
fitness
ofoffspring
varianceinthefuture
thereis greater
sexratioas the
ofone sex relativeto theother,thena parentin good As Ehrlichet al. (1984)noted,defining
ofmalesandfemales
ina population
moreofthe relative
proportion
willbenefit
condition
byproducing
physical
ofdefinition
difficulties
andcompuhighvariancesex.All ofthesemodelsfailtoexplainthe concealssubstantial
thatonlysexually
sex ratiosexhibitedby reptileswithenvi- tation.We considerit imperative
enigmatic
be includedin calculations
of sex
ronmental
sex determination
(Bull andCharnov1989). matureindividuals
Gibbons ratio.The adultsexratiois important
In a recentreviewof sex ratiosin turtles,
demographically
factors
thatcan in- becauseofthepotential
influence
thattherelative
fourdemographic
(1990)identified
proThe first portionof thesexescan haveon timespentsearching
fluencethesex ratioof a naturalpopulation.
to formates,intrasexual
referred
and annualpropafactoris thesexratioat hatching
competition,
(hereafter
ofskewed guleproduction.
as theprimary
sexratio).Evidenceinsupport
fortaxaas diverse Emlenand Oring(1977)advancedtheconceptofan
sexratioshasbeenreported
primary
sex ratiothattheydefinedas the"average
as insects(King1989)andbirds(Howe 1977).Skewed operational
sexratiosareespecially
femalesto sexuallyactivemalesat
possibleinanimalswith ratioof fertilizable
primary
suchas someturtles anygiventime."Thisdefinition
environmental
sex determination
wascriticized
byKluge
and a varietyof otherpoikilotherms
(Bull and Vogt (1981) becauseit did not definethe durationof the
1979,Bull 1980,Morrealeet al. 1984,Fergusonand sampling
period,ortheproblems
associatedwithdetersexualactivity.
Another
Joanen1982,VogtandBull1982a,1984,Conover1984, mining
definition
wasproposed
Middaughand Hemmer1987,Deemingand Ferguson byEhrlichet al. (1984) in theirworkwithbutterflies.
differentialTheydefined
1989,Langet al. 1989).The secondfactor,
realizedsexratioas theratioofmalesina
unitparticipating
of the sexes,has also been suggestedas a demographic
mortality
in theadultflight
of a
cause of skewedsex ratiosby Selander(1965),Howe singlegeneration
tofemalesinthesameunitandgener(1977), Hurly(1987) and Elmqvistet al. (1988). The ation.
thirdfactorthatmaycauseskewedsex ratiosis differ- In Malaclemys,
strictadherenceto the definitions
and immigration
betweenthe sexes proposedbyEmlenandOring(1977)andEhrlichet al.
entialemigration
factoris differential(1984) is complicated
(Morrealeet al. 1984).The fourth
by spermstorage(Hildebrand
betweenthe sexes (Kozlowski1989, 1929)and overlapping
age at maturity
generations,
respectively.
Thus,
Gibbons1990,Lovichet al. 1990).Resourcecompeti- in thispaperwe definefunctional
sexratioas therelationhasbeensuggested
as a causeofsexratiovariation tiveproportion
of sexuallymaturemalesto sexually
in someorganisms
(Silk 1984,Chapmanet al. 1989a, maturefemales.
King1989).However,the"localresourcecompetition
thatthesexes
hypothesis"
is based on theassumption
exhibit
ofdispersal
differential
(Chapmanetal.
patterns
The studyanimal
theresourcecom1989b).Becauseofthisrelationship,
tothedifferential
modelis subordinate
emigra- Thediamondback
petition
istheonlyspeciesofturtle
terrapin
in
tionand immigration
modelmentioned
above.
NorthAmericathatinhabitsbrackishcoastalhabitats
A fundamental
sex exclusively.
in studiesconcerning
assumption
It is widelydistributed
alongthecoastof
ratiosis thatsamplingis not biased(Gibbons1970). the UnitedStatesfromCape Cod, Massachusetts
to
Reportsof unbalancedsex ratioscan be causedbybi- CorpusChristi,Texas. This speciesexhibitsdramatic
asedcollecting
(ReamandReam1966)orby femaledominated
techniques
sexualsizedimorphism
(Gibbonsand
different
betweenthesexes(Hurly Lovich1990). In our population,adultmaleshave a
captureprobabilities
1987). Minimization
of these biases is essentialfor meanstraightline
plastronlengthof 102 mmand feofsex ratios.
meaningful
interpretation
maleshavea meanof148mmfora femaletomalebody
In thispaper,wediscussthemale-biased
sexratioina size ratioof 1.45.Mean maleandfemalemassis 242g
terrapin
(Malaclemys and705g, respectively,
populationof the diamondback
fora femaleto malemassratio
of the biased of 2.91. Adultsare easilysexeddue to differences
terrapin)
and evaluatethe applicability
in
pro- bodysize and othersecondary
samplehypothesis
andeachofthefourhypotheses
sexualcharacteristics.
posed by Gibbons(1990) to our data. We use the Femaleshave proportionally
widerheadsthanmales,
"stronginference"
procedureof Platt(1964,see also and maleshavelongtailswiththecloacalopeningsit127
OIKOS 59:1 (1990)
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Table 1. Yearly variationin sex ratios (M:F) of diamondback
terrrapinsfromKiawah Island, South Carolina. Ratios desigfrom1:1 at P ' 0.05.
nated withan asteriskdiffersignificantly
Males
Females
Ratio
1983
Firstcapture
24
4
6.00*
1984
Firstcapture
All captures
39
49
12
13
3.25*
3.77*
1985
Firstcapture
All captures
4
5
5
6
0.80
0.83
1986
Firstcapture
All captures
37
69
36
43
1.03
1.60
1987
Firstcapture
All captures
26
38
17
26
1.53
1.46
1988
Firstcapture
All captures
99
127
62
85
1.60*
1.49*
1989
Firstcapture
All captures
36
70
13
29
2.77*
2.41*
Combined
Firstcapture
All captures
265
382
149
206
1.78*
1.85*
Year/sample
in sex ratio(M:F) ofdiamondback
terrraTable3. Variation
pinsfromKiawahIsland,SouthCarolinaas a resultof samwithan asterisk
differ
Ratiosdesignated
plingtechnique.
sigfrom1:1 at P ' 0.05.
nificantly
Technique/
sample
net
Trammel
Firstcapture
All captures
Seine
Firstcapture
All captures
Combined
Firstcapture
All captures
Males
Females
Ratio
100
161
83
113
1.20
1.42*
127
152
49
58
2.59*
2.62*
227
313
132
171
1.72*
1.83*
saltmarsh.The climateis subtropicalwithtemperatures
fallingbelow freezingon fewerthan 20 d duringthe
winter.Tidal creekswithinthesalt marshstudyarea are
subject to 2 m dailytidal fluctuations.A more detailed
descriptionof Kiawah Island is given in Gibbons and
Harrison(1981).
Techniques
A varietyof collectingtechniqueswere used including
dipnetting,hand capture, seining,trammelnets, and
uated posteriorof the shell margin.Aspectsof the nat- trawling.The vast majorityof specimenswere collected
ural historyof this species are reviewedin Ernst and withtrammelnetsand seines. A totalof 414 individuals
were captured588 times. Individualswere markedfor
Barbour (1972) and Palmer and Cordes (1988).
futurerecognition,sexed, measuredand released at the
pointof capture.Estimatesof sex ratiosforotherpopulationswere obtained fromthe literature.Ratios were
The studysite
tested for significantdeparturefrom1:1 using a ChiTurtles
werecollectedfrom1983to 1989insaltmarshes square testcorrectedforcontinuityat an alpha level of
aroundKiawahIsland,SouthCarolina,USA. Kiawah 0.05 (Zar 1984).
Island is an Atlanticcoast barrierisland located about
25 kmsouthwest
of Charleston,
SouthCarolina.The
3200 ha, halfofwhichis
islandcomprisesapproximately
Table 2. Monthlyvariationin sex ratiosof diamondbackterrapins fromKiawah Island, South Carolina. Ratios designated
withan asteriskdifferfrom1:1 at P ' 0.05.
Month
Apr
May
Jun
Jul
Aug
Firstcapture
All captures
Sex
Sex
M
F
Ratio
M
F
Ratio
117
46
45
30
22
58
47
14
23
6
2.02*
0.98
3.21*
1.30
3.67*
167
73
58
50
24
86
57
17
35
9
1.94*
1.28
3.41*
1.43
2.67*
Table4. Sexratiosofdiamondback
terrapins
invariousaquatic
habitats
ofKiawahIsland,SouthCarolina.Ratiosdesignated
withan asterisk
differ
from1:1 at P ' 0.05.
Firstcapture
All captures
Sex
Habitat
Kiawah
River
Terrapin
Creek
Fiddler
Creek
Oyster
Creek
Sex
M
F
Ratio
M
F
Ratio
11
10
1.10
13
12
1.08
54
39
1.38
119
73
1.63*
122
68
1.79*
159
86
1.85*
7
3
7
4
1.75
2.33
128
OIKOS 59:1 (1990)
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Table 5. Sex ratiosof diamondbackterrapinsas reportedin selectedreferences.Seasonal variationin sex ratiosis reportedwhen
from1:1 at P _ 0.05.
available. Male to femaleratiosdesignatedwithan asteriskdiffersignificantly
Reference
Locality
Males
This study
Cagle (1952)
Seigel (1984)
South Carolina
Louisiana
Florida
Hurd et al. (1979)
Delaware
Bishop (1983)
South Carolina
265
57
5
9
4
251
176
195
149
13
42
90
22
336
144
86
1.78*
4.38*
0.12*
0.10*
0.18*
0.75*
1.22
2.27*
Sachsse (1984)
Captivity
132
41
50
40
3
2
3.30*
13.67*
25.00*
Hildebrand(1929)
Captivity
239
1058
0.23*
Hildebrand(1932)
Captivity
209
1233
0.17*
Hildebrandand
Hatsel (1926)
Captivity
15
85
0.18*
22
Females
43
M:F ratio
0.51*
Comments
Banana River, Feb-Nov
Indian River, Feb-Nov
Indian River, Mar-Apr
1975
1976
Overall ratio
1979
1980
1981
Hatchlingsex ratio
under artificialconditionsat 27 ? 20C
Hatchlingsex ratio
underartificialconditions
Hatchlingsex ratio
underartificialconditions
Hatchlingsex ratio
underartificialconditions
behaviorofthesexes,determination
oftheage or size
at maturity,
or a combination
ofthesefactors.
It is easy to imaginehow a certaincollecting
A totalof265 malesand 149femaleswerecollecteda
techtotalof382and206times,respectively.
Each malewas niquecouldbe biasedtowarda givensex.Forexample,
recaptured
a meanof 0.44 timesand each femalea in speciessuch as Malaclemysthatexhibitdramatic
of recaptures
did sexualsizedimorphism,
meanof 0.38 times.The proportion
use oftrapsornetswitha mesh
notdiffer
significantly
betweenthesexes(Contingencysizesmallenoughto letthesmallermalesescapewould
tableanalysis,
x2= 0.57; P > 0.10). The proportions
of resultina femalebiasedestimate.
Thiswasnotthecase
first
andoftotalcaptures
captures
arebothsignificantlyin our studysincemeshsize was considerably
smaller
biasedtowardmales(P < 0.05). Sex ratiosweremale thanthesize at whichmalesreachsexualmaturity.
biasedin all yearsforwhichrelatively
The sexesmayalso segregateintoslightly
largesamples
different
wereavailable,somesignificantly
so (Table1). Monthly microhabitats
at certaintimesof the year.This may
variation
in sex ratiowas generally
malebiased(Table explaintheheavilyfemale-biased
samplesreported
for
2). Sex ratioswere also male biased forbothmajor Malaclemyspopulationsin Florida(Table 5). Seigel
collecting
techniques
(Table3). Seiningproducedesti- (1984) set trammel
netsadjacentto the onlyknown
matesof male bias approximately
two timesgreater nestingsitein his studyarea (Seigel 1980a).The disthandatafortrammel
nets.Sex ratiosderivedfromthe proportionate
numberof femalecapturesappearsto
combineddata wereintermediate
butstillsignificantlyhavebeentheresultofthissampling
bias.Furthermore,
malebiased.All majorhabitatswithinthesaltmarsh thesmallnumbers
ofmalesreported
bySeigelmaynot
exhibited
a male-biased
sexratio(Table4). Estimates
of reflecttheiractualabundance.Large aggregations
of
sex ratiosforotherpopulationsrangefromstrongly terrapins
wereoccasionally
seen in hisstudyarea,but
femalebiasedto strongly
malebiased(Table5).
notcaptured(Seigel1980b).
in the behaviorof the sexes can also
Differences
affecttheperception
of sex ratio.This is particularly
ifthebehaviors
important
affect
theprobability
ofcapture.Forexample,concentrating
collecting
efforts
durDiscussion
thenesting
ing
season
can
result
in
female-biased
samSamplingbias
ples of mostspeciesof turtles(Gibbons1990). ConThe importance
ofsampling
biasmustbe considered
in versely,
thegreater
captureofmalesinsomeseasonsis
anystudyofsexratios(Gibbons1970).The perception probably
a reflection
ofincreased
mating
activity
bythis
ofpopulation
sexratiocanvaryas a function
ofcollect- sex (Morrealeet al. 1984,Parker1984).
ingtechnique,
microhabitat
sampled,differences
inthe
Another
problem
thatcanlead to biasedestimates
of
Results
129
9 OIKOS 59:1 (1990)
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it is also
ofsexualmatu- low incubation
sexratiosis theimproper
determination
temperatures.
Alternatively,
rityin one or bothsexes(Gibbons1970).In Malacle- possiblethatdifferential
ofmalesandfemales
mortality
mys,femalesmaturelaterandat a largerbodysizethan occurredduringembryonic
as a resultof
development
ofmaturity
infemalesat bodysizes incubationtemperature.
This phenomenonwas remales.Assignment
smallerthan thatat whichmaturity
actuallyoccurs portedbyBurgerandZappalorti(1988)forpinesnakes
wouldlead to increasing
femalebias in thecalculated (Pituophismelanoleucus).They foundthatmale:female
of immature
femalesin sexratiosoflivehatchlings
sex ratio,due to theinclusion
variedfrom0.11 at 21'C to
thesample.We avoidedthisproblemby determining1.40at 320Cundercontrolled
the
conditions;
however,
infemaleswithX-ray sexratioofliveandstillborn
thelowerlimitofsexualmaturity
combined
wasnot
embryos
different
photography
(Gibbonsand Greene1979).
significantly
fromunity.In contrast,
Vogtand
suchas thesemaybe responsible
Explanations
for Bull (1982a) concludedfromlaboratory
studiesof 14
manyofthefemale-biased
sex ratiosreported
in Table generaof turtles
thatsurvivalof embryos
to hatching
5. Furthermore,
theseproblems
servetounderscore
the was sufficiently
highto rejectthehypothesis
of differofconducting
importance
in anyas- entialembryonic
thorough
sampling
as a resultof incubation
mortality
sessment
ofsex ratios.
It is difficult
temperature.
to interpret
Sachsse's(1984)
Resultsforour studyarea showthatsex ratiosvary results
forMalaclemys
as proofforESD sincehe didnot
fromyearto yearand as a function
of sampling
tech- reportthe sex ratioof embryosthatmayhave died
nique.In spiteof thisvariance,samplesare stillmale duringincubation.It is also possiblethatunhatched
biased.In addition,overallrecapture
are eggs resultedfrominfertility
probabilities
insteadof mortality.
thesameforbothsexes.The probability
ofcapturing
a Hatching
successis only69% inMalaclemys
nestsunder
malewas greateroverallthanforfemalesdue to their fieldconditions(Burger1976). However,her data
numerical
advantage.However,individualmalesand shouldbe viewedwithcautionsinceshe periodically
femaleswereequallylikelyto be recaptured.
Based on uncovered
neststo determine
timeofhatching
(Burger
theseresults,
we rejectthehypothesis
thatmale-biased 1977).
sex ratiosin Malaclemys
on KiawahIslandare due to
It is tempting
to speculatethatESD wouldresultin
sampling
bias.
biasedadultturtlesex ratiosin nature.Vogtand Bull
(1984)observedthatundernaturalconditions
nestsex
ratiosof two speciesof the turtlegenusGraptemys
tendedto be all-maleor all-female
withan overallexSkewed primarysex ratios
cessof females.Nestswithmaleswereassociatedwith
In manyspeciesof reptiles,
sex is heavyvegetation
particularly
turtles,
andcool temperatures
andnestswith
determined
byincubation
temperature
(Bull and Vogt femaleswerelocatedin openareasexposedto thesun.
1979,Bull 1980,Morrealeet al. 1982,Vogtand Bull Sex ratiosvariedbetweennesting
beachesin response
1982a,1984). These studiesrevealedthattheeggsof to thedifferences
in theavailability
of thesetwocatemanyspeciesof turtlesdevelopas males at low in- goriesofnestsites.Sinceall-female
nestshatchedinless
cubationtemperatures
and femalesat highones. Al- timethanall-malenests,sex ratiosof emerging
hatchthoughpivotaltemperatures
vary,theyare generally lingswerestrongly
femalebiasedearlyintheseasonand
within
therangeof260-290C.
Itis important
tonotethat strongly
malebiasedlaterin theseason.Subsequent
to
not all speciesof turtlesare knownto exhibitenvi- thisstudy,Vogt(1980)reported
a female-biased
adult
ronmental
sex determination
(ESD). At leasttwospe- sexratioforhispopulation.
Thefemale-biased
adultsex
cies haveheteromorphic
sex chromosomes
interpretedratiosmayhave been due to samplingbias sincehe
as an XX/XYsexdetermining
system
(Siteset al. 1979, trappedmainly
nearareaswherefemaleswerelikelyto
CarrandBickham1981).In addition,
somespeciesnot nest.
knownto possessheteromorphic
sex chromosomes
do
Nest siteselectionin Malaclemys
was describedin
notexhibitsex ratiovariation
in responseto differentdetailbyBurgerand Montevecchi
(1975). Whencomincubation
temperatures
(Vogtand Bull 1982b,Bullet paredto randomly
selectedsitesin theirstudyarea,
al. 1985,Georges1988).Otherspeciesapparently
show actualnestsiteswerelocatedinstable,highduneareas
an interaction
betweentemperature
and geneticsex withlow vegetative
cover(less than20%) moreoften
determination
(Merchant-Larios
et al. 1989,Servanet thanexpected.Seigel(1980a)reported
thatMalaclemys
al. 1989).
in Floridanestedon elevateddikeroads.TheseobserThe questionofsex determination
hasnotbeenade- vationson nestsiteselectionagreewithoursin that
quately addressed in Malaclemys terrapin. Sachsse Malaclemys
nestson Kiawah Island have onlybeen
(1984)reported
thata groupofeggsincubated
at 27 + observedon smallsandyislandsand beachesin the
20Cresultedin a hatchling
successrateof50% witha marshwithlow vegetative
cover,exposedto considsex ratioof52 malesand 2 females.Theseresultssug- erableinsolation.
IfMalaclemys
follows
thenormalpatgestthatMalaclemys
mayhavethesamepattern
ofsex ternof ESD as suggested
by Sachsse(1984),thenthe
determination
reportedformanyotherspeciesof tur- relatively
open areas selectedfornestsitesmightbe
tles:largernumbers
ofmalesareproducedat relatively expectedtoproducea femalebiasas shownbyVogtand
130
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Bull (1984) forGraptemys.This is clearlynot the case
withour data, but such an explanationcannot be entirelyruledout forthe female-biasedratiosreportedby
Seigel (1984) (Table 5). The highlyfemale-biasedsex
ratiosreportedin Table 5 by Hildebrandare undoubtedly due to the artificialconditionsunder which eggs
were incubated.
We suggestthatin animals such as turtles,that maturelate in lifeand have a relativelylong lifespan(Gibbons 1987), variationin nest site selection and environmentaltemperaturesduringa female'sreproductive
in year-tolifewill tend to balance out any differences
year hatchlingsex ratios. Evidence in supportof this
hypothesiswas provided by Zweifel (1989) for the
picta. He reportedthatthesex
paintedturtleChrysemys
survivinguntil
ratio (based on the numberof offspring
developmentof secondarysexual characters)of broods
of a single female turtlevaried fromall males to all
femalesduringa five year period. However, the total
summedto unity.Mrosovskyet al. (1984a) foundthat
sex ratios of hatchlingloggerheadturtles(Caretta caretta)in South Carolina and Georgia varied fromno
females in nests laid at the beginningof the nesting
season in late May, to 80% femalesfromnestslaid in
early July,to 10% females from nests laid in early
in sex ratios
August. Despite such dramaticdifferences
withina season, the overallsex ratiowas near 1:1 when
data were combinedwithnestingfrequencydata over
six years.Similarresultswerereportedby Mrosovskyet
al. (1984b) for two other species of sea turtles.It is
doubtfulthat femalescan predictand compensatefor
variancewithina season since sex is deenvironmental
terminedseveralweeks afteroviposition(Yntema 1979,
Bull and Vogt 1981). Based on thisbody of evidence,
we tentatively
rejectthehypothesisthatthemale-biased
sex ratio in Kiawah Malaclemysis due to skewed primarysex ratios.
rateson nesting
can be
Predation
femaleMalaclemys
veryhigh.Seigel(1980c)reported
thatat least10% of
thefemalesin hisstudysitewerekilledin one yearby
he reportedheavilyfemalepredators.Interestingly,
biasedsex ratios(Table 5) in spiteof sucha highinWe haveoccasioncidenceoffemalespecific
mortality.
killed
allyobservedtheremainsoffemaleMalaclemys
(presumedly
duringnesting)on KiawahIsland.Howevidenceto conever,at thistimewe haveinsufficient
cludethatfemalesare preyeduponas heavilyas suggestedbySeigel(1980c).
The frequency
of predator-related
injurieshas been
used by othersto estimatepredatorintensity
(Rand
1954,Schoener1979,Schoenerand Schoener1980).
sinceinHowever,cautionis advisedin interpretation
of predatorinefficiency,
not
juriesmaybe indicative
ofmortality
factors
intensity
(Schoener1979).A variety
forMalaclemys,
can be envisioned
especially
juveniles.
is preHowever,thebehaviorof juvenileMalaclemys
thesamein bothsexes.Becauseofthis,rates
sumably
of mortality
shouldbe similarformalesand females
untilattainment
ofmaturity.
In ourmarkedpopulation
of Malaclemys
17 females(12%) weremissing
one or
morefeet,probably
as a resultofpredatorencounters
withterrestrial
mammals
(alligators
arenotfoundinthe
studyarea). Twentymales(8%) exhibitedsimilarinof injuredindividuals
juries.The proportion
did not
differ
betweenthesexes(Contingency
significantly
tax2= 1.35;P > 0.10). Basedontheseresults
bleanalysis;
we rejectthehypothesis
thatmale-biased
sex ratiosin
on KiawahIslandare due to differential
Malaclemys
mortality.
It is important
to notethatMalaclemys
(particularly
females)wereheavilyexploited
as a gourmet
fooditem
aroundtheturnofthiscentury
(Coker1920).Thisis no
longerthecase at ourstudysiteandthusis an unlikely
forthemale-biased
explanation
sex ratioobserved.
Differential
mortality
Differential
immigration
and emigration
Differentialmortalityof the sexes has oftenbeen invoked as a cause for biased sex ratios (see review in
Howe 1977,Ehrlichet al. 1984,Hurly1987,Burgerand
Zappalorti 1988, Elmqvist et al. 1988). Evidence for
biased adult turtlesex ratiosdue to differential
mortality was reportedby Gibbons (1990). He observed a
scriptaon a barrier
predominanceof female Trachemys
island near Kiawah (Gibbons et al. 1979). The relative
scarcityof males may have been a consequence of alligator (Alligatormississippiensis)predation.Male Trasmallerthanfemales(Gibbons
chemysare significantly
and Lovich 1990) and are presumablymore susceptible
to largepredatoryalligatorsin therelativelyvegetationfree habitat. High female specificpredationhas been
reportedfornestingturtles(Shealy 1976,Seigel 1980c),
buttheseauthorsdid notcommenton itspossibleeffect
on the populationsex ratio.
Maleturtles
ofmanyspeciesareknowntotravelgreater
distancesand movemoreoftenbetweenpopulations
thanfemales(Morrealeet al. 1984,Parker1984,Gibbons1986,Dodd etal. 1988,IngoldandPatterson
1988,
Lovich1990).Thesedifferences
in activity
are thought
to be representative
of differential
reproductive
strategiesbetweenthesexes.The following
predictions
are
associatedwiththishypothesis
(Morrealeet al. 1984):
1) malesbecomeactiveearlyto increasetheirchances
of matingwiththeearliestactivefemale(see Wiklund
andFagerstrom
1977),2) malesmoveto increasetheir
formultiplematings,
opportunities
and 3) duringthe
seasonmatesearching
nesting
activity
bymaleswillbe
reducedwhereasfemalemovements
will increaseas
theyseek nestsites.Because of thisdifference
in the
movement
patternsof males and females,sex ratios
may fluctuateover timein some populations.It is
131
9- GIKOS 59:1 (1990)
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All use subject to JSTOR Terms and Conditions
importantto note that departuresfromunityin local
populationsmay be balanced by immigration
and emigrationto and fromotherpopulations.
Verylittleis knownof movementpatternsin Malaclemys. Hurd et al. (1979) found littleevidence of immigrationand emigrationin the Malaclemyspopulation
theystudiedin Delaware. Our resultsforKiawah were
similarin thatthe vast majorityof specimensexhibited
highyear-to-year
site fidelity.Individualmales and females were oftenrecapturedwithinseveral metersof
theoriginalpointof capturein as manyas threesuccessive years, includingperiods before and aftertropical
stormsand hurricanes.Major displacementsof 100-200
m were seen in onlytwo males and fourfemales.Based
on these results,we reject the hypothesisthat malebiased sex ratiosare due to differential
patternsof immigrationand emigrationbetweenthe sexes.
ographicvariationin growthrate among the races for
whichdata have been reported(Seigel 1984). In spiteof
thisvariation,male Malaclemysmatureearlierthanfemales in the same population.
We propose that the male-biased sex ratio in our
populationof Malaclemysis a resultof differential
maturityof the sexes. Otherfactorsmaymodifythe resultantsex ratiosomewhat,but theirinfluenceappears to
be minimal.
Conclusion
Biased sex ratios can result fromseveral factorsincluding biased sampling,skewed primarysex ratios,
differential
mortality,
differential
immigration
and emigration,and differential
age at maturity.We used the
"stronginference"procedureof Platt (1964) (see also
Cousens
1985) to formulateour conclusions.Each exDifferential
maturity
planation was tested as an alternativehypothesisto
Accordingto Gibbons (1990), thesinglemostimportant determineits utility.Only differential
age at maturity
influenceon the sex ratioof some turtlepopulationsis provides a satisfactoryexplanation for the strongly
the differentialrate of maturityof the sexes that is male-biasedadultsex ratioexhibitedbyour studypopucharacteristic
of some species. Males of theturtleTrach- lationofMalaclemysterrapin.The potentialimportance
emysscriptamatureseveralyearsearlierthanfemalesin of the other factorsis not diminishedby this finding.
the same population(Cagle 1944, 1948, 1950, Gibbons However,theirindividualeffectsare apparentlyinsuffiand Lovich 1990, Gibbons et al. 1981). Gibbons (1990) cientto explain the extentof bias observed.
demonstratedthatifno otherfactorsare involvedthat
Our findingssuggestthatadult sex ratiovariationin
resulteitherin differential
mortalityrates of the sexes animalswithsexual differences
in the timingof maturior in differential
ratiosat hatching,Trachemyspopula- ty,can be explainedwitha simplemodel. We propose
tionsexperiencingjuvenile recruitment
will have more that the sex that maturesearlierwill predominatenuadult males than females. Conversely,Lovich et al. merically.A major assumptionof thismodel is thatthe
(1990) observed that in the wood turtle(Clemmysin- otherpotentialfactorshave a minimalinteractiveeffect
sculpta), a species in whichfemalesmatureearlierand on the resultantsex ratioand thatthe populationexpeat a smallersize thanmales, femalesoutnumbermales riencesregularrecruitment
of juveniles.
in populationsfor which large sample sizes are avail- We thankthemanypeoplewhoassisted
able. Thus, it appears thatthe sex thatmaturesearlier Acknowledgements
us withour collectionefforts.
They includeB. Botts,L.
will predominatenumerically.
Brandt,C. Culbreath,
J. Gibbons,M. Gibbons,S. Gibbons,
Juvenile male and female Malaclemys apparently D. Kling,R.
Lovich,S. Lovich,T. Mills,S. Morreale,T.
grow at the same rate forthe firstthreeyears (Coker Owens,J.Pechmann,
J.Schachter,
D. Scott,R. Semlitsch
and
1920,Seigel 1984). Males matureat about 90 mmbefore P. Stangel.We extendspecialthanksto themanagement
of
us accessto thestudysite.Earlier
the end of theirthirdyear (Cagle 1952, Seigel 1984) at KiawahIslandforallowing
versions
ofthemanuscript
benefitted
from
criticisms
offered
by
which time their rate of growthslows considerably J. Wolff,
J. Congdon,D. Gistand T. Tucker.Researchand
(Coker 1920, Hildebrand 1929, Cagle 1952, Seigel manuscript
preparation
weresupported
byContract
Number
1984). At the size at whichmales reach maturity,fe- DE-AC09-76SR00819betweentheU.S. DeptofEnergyand
males are only one half theiradult size (Coker 1920). theUniv.of Georgia'sSavannahRiverEcologyLaboratory.
Researchwasalsosupported
bytheEugeneP. OdumCoastal
Female growthcontinuesat the juvenile rate untilthey Conservation
Awardfrom
theSierraClubGulfCoastRegional
mature afterthe sixth year at between 160-176 mm Conservation
Committee
awardedto JEL.
(Cagle 1952). Some femalesmaymaturein theirfourth
year(Hildebrand 1932) at bodysizes as smallas 132 mm
(Montevecchiand Burger1975,Seigel 1984). The smallest male in our populationthatexhibitedwell defined
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