Estimation of von Bertalanffy Growth Curve Parameters from Recapture Data

Author(s): Ian R. James

Source: Biometrics, Vol. 47, No. 4 (Dec., 1991), pp. 1519-1530
Published by: International Biometric Society
Stable URL: http://www.jstor.org/stable/2532403 .
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 47, 1519-1530
BIOMETRICS
December1991

Estimation
ofvonBertalanffy
GrowthCurveParameters
from
RecaptureData

Ian R. James
SchoolofMathematical
andPhysicalSciences,MurdochUniversity,
Murdoch6150,Western Australia

SUMMARY
A simplemethodofconstructing estimating forparameters
functions in thevonBertalanffygrowth
modelE[y(t)] = L[ 1 - exp(-Kt)]is presentedfortag-recapture
datawhentheage oftheanimalis
unknown.The estimating functions are unbiasedunderverygeneraldistributional assumptions
providedK does notvarybetweenanimals.Simulations of growth in lobsters
and whelksindicate
thatthemethodperforms wellprovidedtheinitialcapturetimesand recapture varyover
intervals
reasonableranges.Comparison is madewithmethods basedon leastsquares,whichhavebeenshown
to be generally
inconsistent.

1. Introduction
The vonBertalanffy
growth curveis usedextensively in fisheries
and otherareasto model
thegrowthof an animalas a function of age fromsomeoriginto.If y(t) representsthe
growth measurement(whichwe refer to as lengthforconvenience) aftertimet,thenfora
singleanimalthemodelassumes

E[y(t)] = L[1 - exp(-Kt)] (1)

forpositiveparameters L and K. Withthisparameterisation L is referred to as the

asymptotic or maximumlengthoftheanimal,whileK regulates theexpectedpercentage
of maximumlengthachievedaftera particularage. Therehas been discussionin the
literature
aboutwhether suchinterpretationsarebiologically
meaningful [see,forinstance,
Knight(1968)].
Iftheavailabledataconsistofpairs(y(t),t) and theparametersL andK areassumedto
be thesameforeachanimal,thentheestimation problemmaybe approached byrelatively
standardnonlinearregression methods,possiblyusingreparameterisation to improve
computational and statisticalproperties(Kimura, 1980; Gallucci and Quinn, 1979;
Ratkowsky, one mightassumethatthe parameters
1986). More realistically, L and K
varybetweenanimals accordingto some distribution, in which case one has a
random-coefficients model and interest centreson the estimationof properties of the
see,forinstance,
distribution; Sainsbury(1980) and Palmer,Phillips,and Smith(1991).
We areconcernedin thispaperwithrecapture data forwhichtheage oftheanimalis
unknown, so thattheavailabledata consistof thelengthsat each captureand thetime
incrementsbetweenmeasurements. Fora singlerecapture, we observeforeachanimalthe

Keywords:Distribution-free
estimation;
Growthcurves;
Simulation;
Tag-recapture
data;Unbiased
estimating
functions.
151l9

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1520 Biometrics,
December1991
lengths
y,andY2 initially
and at recapture,
and thesingletimeincrement
A?.From(1),
y, = L[1 - exp(-Kt1)] + el,
(2)
Y2 = LI1 - exp[-K(t, + )]} + C2,

wheret1is theage at initialreleaseand el, C2 are zero-mean

residuals.
It followsfrom(2) by considering the meansof Y, and Y2 and eliminating
the term
exp(-Kt1) thatifI = Y2 - y, is the lengthincrement,then
E(I) = [L - E(yl)][1 - exp(-Kz?)]. (3)
Thisexpression has led to widespread use ofleast-squaresestimation methodsbasedon I
as theresponsevariableand an approximation to theright-hand sideof(3) as its"mean,"
theapproximation involving replacement ofE(yl), whichdependson theunknowntl,by
the observedy, (Fabens,1965; Kirkwoodand Somers,1984). However,thesemethods
producegenerally inconsistent estimators thatcan havelargebiases(Mallerand deBoer,
1988).
As discussedbyFrancis(1988),theproblemis thaty,is a randomvariablerather thana
fixedparameter.Francisrefers to(3) withE( yl) replacedbyy,as a vonBertalanffy "model"
fortagging data,presumably to be interpreted as a modelfortheconditionalmeanofI
givenyi,and pointsto incomparability oftheparameters in this"model"and thosein (2).
Thisis somewhat misleading, however. Thereisonlyoneunderlying vonBertalanffy model,
givenfora singleanimalby(1), and theapproximation basedon (3) is merelya construct
to be usedforestimating parameters in thatmodel.
In Section2 we indicate,by considering estimating functions, whyFabens' (1965)
methodusingleastsquaresproducesbiasedestimators, and we providea modification
thatgivesdistribution-freeestimators whichshouldbe consistent undermildconditions.
In Section3 finite-sample propertiesof thenewestimators are illustrated
by simulation,
whilein Section4 data on growthof thewhelkDicathaisaegaota are analysed.In our
treatment weallowL tovarybetween animals,butweassumethatK is constant. In practice
K mayalso varywitha relatively smallvariance(Sainsbury, 1980;Palmeret al., 1991).
The effectsofthisarebriefly considered in Section5, togetherwithextensions to thecase
wheremultiple recaptures areavailable.

2. Estimation

2.1 Introduction
Assumethateach animal is subjectto a singlerecaptureand that(2) holds forthe
measurements. The residualsareallowedto be correlated and haveunspecified
arbitrarily
variances,and L to varybetweenanimalsaccordingto a distribution withmeanLo and
varianceCL. On theotherhand,K is takento be constant,Ko say,overall animals.
Usingobviousnotation, let
Ti = Y2i - Yli - (Lo - yli)[l - exp(-KoAi)]
forthe ith animalin a sampleof size n. It thenfollowsfrom(3) thatE(,qi)= 0, the
expectationherebeingalso overthedistribution ofL. In general,thedistributions
ofthe
maydependon L, and thiscomplicates
residuals for
theexpression var(,qi).Whilstit is not
in
necessary our subsequentdiscussion, if we to
were assume that the residuals were
independent ofL, thenvar(fl1)
= E(n7) is givenby

2i+ Cl2iexp(-2KOi\i)
-2p11~O2exp-Ko~~)~L[
eXP(-KOl\i)]2~~~~~~~xp~~
- 2PiCliC2ieXP(-K0i\i)
+ CL[1 -

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 Estimation
ofGrowth
fromRecaptures 1521
whereoI, 2i, and Pi are the variancesand correlationcoefflcient
of the residualsel
and C2i. The varianceand correlation
structure
maydependon age at firstrelease,and
meansand variancesare conditional on theAibecausethesearegenerally
determined by
thesampling strategy.
If thegrowthfora singleanimalis deterministiconce itsparameters
are chosen,the
residualshavezerovarianceand theformula to
simplifies
var(rqi)= cr2[1 - exp(-KoA,)]2 (4)
1980;Kirkwoodand Somers,1984),whereasifL is assumedconstant
(Sainsbury, and the
residuals
independent
withconstant
varianceC2,
var(,qi)= a 2[1 + exp(-2KoAi)]j. (5)
Neither is likelyto accurately
ofthesesimplifications describe in practice,
thetruesituation
and themethodwe introduce belowavoidsthenecessity ofhavingto specifytheformof
variance.

2.2 Least SquaresApproaches

Based on the mean-zeroproperty of the mi,it is tempting to estimateKo and Lo by
minimising thesumofsquaresE t (Fabens,1965)ora weighted sumofsquaresassuming
a simplevariancestructure
suchas (4) or (5) (Kirkwoodand Somers,1984).However,we
do nothavetheusualregressionsituation ofa responsevariableand associatedmean.The
mqiare compositefunctions
of bothobservations and parameters, and thetwocannotbe
separated.Consequentlytheusual desirableproperties of leastsquaresestimators
do not
hold.
To seethis,let
fi = E [exp(-Koi\i) - 1]qj,

f2 = E Ai(Lo - yli)exp(-KoAj)qi.
Thentheestimating equationsforFabens'method, obtainedbyequatingpartialderivatives
ofE q; to zero,maybe written A1= 0 and f2= 0, wherethe"hat"indicatesreplacement
of parameters by theirestimates.An important ingredientin the usual derivationof
properties suchas consistencyand asymptotic normality ofestimatorsfromsuchequations
is thattheestimating functionsf' andf2 shouldbe unbiased,following theterminology of
Godambeand Heyde (1987); namely,E(f1) = 0 and E(f2) = 0 [see, for example,
Maritz(1981,?1, AppendixA)]. Whilstfisatisfies thiscondition,E(f2) involvesE(yliti),
whichin turndependson theunknownage oftheanimalifL is notconstant, and it is
easy to checkthatf2 is not an unbiasedestimating functionunlessthe model has no
residualsand (J = 0. It is thisbias inf2 thatleadsto thebiasesin parameter estimators
notedby Mallerand deBoer(1988). Similarcommentappliesto weighted leastsquares.
Morton(1981a) notedthesamebias problemin leastsquaresestimating functionsrelated
to insectdevelopment times.
It maybe possiblein somecasesto correct forthebiasinf2.Thisis true,forinstance, if
L is constant and theresidualsare independent withconstantvariancea 2. Thenone can
showthatE(Af)= E Aizexp(-2KO A,)a2, and sinceE[n-1E ~7t(l + exp(-2KOizi))]= U2
this bias may be correctedusing observablequantities.Further,if one minimises
E exp(-2Kq2/[l)],
%I[1 + obtainedbyweighting each termby theinverseof itsvariance,
thenestimating functionsobtainedbydifferentiation are unbiased.The following simula-
tionsillustratetheuse oftheseestimating functions
comparedwiththoseofFabens(1965).
We tookn = 200, K0 = .0007,and Lo = 115,to approximate theparameters foundin

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1522 Biometrics,
December1991
westernrocklobsters
(see ?3),theresidualswerenormalwithvariancea 2 = 4, and theage
and increment wererespectively
distributions uniform over300-1,000daysand 200-900
days.Meansand standard deviationsof446 replications
forwhichtheiterationsin Fabens'
methodconverged wereas follows:

Fabens'method leastsquares
Weighted
Ko Lo Ko Lo
Mean .00075 110.62 .00070 115.63
SD .00004 4.02 .00004 4.67

Whilstthebias correction underthesestrictconditions,

appearsto be successful it is our
aim to maketheestimation methodappropriate to thegeneralconditionsoutlinedat the
beginning forthebiasin leastsquaresmethods
ofSection2.1,and thencorrecting doesnot
seempossible.Alternative functions
estimating areconsidered in thenextsection.

2.3 UnbiasedEstimating
Functions
A straightforward
wayofobtaining unbiasedestimating
functions fromtheqiis to ensure
that any multiplying weightsare functionsonly of the Ai and the parameters. Let
h1i(A,Ko,Lo) and h2i(A,Ko,Lo) be twosuchfunctions.
It followsimmediatelythat
E[Z h1i(A,Ko, Lo)n] = 0 and E[Z h2i(A,Ko, Lo)i] = 0,
givingcorresponding
estimating
equations
E Ko,Lo)7i = 0 and L h2i(A,Ko, Lo)"i = 0.
h1i(A,
It remainsan openquestionas to whichfunctions h, and h2are "best."Application
of
theresultsin Morton( 1981b) givesoptimalweightsthatgenerallydependon theunknown
ages at initialrelease(R. Morton,personalcommunication), so some modification is
required.Verysimplechoiceswhichwehavefoundto workreasonably wellin simulations,
andwhichareconsidered intherestofthispaper,arehii1 andh2i =Li, givingestimating
equations
1=Ei=0 and g = A Lri = O. (6)
Theseequationsrequirethatnot all Ai be equal, whichwillgenerally be the practical
andwhichwillbe assumedhenceforth.
situation, We conjecture thatifL is allowedto vary
between thenidentifiability
individuals, problems preventconsistent distribution-free
esti-
mationoftheparameters ifAi= i\forall i.
Sinceg1and g2are sumsofindependent, non-identicallydistributed
randomvariables,
theywill,aftersuitablestandardisation,
be asymptotically bivariatenormalprovidedthe
standardisedtermsin thesumsbecomeuniformly asymptoticallynegligible (Rao, 1973,p.
128),whichin practicedemandsthatno smallnumberofrecapture intervals Aidominates
therest.Generalestimating equationtheory[see,forexample,Maritz(1981, ?1.7)] may
thenbe used to showthatthe estimators Ko and Lo are consistentand asymptotically
normally distributed
undermildconditions, withcovariancematrix
C = E(G)-'DgE(GT)-',
where

G-= (g1/0K0 0g1/0LoA\

\0g2/OKo0g2/OLo,/

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 Estimation
ofGrowth
fromRecaptures 1523
and Dg is thedispersion
matrixof(g1,g2).The observedG withparameters
estimated
and
theestimate

Dgf E i~
"~<
tiZ\2 Z2

can be used to provideestimates of C. If a restricted

varianceformsuchas (4) or (5) is
assumed,thentailoredmodifications of Dg mayprovidemoreprecision,althoughour
limitedsimulation experience suggests thatanygainsare smalland thegenerality is lost.
Generalizationto otherfunctions hi and h2is clear.
It shouldbe notedthattheseresultsare asymptotic and approximations maybe poor
withsmallsamples.Indeed,itis possiblefortheestimating equationsto haveno solution,
iftherecapture
particularly intervalszAiare small.Thisis evidencedin thesimulations in
Section3, and it wouldgenerally indicatean attemptto estimateparameters froman
inadequatedataset.Mallerand deBoer(1988) notedthatleastsquaresmethodsmayalso
failto havesolutionsin thelegitimate parameter space.
Jointconfidence regionsfortheparameters Ko andLo, and testsofhypotheses regarding
theseparameters, maybe basedon theasymptotic normalityofg1andg2in theusualway
forestimatingfunctions providedsamplesizesarelarge.
In additionto estimationofthemeanLo, itwilloftenbe usefulto estimate thebetween-
animalvariance(2 . Thiscan be readilydone ifit is assumedthattheresidualvariances
are smallbycomparison witha2, so that(4) is a goodapproximation. The varianceofL
can thenbe estimated approximately by

1= n' ';i/[1 - exp(-KRo ,)]2. (7)

2.4 Distribution
ofAgeat FirstRelease
The ages at firstreleaseare regardedas fixedquantitiesin (2). However,one mightalso
wishto considerthedistribution oftheseages,regardingt1as a randomvariable.Assume
thatt1and L areindependent. Thenfrom(2) it followsthat
E = E[exp(-Koti)] = 1 - E(yi)/Lo,
whereE(y1) is no longerconditional
on ti. If,in addition,thevarianceoftheresidualsis
smallbycomparison withCL, then
V = var[exp(-Kot1)] E(yI L)/(c2 + Lo) - [E(y1)/Lo]2.
The meanand varianceoft1can be approximated
undertheseconditions
by
E(ti) ~V/(2KOE2) - log(E)/Ko, (8)
var(t1) V/(KoE)2.

andSimulations
3. Computation
Jointsolutionof 'I = 0 and g2 = 0 can be readilycarriedout by a varietyof numerical
methods.One approachis to solveforLo in termsofKo fromgl followed by substitution
intog2,thusconvertingtheiterativesearchto onedimension.A simplegraphicalapproach
in whichbothg2 and Lo are plottedas functions of Ko can thenbe implemented, or a
bisectionmethodcan be used.Alternatively, we havefoundit quiteefficient
and easyto
programa simpleNewtontwo-dimensional method.Typicallyonlyfouror five
iterative
iterations
are neededto achievea highdegreeofaccuracyfromreasonablestarting values.

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1524 Biometrics,December 1991
A comprehensive simulationanalysisof the estimationmethodbased on (6) is not
attempted here.Insteadwe investigate itsperformance in twosituations withparameters
thatreflectapproximatelythegrowth patterns in western rocklobstersand in whelks.
FollowingMallerand deBoer(1988),thegrowth ofwestern rocklobsters was simulated
bychoosingtheparameter Ko to be fixedat .0007,and L normally distributed
withmean
115 mm and standarddeviation10 mm. The growthfora singlelobsterwas assumed
deterministiconce itsparameters werechosen.Four combinations of distributions
of t1
and l\weregenerated. The distribution
oft1wastakenas uniform from360 daysto 1,080
days,or from720 daysto 1,440days,whilethez? weregenerated uniformly from30 days
to 360 daysor 30 daysto 1,080days.
Thewhelkshelllength parameters werebasedon thoseestimated forthewhelkDicathais
aegaota byPalmeretal. (1991).Parameter Kowasfixedat .0015,L wasnormally distributed
withmean 50 mm and variance30 mm2,and residualsei and C2 wereindependently
generatedwithmean zero and variance2. Recapturetimeswere as forthe lobster
simulations,whiletheagesat firstreleasewereuniform from100daysto 500 daysorfrom
300 daysto 1,000days.
In bothsetsof simulations, samplesizes of 200 and 500 wereconsidered, and 200
replicationsweregenerated foreach set of parameters. Estimateswereobtainedby the
bisectionmethodto avoidanyproblems withstarting values.
The resultsofthesimulations are givenin Tables 1 and 2, whereforcomparison the
estimatesobtainedfromFabens'(1965) methodarealso shown.The methodbasedon (6)
givesestimateswithlargestandard errorsiftherecapture intervals
aresmall,butitperforms
extremely wellwhenrecapture intervalsvaryoverthewiderrange.Notethat(6) relieson
variationin thezAi
to ensurethatgl andg2differ. It is instructive
to notethesmall"range"
of the growthcurve fromwhichdata are availableforestimationin some of these
simulations.For instance,
thelobstercurvetakesapproximately 3,300daysto reach90%
ofitsasymptotic value,whilewe areconsidering recapture timesbetween30 and 360 days.
In addition,forthesmallerages at firstrelease,thesedata are concentrated towardsthe

Table 1
Simulationsofwestern
rocklobster
growth.In eachcase L - N( 115,100),Ko= .0007,and 200
replications
weregenerated.
U(a, b) denotestheuniformdistribution
on(a, b). Entriesare inthe
ordermeanfrom(6), SE, meanfromFabens'method, SE
n = 200 n = 500
U(30, 360) U(30, 1,080) U(30, 360) U(30, 1,080)
t, ko LO ko Lo ko Lo ko Lo
U(360,1,080) .00073a 125.5 .00072 114.8 .00070 119.1 .00069 115.9
.00029 45.9 .00011 8.8 .00018 20.1 .00006 4.9
.00046 148.5 .00048 140.6 .00046 148.6 .00048 139.8
.00005 10.4 .00005 9.6 .00003 6.5 .00003 5.2
U(720, 1,440) .00082b 121.2 .00071 115.6 .00074 117.7 .00071 115.0
.00049 31.7 .00012 7.4 .00025 19.4 .00007 4.5
.00029 188.1 .00030 171.7 .00029 187.3 .00031 168.7
.00005 21.9 .00005 17.2 .00003 12.5 .00003 9.5
a 3 caseswithno solution.
b2 caseswithno solution.

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 EstimationofGrowth
fromRecaptures 1525
Table 2
Simulations
ofwhelkgrowth.In eachcase L - N(50, 30), Ko = .00 15, C, C2 N(0, 2) and 200
replications
weregenerated.
U(a, b) denotestheuniform distribution on(a, b). Entriesare inthe
ordermeanfrom(6), SE, meanfromFabens'method, SE
n =200 n = 500
U(30, 360) U(30, 1,080) U(30, 360) U(30, 1,080)
ko Lo ko Lo ko Lo ko Lo
U(100,500) .00159a 56.4 .00150 50.3 .00148 52.5 .00149 50.2
.00068 29.9 .00016 2.2 .00038 8.7 .00010 1.3
.00124 56.2 .00120 54.7 .00125 55.5 .00120 54.5
.00018 5.0 .00013 2.6 .00010 2.8 .00008 1.5
U(720, 1,440) .00187b 55.3 .00152 50.3 .00152c 56.7 .00152 50.0
.00117 21.2 .00029 2.3 .00072 22.6 .00016 1.3

.00106 57.2 .00090 57.8 .00104 57.4 .00091 57.4

.00014 3.6 .00011 2.5 .00009 2.2 .00008 1.6
a
4 cases with no solution.
b 18 cases with no solution.
3 cases with no solution.

beginning ofthegrowth curve.The largestandard reflect

errors in estimating
thedifficulty
bothKoand Lo undertheseconditions.
As notedby Sainsbury (1980) and Mallerand deBoer(1988),Fabens'methodtendsto
producebiasedestimates, withKo typicallyunderestimatedand Lo overestimated,though
estimates aremuchlessvariablethanfrom(6) whentherangeoftherecapture intervalsis
small. Relativelystable,thoughinconsistent, estimators
are obtainablefromFabens'
methodevenwhenall A\i areequal (Mallerand deBoer,1988),and thisstability
is reflected
in the simulations. Fabens' methodwouldbe expectedto becomeless biasedforsmall
initialagesat release,whentheeffect ofYi in theestimating
functionf2is small,and when
variationin L and theresidualsis small.
Whentherecapture intervalsAi are small,theestimator Lo from(6) tendsto be very
skewedtotheright, as showninFigure1,whichgivesnormalQ-Q plotsforthestandardised
statistics(Ko - K0)/est.SE(Ko) and (Lo - Lo)/est.SE(Lo) forfoursimulationsof the whelk
data. The normalapproximations are quitereasonablewhenthe A\i varyoverthewider
range,and thestandardised Ko estimator is betterbehaved. Correlations
betweenKo and
Lo are typicallyvery high, as illustrated in the scatterplotsof parameterestimatesin
Figure2. The relationship betweenLo and Ko is relatively linearwhentheAivaryovera
widerangeofvalues.However,whentheA\i aresmall,a strongcurvedrelationship
persists,
variabilityis high,and, as notedabove,Lo has considerable skewnessto theright.This
skewness maybe anticipated fromtheinverserelationship obtainedwhenLo is solvedin
termsof Ko fromgi = 0.
As a comparison, thecorresponding scatterplotsforFabens'methodare also givenin
Figure2. Mostnotableis thesimilarity in scatterofthepointcloud,anditsbiasin location,
whentheA\i varyoverthewiderrange,and thecompactness ofthepointcloudrelativeto
(6) whentheAiaresmall.
Reparameterisation alongthe linesdiscussedby Ratkowsky (1986) mightbe used to
produceparameters whoseestimators from(6) are betterapproximated by normality,
thoughthehighvariability willpersistifthez\iaresmall.

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 1526 Biometrics,
December1991
(a) (a)
3 3 I I

2 2

0 /7
x --

-2 -2

3 3 l ll-3
-3 -2 -1 0 1 2 3 -10 -5 0 5

Standardised K estimate Standardised L estimate

w 1~ ~ ~~~~~U -1-
(b) (b)
3
-

2 2

0
Cd)
0~~~~~~~ u
J
L

-2 -2

-4 -2 0 2 4 -4 -2 0 2 4

Standardised K estimate Standardised L estimate

Figure1. Q-Q plots of standardised estimatesfrom(6) forsimulatedwhelkdata, n 500,

Lo= 50, a'l (a) t1 -U(100, 500),A U(30,360);
30, Ko0 .0015, el, E2 -N(0, 2) (seetext).
(b) ti -U(300, 1,000),A -U(30, 1,080).

4. WhelkData

Phillipsand Campbell(1968) analysedgrowthin shelllengthofthewhelkDicathaisaegaota

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 ofGrowth
Estimation fromRecaptures 1527
(a) Method(6) (a) Fabens'method
150 150

100 100

E
u_
50 50

o 0
0.000 0.001 0.002 0.003 0.000 0.001 0.002 0.003

Estimate of K Estimate of K

(b) Method
(6) (b)Fabens'method
65 65 I

60 60

0 :j

on 555
55

50 ..;50

45 I-
45
0.0005 0.0010 0.0015 0.0020 0.0025 0.0005 0.0010 0.0015 0.0020 0.0025

Estimate of K Estimate of K

Figure 2. Scatterplotsofparameter
estimates forsimulatedwhelkdata,n= 500,Lo = 50, fo=30,
Ko = .0015,
el, C2 N(O,2) (seetext).(a) the U(100, 500),A -eU(30,360);(b) t1 - U(300, 1,000),
A -U(30, 1,080).

applyestimationmethod(6) to thisextendeddata set.The data consistof measurements

on 539 whelks,all of which were recapturedat least twice afterinitial release, with a
maximumnumberof 14 recaptures.Since themethodoutlinedabove is designedforsingle
forillustrative
recaptures, purposestherecapture intervalsweretakenas (i) thetimefrom

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1528 Biometrics,
December1991
medianrecapture interval
was 150days,witha rangeof30 daysto 1,368days,themean
initiallengthwas29.5 mm,and themeanfinallengthwas 34.3 mm.For(ii),therecapture
intervalsrangedfrom30 daysto 2,256days,witha medianof 426 days,whilethemean
finallengthwas 39.1 mm.
Estimates and standard
errorsbasedon (6) aregivenbelow:

(i) Shortest
recapture
interval interval
(ii) Longestrecapture
Ko Lo Ko Lo
Est. .0014 49.6 Est. .0014 49.8
SE .00063 7.92 SE .00014 1.21

The estimatesaresimilarin thetwocases,butthestandard errorsaresignificantlysmaller

usingthelongerrecapture times,as expectedfromsimulations. The estimates for(Ko,Lo)
usingFabens'methodare respectively (.0013,50.3) and (.0012,50.8). For thesedatathe
estimatesare verysimilarto thosefrom(6), withKo slightly lowerand Lo slightly higher,
in accordancewiththedirections ofbiasesnotedearlier.
Palmeret al. (1991) obtainedestimates of48.9 mmand .002 forLo and themeanofK
fromtherandomcoefficients model.Theirmethodusedall oftherecapture data.
Using(7), thestandarddeviationof L is estimated as 16.3 mm fromdata set(i), and
12.9mmfromdata set(ii). Theseestimates differ
considerably fromtheestimateof 5.56
mmobtainedbyPalmeret al. It shouldbe remembered, however, that(7) does notallow
forvariationin K or theresiduals,and willgenerallygivean overestimate.
Based on approximations (8), estimatedmean age at firstreleasewas 672 days,with
standarddeviation122days.

5. Extensionsof the Method

5.1 RandomK
In thepreceding discussionK has beenassumedconstantfromanimalto animal.IfK is
randomwithmeanKo and variancea2 > 0, thenE(,qi)$ 0. It willtypically be thecase,
however,that U2 is smallby comparisonwiththe varianceof qj, so thattheestimating
functionswillstillbe approximatelyunbiased.No comprehensive analysisoftheapproxi-
mationis attempted here,buttheeffectsare illustrated by somesimulations.
briefly For
thesetheparameters werechosenas forthewhelkdatain Section3 withsamplesize 500,
t1uniformlydistributed over300 daysto 1,000days,and l\uniformlydistributed
overthe
range30 daysto 1,080days.The asymptotic lengthparameter L was normalwithmean
50mmandvariance30 mm2,andtheresiduals werenormalwithvariance2. K wasnormal
withmean.0015 and standarddeviations(i) .00025 and (ii) .0004. Mean estimatesand
standarderrorsfrom200 replicates wereobtainedas below:

(i) SD(K) = .00025 (ii) SD(K) = .0004

Ko Lo Ko Lo
Mean .00150 49.72 Mean .00148 49.14
SE .00018 1.509 SE .00019 1.590

Whilstfurther
investigation
oftheeffectsofrandomK iswarranted,
theseexamplesindicate
thatevenquitehighrelativevariation
in K maynotundulybiastheestimates.

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 ofGrowth
Estimation fromRecaptures 1529
5.2 MultipleRecaptures
Withmultiple recaptures equationscan takemanydifferent
theestimating forms.Suppose,
forexample,thateachanimalis subjecttotworecaptures, givingmeasurements, in obvious
AIi = t2i - tli, A2i = t3i - tli. In thiscase natural
notation,yli, y2i, y3i, and increments
estimatingequationswouldappearto be similarto
Enli = 0 and En2i= ?,

where
77li = y2i - yli - (Lo - yiv)[l - exp(-Ko Ali)],
72i = Y3i - Yli - (Lo - Y1i)[l - exp(-K0A2i)].
Our limitedexperiencewiththeseequationssuggests to have n
thatit is moreefficient
animalswithtworecaptures than2n animalswithsinglerecaptures overthesame time
span,as mightbe expectedgiventhatestimatesofcurvature and asymptoteare required.
Notethatwithtworecaptureswecan allowall animalstohavethesamerecapture intervals.
Withmorethantworecaptures, or withunequalnumbersperanimal,theconstruction
ofappropriate equationsis notclear.Withmultiplerecaptures,
estimating theindividual
growthcurvesmaybe estimated,thusproviding muchmoreinformation thanis available
fromsinglerecaptureswithunknownages of release.These issueswill be addressed
separately.

6. Discussion
The estimation methodbased on (6), or modifications usingotherfunctions hi and h2,
appearsto overcometheproblemsofinconsistency inherentin theleastsquaresmethods
ofestimation in thevon Bertalanffygrowth modelfromsingle-recapture data.It willgive
parameter estimates withconsiderablevariationand skewness, or possiblyno solutionat
all,ifrecaptureintervalsvaryovera smallrange,butthismaybe a desirablewarning that
toomuchis beingexpectedofthedatainthatcase.The methodis verysimpleand requires
fewmodelassumptions.
Thereare severalaspectsofthemethodneedingfurther work,however.Theseinclude
moreprecisestudyof asymptotics, choiceof optimalestimating functions, methodsof
handling mixedmultiple-recapturenumbers, and theeffectsofrandomK. In particular, it
willbe important to seeifmodifications
ofgl andg2 thatretaintherelatively lowvariation
ofFabens'method,whilstalso correcting forbias,can be foundforsmallAi.Otherissues
to considerincludetheincorporation ofcovariatesin a generalwayand possibly theuse of
morerobustequations.

ACKNOWLEDGEMENTS

RossMallerbrought theestimation problemstudiedhereto myattention,

and hasassisted
withmanyhelpfuldiscussions. PermissionfromDrs BrucePhillipsand NormCampbell
to use thewhelkdata is gratefully
acknowledged.MarkPalmerprovidedpreprints of his
workand examplesofappropriate data.Thisworkwaspartially
supportedbya University
ofWestern SpecialResearchGrant.
Australia

RESUME
Une methodesimplepour construire des fonctionsd'estimationdes parametres
du modelede
croissance E[Y(t)]= L[1 - exp(-Kt)]estpresentee
de vonBertalanify pourdesdonneesdemarquage-
recapture
quandl'agede l'animalestinconnu.Les fonctionsd'estimationsontnonbiaiseessousdes

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1530 Biometrics,
December1991
hypotheses distributionnelles
tresgenerales
pourvuque K nevariepasentreanimaux.Des simulations
de croissancede Homardset de Buccinsindiquent que la m&thode se comportecorrectementsi les
tempsde capture de recapture
etlesintervalles surdesdomainesraisonnables.
varient La comparaison
est faiteavec les methodesbaseessur les moindrescarres,donton sait qu'ellessonten general
inconsistantes.

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ReceivedJune1989;revised
December1989andMay 1990;accepted
August1990.

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