803

RestingandPeakMetabolicRatesof ArcticTern
NestlingsandTheirRelationsto GrowthRate
Marcel andClausBech2
Klaassen',*
1DLOInstitutefor Forestryand NatureResearch(IBN-DLO),P.O. Box 9201,
NL-6800HB Arnhem,The Netherlands;2Departmentof Zoology, Universityof
Trondheim, N-7055 Dragvoll, Norway

Accepted 2/4/92
Abstract
We measured resting and peak metabolism in relation to growth rate in arctic
tern Sterna paradisaea chicks over the first 10 d after hatching. For chicks with
varying growth rate, body mass seems to be a better predictor of resting metabolic
rate than age. The effect of changes in growth rate on resting metabolism of arc-
tic terns is smaller than that found interspecifically in hatchlings. It is possible
that differences exist in the heat increment offeeding between fast and slow
growers that would further reduce the effect of growth rate on resting metabolism.
Chicks that had body masses lower than 75% of that expected for their age were
metabolically inferior in withstanding a thermal challenge compared with chicks
of the same age but of normal mass. In contrast to resting metabolic rate, the ex-
tent of peak metabolic rate is related to both body mass and age. Thus, in part,
the maturation of the thermoregulatorji system proceeds steadily with time even
when body mass lags behind.

Introduction

Several seabird species display considerable intraspecificvariationin field

growth rates (e.g., Langham1972; Lemmetyinen 1972; LeCroyand LeCroy
1974; Becker and Finck 1985; Coulson and Porter1985; Becker and Specht
1991; Klaassenet al. 1992). In a laboratorystudy on common terns, Sterna
hirundo, and sandwich terns, Sterna sandvicensis, Klaassen et al. (1992)
concluded that the energy requirements for development were strongly
dependent on growth rate. In both species, the slowest-growing chicks
needed 24%less energy over the total developmentalperiod thanthe fastest-

* Present
address:
MaxPlanck
Institut D-W-8138
furVerhaltensphysiologie,
Vogelwarte, Federal
Andechs, Re-
ofGermany.
public

Physiological
Zoology 1992.c 1992byTheUniversity
65(4):803-814. ofChicago.
Allrights
reserved.
0031-935X/92/6504-9179$02.00
804 M.Klaassen
andC.Bech

growing conspecifics. Also, maximumgross energy intake,which is reached

at a certainday duringdevelopment, was 37%lower for the slowest growers.
These differences in energy requirement between fast and slow growers
were explained by energy savings in maintenance metabolism and heat
increment of feeding due to the smaller food intake. However, extra energy
savings might also originate from growth-rate-dependentdifferences in
resting metabolism as found interspecifically (Drent and Klaassen 1989;
Klaassen and Drent 1991). The question arises whether this interspecific
finding also applies to intraspecificdifferences in growth rate.
Assuming a close coupling between basal or resting metabolism and
working capacity,as has been suggested for both adult birds (Brody 1945;
Drent and Daan 1980; Kerstenand Piersma 1987; Daan, Masman,and Gro-
enewold 1990) and chicks (Drent and Klaassen 1989; Klaassenand Drent
1991), a decrease in basal or resting metabolism with decreasing growth
rate should also be accompanied by a decrease in peak metabolism (i.e.,
thermogenic capacity).This might underlie some of the mortalityassociated
with reduced growth rates in nestlings (e.g., terns: Langham1972; Lem-
metyinen 1972; LeCroyand LeCroy1974; Becker and Finck 1985; Becker
and Specht 1991).
To test the hypothesis that resting and peak metabolism relate directly to
growth rate, we measured these parameters in arctic tern chicks, S. par-
adisaea, over the first10 d afterhatching. Chicksof these ages lack sufficient
thermogenic capacityto maintainbody temperatureat the lowest prevailing
ambient temperatures(in the absence of brooding parents) (Klaassenet al.
1989a; Klaassen,Bech, and Slagsvold 1989b).

Material
andMethods

The study was carried out in the arctic tern colony of Ny Alesund, Spits-
bergen, (790N, 120E) duringJuly and August 1990. The colony was visited
regularly,and individuallymarkedchicks of known age were weighed with
a Pesola spring balance. Forty-sevenchicks were taken from the field and
transportedto a nearbylaboratory.Metabolicmeasurementswere conducted
in an open-flow indirect calorimeter. In this system air was drawnthrough
a 2-Ltemperature-controlledmetabolic chamberat a flow rate between 135
and 330 mL/min depending on the size of the chick. The effluent air was
dried with silica gel afterwhich flow and oxygen concentrationwere mea-
sured (with an Applied ElectrochemistryS3A). In the calculationof oxygen
consumption (Vo2) (Hill 1972), we corrected for CO2production using a
 Arctic
Tern
Chick
Metabolism
805

respiratoryquotient earlier measured in arctictern chicks of 0.70 (Klaassen

et al. 1989b).
Afterbeing collected from the field, the chick's body mass was firstmea-
sured to the nearest 0.1 g. Formeasuringbody temperaturea thermocouple
was inserted into the cloaca and kept in place by taping the thermocouple
wire to the rectrices.The chick was then placed in the brassmetaboliccham-
ber. Direct cooling of the chick by the metal jacketwas prevented by a thin
rubber layer on the floor of the metabolic chamber.The initial air temper-
atures were 360C for the smallest and 31'C for the largest chicks, which
were thermoneutraltemperatures.After 1.5 h at thermoneutrality,the am-
bient temperaturewas decreased at a constantrate of 0.20C/min. When the
chick was exposed to ambient temperaturesbelow thermoneutrality,body
temperatureslowly decreased and Vo2 increased.When the chick could no
longer cope with the ambient temperature,thatis, when Vo2 decreased and
body temperaturestartedto decrease sharply,the experiment was stopped
and the chick was removed from the chamber. The chick's body mass was
again measured, and then it was returnedto the field after rewarming.The
body mass used in calculatingthe mass-specificmetabolic ratewas the mean
of the initial and final mass (the averagebody-massdecrease during exper-
iments was 8.0%;SD = 4.7%, n = 47). Each chick was only used once for
metabolic measurements.
During the experiments, ambient temperature,body temperature,and
Vo2were recordedcontinuouslyon a datalogger (GrantSquirrel,type 1203).
Afteran experimentalrun,all datawere transferredto a computerfor analysis.
As the metabolic measuringsystem had a delay and mixing effect as a result
of the relatively large volume and low flow rates used, instantaneousVo2
rates were calculated with equations given by Niimi (1978). We defined
resting metabolism as the lowest mean rate of Vo2 over a 20-min period
when the chicks were subjected to thermoneutralconditions. We abstain
from referringto these minimum metabolism values as basal metabolic rate
because we do not know whether chicks were completely postabsorptive
during physiological measurements. Peak metabolism was defined as the
highest meanVo2over a 20-minperiod duringexposureto subthermoneutral
temperatures.Forfive birds,ambient temperatureof the metabolic chamber
could not be lowered sufficientlyto induce a peak metabolic rate (PMR).

Results
A logistic equation (Ricklefs 1967) was fitted to the field measurements of
body mass, describing average or expected body mass (mexp, g) with age
(d, in days):
806 M.Klaassen
andC.Bech

116.6
mexp 1+ (1)
10.3e-0.254d

Forthe individualchicksin the metabolicexperimentsan indexof growth

rateis obtainedby calculatingthe residualbody mass (mes, %),which is
the deviationof the bodymass(m, g; fig. 1) fromthe expectedbodymass
for thatage (eq. [1]):

m- mexp x 100.
mres = (2)
mexp

However, for very young chicks, with low expected body masses, the cal-
culated mres is very sensitive to small changes in m. Therefore, we did not
include mres for chicks younger than 3 d of age in our analysis. Chicks
sampled for the metabolic experiments usually had growth rates below av-
erage (fig. 1); consequently, their mres's were on average below zero and
ranged from -57% to 40%.
As found in arctictern chicks before (Klaassenet al. 1989b), the relation
between mass-specificresting metabolic rate (RMR,mL 02/g- h-1) and m
is best described by a parabolicfunction (fig. 2). Therefore,a second-order
polynomial was fitted through the data to describe RMRas a function of

70
60- O

S40-

o o 8

30
20 O
0

0
110-
0- -0

0 1 2 3 4 5 6 7 8 9
Age (days)

Fig. 1. Body mass of the chicks used for experiments in relation to their
age (day of hatching is day 0). Closed symbols are the chicks that did not
reach the age offledging after being returned to the field. Solid line is the
mean growth curve for all chicks in the same colony (eq. [1]), which is
used as a reference. Broken line indicates 75% of the expected body
mass at a certain age.
 ArcticTernChickMetabolism807

5-

3 *
3
o

2 2-

10 20 30 40 50 60 0 1 2 3 4 5 6 7 8 10
BodyMass(g) Age (days)

Fig. 2. Resting metabolic rate as a function of body mass and age. The
lines are drawn according to the equations in table 1.

mass (table 1). Alternatively,RMRcan also be expressed as a function of

age (fig. 2). For our data, a linear function proved to be appropriatefor
relatingRMRto age (table 1). The RMRresiduals(RMRres, %)were calculated
according to the equation:

RMR - RMRex
exp 100, (3)
RMRres=
RMRexp

where RMRexpis the expected RMRas a function of either m (mass based)

or age (age based) (table 1). Both mass-basedand age-based RMRres's are
positively related with the mres's (fig. 3; table 2). However, the slope of the
relation relating age-based to mres'sis 3.5 times higher than that
RMRres's
for the mass-basedmres's.

TABLE1
Least-squares relations of resting metabolic rate (RMR, mL 02/g * h-')
andpeak metabolic rate (PMR, mL 02g * h-') with age (d, in days)
and body mass (m, g)

Equation r2 SE P n

RMR = .018 + .1409m - .00148m2 ..... .694 .441 <.001 47

RMR = 1.749 + .1935d ............... .366 .628 <.001 47
PMR = -2.356 + .4527m - .00521m2 ... .821 .862 <.001 42
PMR = 2.528 + .7030d ............... .555 1.344 <.001 42

Note.Theinclusionsof m2in the equationswithmweresignificant(P < .001)forboth

RMR (t = -3.897) and PMR (t = -4.537), whereas the inclusions of d2 in the equations with
d were not (t = -0.684, P = .498 and t = -0.621, P = .538, respectively).
808 M.Klaassen
andC.Bech

50 mass-based

40

30

20

10

0
-30
-60 -50 -40 -30 -20 -10 0 10 20 30 40 50
60 age-based

50

40

20

10

- 10

-20

-30

-40

-50
-60 -50 -40 -30 -20 -10 0 10 20 30 40 50
Body Mass Residual(%)

Fig. 3. Association between residuals of both mass- and age-based RMR

and body massfor chicks older than 2 d of age. The least-squareslinear
regression lines are drawn (table 2).

LikeRMR,mass-specificPMR(mL 02/g h-') is also parabolicallyrelated

to body mass and linearly related to age (fig. 4; table 1). The PRMresiduals
(PMRres, %), calculated in a fashion similar to thatfor RMRres's (eq. [3]), are
shown in relation to the mes's in figure 5 and table 2. Below mres of ap-
proximately -25%, mass-based PMRres's tend to varya lot and are very low
in some individuals (fig. 5). However, for mres'sabove -25%, there is a
significant negative relationship between mass-based PMRres's and mres's
(table 2). Also, in the case of the age-based PMRres's, values associated with
mresof less than -25% were, on average,significantlylower than those above
-25% (-52.6%, SD = 2.8%,n = 5 and 10.7%,SD = 12.0%,n = 27, respec-
tively; t = 11.6, P < .001). However, in contrastto the negative correlation
between mass-basedPMRres's and mres's,for mres'sabove -25%, the age-
based PMRres's arenot relatedwith the mres's(table2).
When omitting data points with mres'sbelow -25% in the analysis of
RMRres's as well, this would still result in a significantrelation between age-
 Tern
Arctic Chick 809
Metabolism

TABLE2
Least-square regression of resting metabolic rate residuals (RMRres,%)
and peak metabolic rate residuals (PMRres,%) on body mass residuals
(mres, %)

Equation r2 SE P n

Mass-basedRMRres= -1.939 + .222mres .107 15.505 <.048 37

= .763 + .777mres .......
Age-based RMRres .531 17.703 <.001 37
Mass-basedPMRres= 6.375 - .417mres .... .392 10.675 <.001 27
= 9.270 + .196mres
Age-based PMRres .108 11.598 =.094 27
......
Note. Restingand peak metabolic rate residualswere calculatedaccordingto eq. (3) using
both the mass and age-basedrelationsof RMRand PMR(table 1). For PMRonly datapoints
with a higher than'-25% m,eswere included in the analysis.

based RMRres's and mres's(r2 = .284, n = 31, P<.005). The relation between
mass-based RMRres's and mres'swould become nonsignificant (r2 = .028, n
= 31, P = .368). However, in the discussion below we argue, and present
evidence, that the physiology underlying peak and resting metabolism are
not developing in pace and should thus not necessarilybe treatedin parallel.

Discussion
RestingMetabolic Rate
We hypothesized that basal metabolism is related to chick growth rate in-
traspecifically.This hypothesis is based on the finding that such a relation

10-10

7
7- -

4.

3 O3

2.
2-

0 0
10 20 M
0 4o 5o 0 1 2 4 5 a 7
BodyMass (g) Age (days)

Fig. 4. Peak metabolic rate as a function of body mass and age. The lines
are drawn according to the equations in table 1.
810 M.Klaassen
andC.Bech

exists interspecificallyin avianhatchlings(Drentand Klaassen1989;Klaassen

and Drent 1991). The relation of growth rate to resting metabolism seems
to be largely comparableto thatfound interspecificallyin hatchlings (Drent
and Klaassen 1989; Klaassen and Drent 1991). In this study, the slopes
relating relative resting metabolism to relative growth are 0.22 and 0.78 for
mass- and age-based resting metabolism respectively (table 2). The slope
found interspecifically for mass-based resting metabolism with relative
growth rate for hatchlingswas 0.38 (Klaassenand Drent 1991).
However,althoughwe found a positive relationbetween RMRand growth
rate in our study (fig. 3; table 2), it does not support unconditionally the
hypothesized relationbetween basal metabolism and growth rate.A further
complication is that the heat increment of feeding may be higher in fast-
growing versus slow-growing chicks. Since the chicks used in the experi-
ments had not been fasted before measurement, we cannot exclude the
possibility thatthe barelysignificantrelationshipbetween RMRand growth
rate (table 2) is due mostly to the heat increment of feeding. For arctictern
chicks fed ad lib., the heat increment of feeding is approximately1 mL02/
g* h-1 throughout development (Klaassen et al. 1989b). According to the
equations in table 2, we expect a difference in RMRres between chicks with
mres of -57% and 40%(the values for the slowest and fastest growers in our
study, respectively) of 22% and 75%, when RMRis mass based and age
based, respectively. Resting metabolic rate varies between 1.5 and 3 mL
02/g h-1 (table 1; fig. 2). Thus, even if we assume that the slowest grower
is completely postabsorptiveand the fastestis well fed, the 1.0 mL02/g * h-
difference expected for differingplanes of nutritiondoes not account fully
for the age-based RMRdifferences for the two groups. However, if such
differences in heat increment of feeding exist, the small slope detected
between mass-based RMRresand mres is not persuasive for the existence of
a link between intraspecificbasal metabolic rate and growth rate.
Thus, when seeking to answerwhether basal metabolism and growth rate
are linked, a criticalconsiderationis whetherthe predictedrestingmetabolic
values used for comparison should be expressed as a function of age or
body mass. For the moment, no other studies have been done that resolve
this dilemma. We do note that m explains more of the variationin mass-
specific resting metabolism (69%) than does age (37%, table 1) and that
the mres's explain less of the residual variationin resting metabolism when
it is mass based (11%) than when it is age based (53%,table 2).
In conclusion, when growth rate varies, m is a better predictorof resting
metabolism than age. Also the relation between mass-based RMRres'sand
mres's does not support our hypothesized relation between basal metabolic
rate and growth rate owing to possible differences in heat increment of
 Arctic
Tern Metabolism811
Chick

feeding between chicks. Even if our measurementswere not influenced by

differencesin heat incrementof feeding between fast and slow growers,the
effect of growth rate on resting metabolism is smaller than thatfound inter-
specificallyin hatchlings(Drentand Klaassen1989;Klaassenand Drent1991).
Klaassenand Drent (1991) hypothesized that the interspecific relation
between growth rate and basal metabolism results from a careful tuning of
both parametersin the course of evolving an optimal ontogenetic strategy.
The present study shows that the ontogenetic design of these chicks, with
a fixed ratio between growth rate and basal metabolism, allows little ad-
justmentwhen chicks encounter unfavorableconditions.

Peak MetabolicRate
From the present data it seems as if there is a threshold at approximately
-25% of average growth below which chicks are metabolically inferior in
resisting a thermal challenge (fig. 5). Chicks with mres lower than -25%
were more likely to die afterbeing returnedto the field, as only few of these
chicks reached the age of fledging (fig. 1). Lack(1968) advocatedthe view
that brood size and growth rate are tuned to match the working capacityof
parentsin the course of evolution. Thus, each species has its own specific,
evolutionarilyset, posthatchgrowthrate.Nevertheless,it is clearthatspecies-
specific growth does not preclude that individual chicks have different
growthrateswithin boundariesset by physiologicalconstraints.Forreduced
growth rate, the present data provide such a physiological limit. From a
thermoregulatorypoint of view, growth rates less than 75%of normalresult
in a tendency for chicks to experience hypothermia.
Differentresults were found between age-basedand mass-basedPMRres's
in relation to mrs,,'shigher than -25%. Where mass-basedPMRres's showed
a negative correlation,age-based PMRres's were not significantlycorrelated
with mres's(table 2). This disparity,between the mass-basedand age-based
PMRres's in relation to the mr,,'s,points to an independence between body-
mass growthand the development of the thermoregulatorysystem with age.
If body mass and the thermoregulatorysystem should develop in pace,
there should be a positive, and not a negative, relation between m and
PMRes's. Thus, although m lags behind in the slow-growing chicks, the
thermoregulatorysystem continues to develop (at least in part) in these
chicks with increasing age.
In an arrayof bird species, the ratio between basal metabolic rate and
maximum sustained working level is stable in adults (Brody 1945; Drent
and Daan 1980; Kerstenand Piersma1987;Daanet al. 1990). Also in chicks,
there is a relationbetween basal metabolic rateand peak metabolism (Rick-
812 M.Klaassen
andC.Bech

50 mass-based

40

30

20

-10

CV -10
S
-20

-30

-40

-50
-60 -50 -40 -30 -20 -10 0 10 20 30 40 50

40 age-based

30

20

10

-10

-20

-30

-40

-50

-60
-60 -50 -40 -30 -20 -10 0 10 20 30 40 50

Body Mass Residual(%)

Fig. 5. Association between residuals of mass- and age-based PMR and

body mass for chicks older than 2 d of age. For chicks with m,es higher
than -25% the least-squares linear regression lines are drawn (table 2).

lefs 1989;Drentand Klaassen1989). The relationbetween these high levels

of energy expenditureandbasalmetabolismcan be understoodif we assume
that a change in working capacitynecessitates a rescaling of the metabolic
machineryprovisioningthe animal. Studieson the relationbetween animal
composition and basal metabolism (Koong, Nienaber,and Mersmann1983;
Daan et al. 1989, 1990) give support to the idea that these changes in the
metabolic machinery(including organ size) result in changes in basal met-
abolic rate. Thatthe close coupling between peak and basal metabolic rate
also holds intraspecificallyis not supported by the data presented, at least
not for chicks; it may yet hold for intraspecificdifferences among adults.
Fromfigures 3 and 5 and the equations presented in table 2, it is clear that
for chicks with a growth rate higher than 75%of averagegrowth, the ratio
between peak and resting metabolism declines with increasinggrowth rate.
Thus, the coupling between basal and peak metabolic rate appearsto fade
when growth rate deviates from normal, which is caused by the fact that
 Arctic
Tern
Chick 813
Metabolism

RMRdevelops in pace with m, whereasPMRis more dependenton age.

Our results are thus in contrast with the usual coupling of peak and basal
metabolism often found interspecifically between both adults and chicks
(Brody 1945; Drent and Daan 1980; Kersten and Piersma 1987; Drent and
Klaassen 1989; Ricklefs 1989; Daan et al. 1990; but see Koteja 1987 for the
absence of such a link in mammals) and suggest that such a coupling in
birds does not always imply causality.

Acknowledgments

We thank the personnel at the Norwegian Polar Research Institute and the
Kings Bay Coal Company for generously supporting our work during our
stay in Ny Alesund. We especially acknowledge N. Oritsland for his helping
hand when our oxygen analyzer was damaged on arrival in Ny Alesund. We
also acknowledge the valuable comments of W. A. Buttemer and two anon-
ymous referees. R. Wegman drew the graphs. The study was supported by
grant 2/90 from the Norwegian Polar Research Institute.

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