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Duration of shoot elongation in Scots pine varies within the crown

and between years


Pauliina Schiestl-Aalto, Eero Nikinmaa and Annikki Makela*
University of Helsinki, Department of Forest Sciences, PO Box 27, 00014 University of Helsinki, Finland
* For correspondence. E-mail annikki.makela@helsinki.
Received: 25 April 2013 Returned for revision: 28 May 2013 Accepted: 19 June 2013
Background and Aims Shoot elongation in boreal and temperate trees typically follows a sigmoid pattern where the
onset and cessation of growth are related to accumulated effective temperature (thermal time). Previous studies on
leader shoots suggest that while the maximum daily growth rate depends on the availability of resources to the
shoot, the duration of the growth period may be an adaptation to long-term temperature conditions. However,
other results indicate that the growth period may be longer in faster growing lateral shoots with higher availability
of resources. This study investigates the interactions between the rate of elongation and the duration of the growth
period in units of thermal time in lateral shoots of Scots pine (Pinus sylvestris).
Methods Length development of 202 lateral shoots were measured approximately three times per week during
seven growing seasons in 25 trees per year in a mature stand and in three trees during one growing season in a
sapling stand. A dynamic shoot growth model was adapted for the analysis to determine (1) the maximum growth
rate and (2) the thermal time reached at growth completion. The relationship between those two parameters and
its variation between trees and years was analysed using linear mixed models.
Key Results The shoots with higher maximumgrowth rate within a crown continued to growfor a longer period in
anyoneyear. Higher JulyAugust temperature of the previous summer implied a higher requirement of thermal time
for growth completion.
Conclusions The results provide evidence that the requirement of thermal time for completion of lateral shoot ex-
tension in Scots pine may interact with resource availability to the shoot both fromyear to year and among shoots in a
crowneach year. If growingseason temperatures rise in the future, this will affect not onlythe rate of shoot growth but
its duration also.
Key words: Annual course of growth, daily variation in growth, Scots pine, Pinus sylvestris, thermal growth
requirement, thermal time, dynamic model, phenology.
INTRODUCTION
Shoot elongationintrees typicallyfollows a sigmoidpatternwith
its accelerating, steady and decelarating phases, growth peaking
around the midpoint between the start and the end of the growth
period (Oleksyn et al., 2001; Chuine et al., 2006). Wide empir-
ical evidence suggests that the onset andcessationof shoot exten-
sionare triggeredbyaccumulatedeffective temperature (Beuker,
1994; Chuine et al., 2006; Salminen and Jalkanen, 2007; Seo
et al., 2010), possibly in combination with daylength (Koski
and Sievanen, 1985; Cannell and Smith, 1983; Linkosalo,
2000; Linkosalo et al., 2006; Fu et al., 2012). The rate of
growth, on the other hand, has been suggested to depend on the
overall availability of resources to the apical meristems, which
may vary from year to year (Hesselman, 1904; Persson, 2006;
Salminen and Jalkanen, 2007; Sutinen et al., 2012) but also
during the ontogenetic development of the tree and according
to the position of the shoot within the crown (Nikinmaa et al.,
2003).
Climate change is expected to lengthen the growing season in
boreal forests and to increase the potential productivity through
increasedambient CO
2
concentrationandtemperature. Predictions
often assume that increased net photosynthetic productivity dir-
ectly translates into increased growth (e.g. Valentine et al., 1997;
Bergh et al., 2005; Eastaugh et al., 2011), but this may be ham-
pered by the strong genetic component in the timing of growth
demonstrated by provenance trials (Beuker, 1994; Oleksyn
et al., 2001), where northern species and provenances show
earlier bud burst and shorter duration of the growth period than
their more southern counterparts (Beuker, 1994; Partanen and
Beuker, 1999; Oleksyn et al., 2001; Chuine et al., 2006). To
date, there is not sufcient information about the degree to
which trees could acclimate their seasonal growth pattern
to changes in climate.
In studies on Scots pine (Pinus sylvestris) near the northern
timberline, Salminen and Jalkanen (2007) found that the between-
year variation of height increment was entirely due to variation
in the daily average rate of growth during the growing season,
while the timing was controlled by a xed requirement of accu-
mulated effective temperature. The rate of growth, on the other
hand, was correlated with previous-year summer temperature,
suggesting that the level of resources during the time of bud for-
mation was crucial (Salminen and Jalkanen, 2005). A growth
chamber study in Scots pine on impacts on shoot growth of pro-
longed exposure to increased CO
2
and temperature indicated that
the duration of growth inunits of accumulated effective tempera-
ture was largely independent of the ambient temperature, al-
though the critical temperature sums when calculated from 1
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January increased for both the start and the cessation of growth in
the increased mean temperature treatment (Kilpelainen et al.,
2006).
In one of few studies on the effect of resource availability on
the timing of shoot growth, Remphrey and Davidson (1994)
found an interaction between the duration of shoot extension
and overall resource level in four clones of green ash (Fraxinus
pennsylvanica var. subinterregima). They found that trees dis-
budded and pruned to a single leader showed both faster
growth rates and longer growth duration of the leader than un-
pruned trees. They also compared leader growth with lateral
shoots, nding that the larger shoots grew faster and longer
than the smaller shoots. Both of these results can be interpreted
as impacts of resource availability to shoots on the duration of
the growth period. The pruned trees would have had more
reserve carbohydrates to allocate to the leader than the control,
as the side shoots were disbudded. Within the crown, the distri-
bution of growth rate of lateral shoots during the growing season
is clearly an indication of resource allocation (Nikinmaa et al.,
2003). A correlation between the duration of growth and the
rate of growth could therefore be indicative of an interaction
between direct resource allocation and timing.
In this study, we hypothesize that the requirement of accumu-
lated effective temperature for completion of lateral shoot exten-
sion in Scots pine crowns is correlated with the maximumrate of
shoot extension. As suggested by Remphrey and Davidson
(1994), this correlation should be found among the lateral
shoots of a tree in any given year. In addition, because the
maximum rate of shoot extension has been shown to vary from
year to year with previous-year late summer temperature
(Salminen and Jalkanen, 2005), similar variation with previous-
year late summer temperature should be found in the timing of
shoot extension if our hypothesis holds true.
To test the hypothesis, we formulate a model for shoot elong-
ation in which both growth onset, rate of growth and growth ces-
sation are treated in terms of the accumulated effective
temperature (Sarvas, 1972; Hanninen and Kramer, 2007). The
model is a further development of that presented by Pietarinen
et al. (1982). Here, the model is parameterized and calibrated
for Scots pine in southern Finland, to analyse the relationship
between the accumulated effective temperature required for
growth completion and the maximum growth rate. For testing
the above propositions, we study the co-variation of model para-
meters relatedtogrowthrate of shoots andthe time of completion
of the growing season within the crown, between trees and
between years by means of mixed linear models. The results
are compared with the conventional temperature sum model by
analysing the relationship between the present model para-
meters, nal shoot length and 5 8C based temperature sum at
growth completion.
Tocarryout the analysis, we require operational denitions for
effective temperature, growth completion and maximum
rate of shoot elongation, which all, in a lack of unequivocal
direct measurements, are more or less model-dependent. The
concept of effective temperature is based on the idea that
growth, or ontogenetic development in general, is proportional
to temperature while within an effective range, for example
greater than a threshold (Hanninen and Tanino, 2011). This
implies that the accumulated growth is proportional to the accu-
mulated effective temperature, often called thermal time (for
reviews, see HanninenandKramer, 2007; Fuet al., 2012). Acon-
ventional denition of thermal time is the sum, S (8Cd) of daily
temperatures, T
k
, exceeding a threshold, T
th
, from a specied
date, k
0
, onwards:
S =

365
k=k
0
T
k
.T
th
T
k
T
th
(1)
In an early pioneering study, Sarvas (1972) proposed a logistic
model for effective temperature:
r(T) =
0, T , 0
1
1 +e
a Tb ( )
, T 0
_
_
_
(2)
Above, r(T) is the normalized (unitless) effective temperature
and a and b are parameters. Hanninen and Kramer (2007) esti-
mated the parameters for boreal Scots pine so as to make r(T)
for the lower temperature range proportional to the temperature
exceeding 5 8C, demonstrated in many earlier studies to be an
adequate denition of effective temperature for boreal Scots
pine (Sarvas, 1972; Kilpelainen et al., 2006; Salminen and
Jalkanen, 2007). In analogy with the temperature sum, this equa-
tion can be used for dening a corresponding thermal time, s, as
the time integral of r(T):
s t
f
( ) =
_
t
f
t
0
r T t ( ) ( ) dt (3)
where T(t) is temperature at time t, and t
0
and t
f
are start and end
times of accumulation of thermal time. Note that the unit of s is
days because r(T) is unitless.
Elongation growth has usually been modelled by means of a
logistic function which is a solution of a differential equation
that operates either on linear time (Chuine et al., 2006) or on
thermal time (Salminen and Jalkanen, 2007). Consistently with
wide empirical evidence on Scots pine (Oleksyn et al., 2001),
the maximumgrowth rate in the logistic model occurs at the mid-
point between the beginning and end of the growth period, its
value depending on the duration of the period and the nal
length of the shoot (Chuine et al., 2006). However, the model
is somewhat problematic theoretically. First, because logistic
growth is proportional to current shoot length, an initial positive
length has to be assumed to incite growth. Secondly, growth is
also proportional to the deviation of current shoot length from
the maximum length, such that the maximum length which is
only approached asymptotically in the model has to be known
a priori. These problems have conventionally been dealt with
by estimating the start and end dates as those where a certain per-
centage of total growth has taken place, such as 5 and 95 %, and
by nding the nal length from model ts to data (Chuine et al.,
2006; Salminen and Jalkanen, 2007). The model employed in
this study provides an alternative approach with similar qualita-
tive behaviour to the logistic model but where the elongation
growth proceeds explicitly in response to the environment,
rather than in response to current shoot length (Pietarinen
et al., 1982; Kanninen, 1985; Kilpelainen et al., 2006).
Schiestl-Aalto et al. Duration of shoot elongation in Scots pine Page 2 of 11

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MATERI AL AND METHODS
Material
The length development of Scots pine (Pinus sylvestris) shoots
was measured in 2002, 2003 and 20052009 at SMEAR II
station in Hyytiala, southern Finland (61 851

N, 17 829

E) and
additionally in a nearby sapling stand in 2008. The habitat at
both sites is medium fertile (VT according to the Finnish forest
classication system; Cajander 1926), the number of trees is
1164 ha
21
at SMEARII stand and 1370 ha
21
at Sapling stand.
The height of the mature trees was 1618 m in 2008 and the
length of the live crown was 56 m. The height of the saplings
was 2 m.
In the SMEAR II stand, the measurements were taken from
1333 shoots from 35 mature trees per year. Measurements
started at 2 to 27 May (Table 1). To select the shoots, the follow-
ingprocedurewas applied: The lengthof the live crownwas mea-
suredandbranches closest toheights 12
.
5, 37
.
5and62
.
5 %of the
crown length fromthe top were chosen. Branches were chosen so
that they were to the same compass direction in one tree and to
different compass direction in different trees, according to the
possible crown access from the measurement tower. From the
selected branches, the terminal shoot of the branch main axis
and the terminal shoot of one side axis were chosen for the meas-
urement. In addition, one side branch from the top whorl was
included in the study. The top shoot of the main trunk was not
measured.
In the sapling stand, one branch from each of the four or ve
uppermost whorls of the saplings was selected randomly. From
these branches the lengths of the terminal shoot of the main
axis, and one terminal shoot of the side branch of the current
year whorl and from the preceding year whorl were measured.
Side branches were randomly selected. From the topmost
whorl of the tree the length of the main shoot and one side
shoot were measured. The total number of measured shoots
was 34.
The length of each shoot was measured three times a week
during the measurement period. The length was measured
from the base to the tip of the shoot, rst with a digital calliper
and later with a ruler. The basal reference point was xed with
a pin attached to the top of the previous year shoot.
Temperature data were measured at the SMEAR II station at
8
.
4 m height. Daily average temperatures were calculated from
half-hourly data.
Model description
The model developed here for the growth of shoot length is
based on the effective temperature concept introduced by
Sarvas (1972) (eqn 2). The progress of thermal time, s (days),
is described using the differential form of eqn (3) as follows:
ds
dt
= r T t ( ) [ ] t t
0
s t
b
( ) = 0
(4)
where T(t) is temperature at time t, t
0
is the start date of thermal
time accumulation and t
b
is the date of bud burst. r[T(t)] is the
value given by eqn (2) of the effective temperature at time t,
with parameters taken from Hanninen and Kramer (2007)
(Table 2). The start date t
0
signies the earliest possible date
for rest break, i.e. the onset, after rest, of ontogenetic develop-
ment that responds to temperature, eventually leading to bud
burst (Hanninen and Kramer, 2007). Rest break is assumed not
to occur before daylength reaches a required value, and, follow-
ing Linkosalo (2000), we set t
0
as 10 March. After this, bud burst
occurs when thermal time has accumulated from s(t
0
) s
0
to a
critical value s
b
. Here, it is convenient to normalize s to vanish
at bud burst, i.e. s
b
s(t
b
) 0(see eqn 6 below). As the accumu-
lation is irreversible, this implies that s(t
0
) , 0, although the
length of thermal time required for bud burst can be expressed
as s(t
b
) s(t
0
) s(t
0
) . 0. Here we assume that s
0
can be
xed for all years and shoots (Hanninen and Kramer, 2007;
Seo et al., 2010), and its value has been set to be consistent
with the results of Pietarinen et al. (1982) (Table 2).
The model nowdescribes the elongation growthof shoots with
respect to thermal time as follows:
dH
ds
= L f s ( ) (5)
where Lis a parameter (mmd
21
) and f (s) denes howthe level of
growth proceeds withthermal time, s. We use a sine function for f
(Fig. 1):
f (s) =
1
2
0,
sin
p 4s s
c
( )
2s
c
+1
0,
_
_
_
_
_
_
_
_
,
s , 0
0 s s
c
s . s
c
_

_
(6)
where s
c
is the value of thermal time at growth cessation. In other
words, growth occurs when thermal time is in the range s [
[0,s
c
], the rate rst increasing until it peaks at s 0
.
5s
c
, then re-
ducing again. This is similar toPietarinen et al. (1982) who mod-
elled the function f in three linear pieces. The sine function bears
a close resemblance to empirical results on the progress of height
growth in Scots pine (Oleksyn et al., 2001).
The nal length of the shoot can now be readily worked out
through integration of eqn (5) over the growth period (s [
[0,s
c
]), using the denition for f (s) in eqn (6):
H t
c
( ) H
b
= L
_
s
c
0
f s ( ) ds =
1
2
Ls
c
(7)
whereH
b
isthe lengthof the budat s(t
b
) 0(see Appendix). This
means that the nal length of the shoot depends on both the
TABLE 1. The number of measured shoots per year and tree
(SMEAR II site) and the starting dates of the measurements
Tree
Year 1 2 3 4 5 6 Sum Start
2002 0 0 1 3 5 4 13 7
.
5
2003 4 0 7 6 5 5 27 19
.
5
2005 7 8 7 6 5 0 33 2
.
5
2006 7 5 7 5 4 0 28 3
.
5
2007 5 7 6 6 0 0 24 21
.
5
2008 7 7 8 6 0 0 28 7
.
5
2009 8 7 0 0 0 0 15 27
.
5
Sum 38 34 36 32 19 9 168
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maximum length growth rate, L, and the thermal time at the end
of the growth period.
Whenconvertedtolengthgrowthwithrespect tocalendar time
instead of thermal time, eqns (4) and (5) yield
dH
dt
=
dH
ds
ds
dt
= L r[T t ( )]f s(t) [ ] (8)
The model thus combines the accumulated effect of temperature
through the function f (s), and the immediate (daily) effect of tem-
perature throughthe function r(T(t)). The parameters and symbols
of the model are summarized in Tables 2 and 3, respectively.
Parameter estimation
Themodel hasthreefreeparameters, s
c
, H
b
andL, tobeestimated
fromthe data collected in this study. For parameter estimation and
model simulation, we solved the differential equations (4) and (8)
using the second-order Euler algorithm with daily time step. The
phase of the annual cycle on day k was therefore calculated as
s
k
(s
c
, H
b
, L) = s
0
+

k1
j=0
r(T
j
) (9)
where s
0
is the initial value of thermal time (on 10 March), T
j
is
daily mean temperature on day j and the notation on the
left-hand-side indicates the dependence of the solution on the par-
ameter values to be estimated. The predicted shoot length on day k
was, respectively,
H
k
s
c
, H
b
, L ( ) = H
b
+

k1
j=0
Lr T
j
_ _
f s
j
_ _
(10)
The parameters s
c
, L and H
b
can be estimated simultaneously
by minimizing the residual sum of squares (RSS) between the
measured and modelled values of shoot length at all points of time:
min
s
c
, H
b
,L ( )

n
i=1
[H
i
s
c
, H
b
, L ( )

H
i
]
2
(11)
wherenistotal number of measurement times, i denotes ameasure-
ment time,

H
i
is measured shoot length at time i and H
i
is the re-
spective length as predicted with the model. Note that this
method uses total lengths rather than growth rates, as the latter
would be derived from consecutive length measurements and
would therefore be autocorrelated (Ljung, 1999).
For initial model calibration and testing, the individual-shoot
data were pooled and mean shoot lengths for all measurement
days were worked out for each site and year. The parameters
were rst estimated for these mean values. Subsequently, the
same method was used for estimating the parameter values for
each individual shoot i, denoted as s
ci
, L
i
and H
bi
. The non-linear
estimation was carried out using Excel solver.
The goodness of t of the model with the estimated parameter
values was assessedusingthefollowingindicators: degreeof deter-
mination, RMSE (root mean square error) and bias (Table 4). The
indicators were calculated for both total length and growth. The
latter was obtained by dividing the length increment between
two consecutive measurements by the corresponding number of
days. Furthermore, wetestedfor trends intheresiduals of themodel
in relation to time or temperature (t-test for correlation coefcient).
Hypothesis testing
In terms of the model, the hypotheses of this study can nowbe
presented as follows:
H1: The end of growth extension expressed as thermal time, s
c
,
increases with increasing maximum rate of shoot extension, L.
H2: The end of growth extension expressed as thermal time, s
c
,
increases with increasing JulyAugust temperature of the previ-
ous growing season.
TABLE 3. Functions and variables used in the model
Function Explanation Units
H Shoot length mm
f Pattern of yearly growth unitless
r Growth/rate of development unitless
s Stage of development d
T Temperature 8C
t Time d
1
0 s
c
s
f
(
s
)
FI G. 1. The yearly growth pattern function.
TABLE 2. Model parameters and their sources
Parameter Explanation Units Value Source*
L Max. elongation rate mm d
21
1
H
b
Initial bud length mm 1
a Growth function parameter 8C
21
0
.
185 2
b Growth function parameter 8C 18
.
4 2
t
0
Date of onset of development 10 March 3
s
0
Shoot growth onset d 0
.
97 4
s
c
Shoot growth cessation d 1
* (1) This study, (2) Hanninen and Kramer (2007), (3) Linkosalo (2000), (4) approximated from Pietarinen et al. (1982).
Schiestl-Aalto et al. Duration of shoot elongation in Scots pine Page 4 of 11

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JulyAugust temperature is used as this is the period after
completion of shoot growth when photosynthesis still occurs at
maximum rate (Hari and Makela, 2003). Below, the methods
for testing these hypotheses are explained in detail.
H1: Relationship between thermal time at growth completion (s
c
)
and maximum growth rate (L). According to eqn (7), the nal
length of shoots is determined by the maximum growth rate L
and the thermal time at growth completion, s
c
. To test hypothesis
H1, we formulated a linear regression model between L
i
and s
ci
for individual shoots. To account for possible differences in
this relationship between trees and years, we constructed a
mixed model where each tree and year were treated as random
effects:
s
c,ijk
= aL
ijk
+d +b
j
+c
k
+1
ijk
(regression 1)
where i is shoot, j is year and k is tree, and s
cijk
and L
ijk
are the
values of these quantities estimated separately for each shoot i,
using the method described in the section of parameter estima-
tion, a and d are xed-effect parameters, b
j
N(0,m) and c
k

N(0,n) are random effects and 1


kij
N(0,s) is model error.
(We also tested for a cross-correlation between the two random
effects but it was not signicant.) We only included trees from
the SMEAR II site in this comparison, as they were the ones
that had been measured repeatedly (Table 1).
A negative correlation (negative a) would be indicative of
cross-correlation between parameters, as it would indicate that
a small L was compensated for by a large s
c
(or vice versa) to
reach the observed nal length (as in eqn 7), while a positive cor-
relation would corroborate the hypothesis that s
c
varies with
shoot growth rate, increasing with increasing L.
H2: Relationship between thermal time at growth completion (s
c
)
and previous year temperature. To test our hypothesis H2, that
s
c
depends on previous summer temperature, we constructed
another mixed model,
s
c,ijk
= aL
ijk
+d +uT
j
+b
j
+c
k
+1
ijk
(regression 2)
where a and u indicate xed effects and T
j
is the mean tempera-
ture of Julyand August in the previous year. Other symbols are as
in regression 1. Growth data of the years 2002, 2003 and 2005
2009 were used as well as temperature data of each preceding
year.
The regressions were calculated using the lmer routine of the
lme4 package of R software. The signicance of the terms was
based on calculated P-values and the regressions were compared
using deviance and Akaikes Information Criterion (AIC).
RESULTS
Performance of the mean shoot model
The mean shoot model captured more than 99 %of the variation
in mean shoot length in the years and sites investigated when the
parameters (s
c
, L and H
b
) were allowed to vary between years.
The relative variation between years in the SMEAR II site was
largest in maximum shoot growth rate L (CV 0
.
33) and smal-
lest in the thermal time at growth completion s
c
(CV 0
.
20)
(Table 5). The degrees of determination of the model were
between 0
.
992 and 0
.
998 for lengths and 0
.
629 and 0
.
950 for
growth rates (Table 6). An average t was obtained for the
SMEAR II stand in 2008 (Fig. 2), while the poor prediction of
growth in 2005 is caused by larger variation of growth in mea-
surements than was predicted with the model. In mid May
TABLE 4. Statistical parameters used for evaluating the model
Statistics Equation
Degree of determination R
2
= 1

n
i=1
(y
i
y
i
)
2

n
i=1
(y
i
y)
2
RMSE RMSE =
...................

n
i=1
(y
i
y
i
)
2
/n
_
Bias BIAS =

n
i=1
y
i
y
i
_ _
/n
y
i
is the value of ith measurement, y
i
is the value of ith prediction, y is the
arithmetic average of the y values and n is the total number of observations.
TABLE 6. Statistical parameters of the t to mean shoot data; the upper values are for length and lower values for growth
2002 2003 2005 2006 2007 2008 2009 2008 Saplings
Degree of determination 0
.
996 0
.
996 0
.
996 0
.
998 0
.
998 0
.
998 0
.
996 0
.
998
0
.
895 0
.
693 0
.
632 0
.
739 0
.
954 0
.
936 0
.
921 0
.
931
RMSE 2
.
464 2
.
636 1
.
051 0
.
913 0
.
612 1
.
130 0
.
489 2
.
069
0
.
705 0
.
972 0
.
453 0
.
453 0
.
201 0
.
304 0
.
248 0
.
572
Bias 1
.
87 10
26
1
.
93 10
25
4
.
99 10
26
5
.
15 10
26
9
.
18 10
26
2
.
03 10
25
7
.
69 10
26
0
.
0913
9
.
83 10
23
0
.
116 3
.
41 0
.
0775 0
.
026 0
.
0282 0
.
0284 0
.
0155
TABLE 5. The values of estimated parameters for mean shoot growth
2002 2003 2005 2006 2007 2008 2009 2008 Saplings x s CV
H
b
9
.
39 10
.
41 13
.
14 19
.
88 14
.
00 13
.
74 19
.
20 15
.
09 14
.
25 3
.
71 0
.
26
s
c
15
.
66 17
.
09 18
.
62 13
.
85 8
.
36 15
.
04 12
.
12 15
.
18 14
.
39 3
.
14 0
.
22
L 14
.
14 15
.
23 6
.
82 8
.
53 6
.
25 9
.
25 8
.
39 17
.
51 9
.
80 3
.
24 0
.
33
x is mean, s is standard deviation and CV is coefcient of variation. The statistics have been calculated excluding the 2008 sapling site.
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2008whentemperatures were exceptionallylow, themodel over-
estimates growth. The rst part of the sigmoid growth function
then appears too high. The predicted nal length is slightly
smaller than measured in all years (about 98 %). In the residuals
of year 2008, there are no trends inrelationtotime (P .0
.
6) or in
relation to temperature (P .0
.
1; Fig. 3).
Variation of model parameters among shoots
The parameter estimation for individual shoots resulted in
good agreement with the theoretical result of eqn (7) (Fig. 4).
The variation in L among shoots was much larger than that
between years, with CVin the range from0
.
5 to 0
.
75. In contrast,
s
c
varied only 814 % among shoots each year (Table 7). The
annual mean values of L obtained from averaging the individual
shoots were very close to those obtained fromtting the average
(R 0
.
97), but the same was not true of s
c
(R 0
.
35). Model ts
were generally fairly accurate for individual shoots, with high
degree of determination and small RMSE and bias (Table 8).
However, a few shoots tted very poorly, possibly due to pro-
blems in data recording or factors not included in the model,
such as insect damage (Table 8).
Variation of thermal time at growth completion (s
c
) with shoot
growth rate (L)
Therewas a signicant positive correlationbetweens
c
andLin
regression 1, with the randomeffects related to year showing ap-
proximately twice as high standard deviation as those related to
tree. The unexplained residual variation was greater than the
random effects, however (Table 9). The random effects related
to year correlated strongly with the previous year JulyAugust
temperature, with the year 2007 forming a clear outlier (Fig. 5).
Variation of thermal time at growth completion (s
c
) with previous
year temperature
When previous year JulyAugust temperature was added to
the xed effects, the randomvariation related to year was consid-
erably reduced, and the effect of T
j
on s
c
was signicant. The de-
pendence of s
c
onLwas highlysignicant (Table9). The AICand
deviation were similar for both models, suggesting that the
random effects related to year captured the same variation in
regression 1 as did the previous year JulyAugust temperature
in regression 2 (Table 9).
DISCUSSION
In this study, we found evidence that the duration of lateral shoot
extension in Scots pine crowns varies among shoots and between
years. First, in accordance with Remphrey and Davidsons
(1994) results on green ash, a dependence of the thermal time
at growth completion (s
c
) on the maximum growth rate of the
shoot (and nal shoot size) within crowns was found, with
higher maximum growth rate indicating later growth cessation
(H1). Secondly, unlike previous results on leader shoots in
Scots pine (Kilpelainen et al., 2006; Salminen and Jalkanen,
2007), we found that the temperature of the previous summer
was related to the time of completion of the growth period in
the subsidiary shoots (H2).
5
4
3
2
1
0
G
r
o
w
t
h

(
m
m

d

1
)
65 305
Time (d)
236 177
R
e
l
a
t
i
v
e

l
e
n
g
t
h
,

m
o
d
e
l
l
e
d
Relative length, measured
10
08
06
04
02
0
0 02 04 06 08 10
5
4
3
2
1
0
5 4 3 2 1 0
M
o
d
e
l
l
e
d

g
r
o
w
t
h

(
m
m

d

1
)
Measured growth (mm d
1
)
10
A
B
C
D
08
06
R
e
l
a
t
i
v
e

l
e
n
g
t
h
04
02
0
Measured
Modelled
65 305
Time (d)
236 177
FI G. 2. Measuredandmodelledshoot length(A) andgrowth(B) intheSMEARII
stand in 2008. Measured values are indicated with dots and modelled values with
line. In(C) and(D), measuredandmodelledvalues are comparedversus a 1 : 1line.
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Previous studies have suggested that the rate of shoot growth,
L, is largely determined by the availability of resources to the
growth sites (Remphrey and Davidson, 1994; Jalkanen and
Tuovinen, 2001; Chuine et al., 2006; Pinto et al., 2011; Guan
et al., 2012). The allocation of resources within a tree is related
to shoot position (Nikinmaa et al., 2003), while the crown-mean
L varies between trees, locations and years (Chuine et al., 2006;
Salminen and Jalkanen, 2007; Pinto et al., 2011). Through the
established relationship between L and s
c
, our results suggest
that the durationof growthcouldalsobe relatedtothe availability
of resources to the shoot. However, the related mechanisms are
not straightforward and probably involve complex interactions
between carbon, nutrients and water at the whole-tree level
(Lavigne et al., 2001; Little et al., 2003; Holtta et al., 2010;
Pantin et al., 2012), which are beyond the scope of this study.
Fromthe point of viewof resource availability, it is interesting
to note that the outlier in Fig. 5, where the previous-year
temperature effect fails to explain the duration of shoot growth
in thermal time, occurred in 2007, the year after the only severe
drought that has been recorded at the SMEAR II station since
1996. This was in the second half of the summer 2006 when
drying out of the soil and reduction of photosynthesis and evapo-
transpiration were observed for a period of about 2 weeks in July
and August (Duursma et al., 2008). Assuming that not only tem-
perature but the overall environmental conditions duringbudfor-
mation affect the value of s
c
(Garrett and Zahner, 1973; Guan
et al., 2009; Dobbertin et al., 2010; Pinto et al., 2011;
Limousin et al., 2012), the drought event offers a plausible ex-
planation for the outlier. However, one should also note that
March 2007 was exceptionally warm (mean temperature
1
.
6 8C in 2007 and 4
.
0 8C on average in the other years) and
was followed by exceptionally cold spells in early April and
early May (mean daily minimum temperature in 114 April
2007 2
.
6 8C, mean of the other years 1
.
9 8C).
The present model derived thermal time froma sigmoid equa-
tion for effective temperature (eqn 2), while many other studies
have used the conventional degree-days approach (Salminen
and Jalkanen, 2005, 2007; Fu et al., 2012). In addition, unlike
in the widely used logistic and Gompertz models, the shoot
elongation model was parameterized with well-dened start
and end dates and without direct reference to the nal length of
the shoot. To assess the results in relation to previous studies,
we computed the correlations between s
c
, L, the effective tem-
perature sum with 5 8C threshold (S) at growth completion (S
c
)
and the nal length of the shoot (H
f
) (Table 10). During each in-
dividual year, the correlation between s(t) and S(t) was almost
one-to-one (R 0
.
999), with an initial period in the spring
when s started to accumulate slightly earlier than S. The start
date of shoot extension (s 0), on the other hand, occurred
after the start of accumulation of S and on average at S
6
.
42 +8
.
18 8Cd during the seven years studied, with a minor
shift from year to year in the relationship between s and S.
However, the correlation between the values at growth comple-
tion, s
c
and S
c
, was still very high in the pooled data set (R
0
.
971). Similarly, both s
c
and S
c
were more strongly correlated
with the nal length of the shoot than with the maximum
growth rate L (Fig. 6). This is understandable in the light of
eqn (7) as H
f
increases with both increasing L and increasing s
c
.
400
300
y = 0499x + 1479
R
2
= 09857
200
H

(
m
m
)
100
0
0 200 400
s
c
L (mm)
600 800
+
+
+
+
+
+
+
+
+
+
+
+
+ + +
+
+
+
+
+
+ +
+
+ +
+
++
+
+
+ +
+
+
+ +
+ +
+
+
+ +
+
++++
++
+
++
++
+
+
++
+
+ +
++
+
+ + +
+ + +
+++ + +
+
+
+
+
+
+ + + +
+++ +
+ + + + + + +
+
+
++++
++ + +
+
++++++ +
+
+
+
+
+ + +
+
+
+ +
+ ++
+
+ + +
+
+
+
+ +++
++ +
++ + + + +
+
+ +++
+
+
+
+
++
+ + + +
+
+ +
+
+++
+
+ + + +
FI G. 4. Test of the theoretical relationship H 0
.
5s
c
L + H
b
in the data with s
c
and L estimated separately for each shoot (n 168). The intercept is an estimate
of the mean initial bud length.
2
SMEAR II
Sapling
A B
1
0
R
e
s
i
d
u
a
l

(
m
m
)
1
2
65 205 36
Time (d)
176 17 157 0 5 10
Temperature (C)
15 20
FI G. 3. Residuals (measuredvalues modelledvalues) of shoot growthin2008inrelationtotime(A) andtemperature(B). SMEARII standandSaplingstanddata are
as indicated in the key.
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Salminen and Jalkanen (2007) concluded that leader shoot
growth terminates on average when 41 % of the long-term
mean S has been reached. In our data, the mean S was
1260 8Cd (0
.
41 1260 8Cd 517 8Cd), and the maximum
value of S
c
was 523 8Cd in the pooled data. This was reached
by a shoot with nal length H
f
307
.
7 mm. This is similar to
the average height growth of trees in the SMEAR II site during
the time of our measurements (32 cm) (J. Levula, University of
Helsinki, Finland, pers. comm.). If the terminal shoot follows
the same pattern as the lateral shoots in the pooled data set, our
results seem consistent with those of Salminen and Jalkanen
(2007, Fig. 6).
In this study, we chose to use a pre-determined value for the
thermal time duration from growth onset to bud burst (s
0
). This
was largely done on technical grounds, as tting four parameters
would have yielded considerable redundancy in the parameter
values due to multiple extrema in the objective function (eqn
11). However, because the accumulation of thermal time is
very slow in the spring, a 10 % ( 1 week) difference in the
time of growth onset would only amount to a difference of
about 12 %in the accumulated thermal time at growth comple-
tion (s
c
). Fixing s
0
therefore had little impact on the estimation of
s
c
which was the primary focus of this study. In comparison,
studies applying the logistic model actually avoid the question
of start time as the start is determined by the middle and the
end (Chuine et al., 2006; Salminen and Jalkanen, 2007).
Kilpelainen et al. (2006) studied height growth of Scots pine in
elevated temperature using a model similar to ours, nding that
both the start and the end times were shifted forward in elevated
temperature. However, in that study degree days (5 8Cthreshold)
were accumulated from 1 January and the temperature was
increased by 6 8C in the winter months. Counting from early
March as suggested by Linkosalo (2000) and/or using our s
for quantifying thermal time would probably have resulted
in much more similar thermal time requirements between
control and treatment. The existence of a threshold thermal
time for bud burst is supported by recent ndings that degree
days (with threshold temperature ,5 8C) adequately explained
TABLE 8. Annual statistics of model ts to individual shoot data
2002 2003 2005 2006 2007 2008 2009
Degree of determination Max. 0
.
996 0
.
999 0
.
997 0
.
998 0
.
995 0
.
999 0
.
999
Min. 0
.
979 0
.
973 0
.
872 0
.
963 0
.
515 0
.
973 0
.
665
Mean 0
.
992 0
.
988 0
.
986 0
.
991 0
.
968 0
.
994 0
.
957
s.d. 0
.
005 0
.
007 0
.
021 0
.
008 0
.
095 0
.
005 0
.
082
RMSE Max. 7
.
374 7
.
267 5
.
239 5
.
520 3
.
878 3
.
502 1
.
489
Min. 0
.
984 0
.
785 0
.
691 0
.
515 0
.
611 0
.
471 0
.
313
Mean 3
.
210 3
.
131 1
.
792 1
.
768 1
.
385 1
.
401 0
.
684
s.d. 1
.
902 1
.
745 1
.
165 1
.
349 0
.
894 0
.
819 0
.
283
Bias Max. 3
.
35 10
25
4
.
93 10
25
2
.
60 10
25
2
.
30 10
25
1
.
02 10
24
5
.
66 10
25
2
.
73 10
24
Min. 2
.
73 10
25
1
.
10 10
24
2
.
08 10
25
4
.
38 10
26
3
.
34 10
25
3
.
17 10
25
1
.
08 10
23
Mean 7
.
37 10
26
4
.
65 10
26
6
.
44 10
26
7
.
50 10
26
1
.
16 10
25
5
.
50 10
26
4
.
47 10
25
s.d. 1
.
55 10
25
3
.
34 10
25
8
.
04 10
26
6
.
40 10
26
3
.
02 10
25
1
.
46 10
25
2
.
79 10
24
TABLE 7. Annual mean values of s
c
and L at the SMEAR site estimated from model ts to individual shoots
2002 2003 2005 2006 2007 2008 2009 x s CV
s
c
x 15
.
05 15
.
60 12
.
29 13
.
37 12
.
92 13
.
18 11
.
56 13
.
42 1
.
33 0
.
10
s 1
.
71 2
.
15 1
.
57 1
.
17 1
.
71 1
.
26 0
.
95
CV 0
.
11 0
.
14 0
.
13 0
.
09 0
.
13 0
.
10 0
.
08
L x 14
.
47 15
.
23 7
.
99 8
.
99 7
.
66 9
.
56 10
.
96 10
.
69 2
.
82 0
.
26
s 7
.
11 10
.
15 5
.
27 5
.
33 4
.
41 7
.
02 7
.
54
CV 0
.
49 0
.
67 0
.
66 0
.
59 0
.
58 0
.
73 0
.
69
x mean, s standard deviation, CV coefcient of variation ( s/x).
TABLE 9. Results of regressions 1 and 2
(a) Fixed effects
Parameter
Estimated
value
Standard
error t P
Regression
1
a 0
.
14841 0
.
01405 10
.
56 ,10
25
d 11
.
83029 0
.
46913 25
.
22 ,10
25
Regression
2
a 0
.
14970 0
.
01398 10
.
712 ,10
25
u 0
.
64574 0
.
20508 3
.
149 0
.
0019
d 1
.
49034 3
.
29560 0
.
452 0
.
652
(b) Random effects
m n s AIC Deviance
Regression 1 0
.
97751 0
.
54308 1
.
16814 572
.
5 556
.
0
Regression 2 0
.
57347 0
.
53588 1
.
16883 569
.
3 548
.
8
The xed effects of shoot growth rate (L
ijk
) and previous year JulyAugust
temperature (T
j
) on the phase of annual cycle at growth completion (s
cijk
) are
denoted by a and u, respectively. d is the xed-effects intercept, m and n are the
standard deviations related to year and tree, respectively, and s is the residual
standard deviation. AIC Akaike Information Criterion.
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the start of primordial shoot development inside the bud before
budburst in Norway spruce (Sutinen et al., 2012).
When collecting data for shoot extension growth, it would be
convenient to be able to use either small trees, or shoots on lower
lateral branches, to minimize the data collection effort. Seo et al.
(2010) found that no differences could be observed in timing
between seedlings and pole stage trees in the timing of leader
growth. The present results suggest, however, that the choice
of shoots within a tree would potentially affect the observed
average timing. After considering the variation caused by
shoot size, the between-tree variation was considerably less
than the between-year variation or the unexplained randomvari-
ation (Table 9). However, this result cannot be generalized to all
between-tree variation, as the trees in the comparison all came
from the same even-aged stand.
The model used in this study was a further development of that
by Pietarinen et al. (1982) with simpler structure and fewer para-
meters. Although in this study the main use of the model was to
provide a theoretical framework for evaluating the start and end
dates and the maximum daily growth rate of lateral shoot exten-
sion, the results also provide insights into how the model should
be further developed and what data would be needed for making
it a more general prediction tool of shoot extension growth in
trees and stands.
The model assuming that shoot growth follows a sigmoid
curve driven by thermal time is widely used, although the den-
ition of thermal time varies (e.g. Mutke et al., 2003; Kilpelainen
et al., 2006; Fuet al., 2012). Althoughthe model generallyagrees
with measurement, some of its assumptions may be over-
simplied. In particular, we found that it overestimates growth
under cold conditions (Fig. 3B). According to Korner (2006)
growth has a certain positive threshold temperature whereas res-
piration also occurs belowthat threshold. If respiration is indica-
tive of development processes growth and development of the
phase of the annual cycle could perhaps be more accurately
describedbyseparate functions. Toimprovethe model inthis dir-
ection, it would be helpful if the development process could be
clearly identied with some measureable physical or physio-
logical events, such as observations of bud development before
budburst (Sutinen et al., 2012).
In this study, the temperature-driven model was able to
account for over 90 % of the daily variation of growth at best.
Considering the measuring accuracy, this is probably as high a
degree of explanation as is feasible. When assessing this, one
has to bear in mind that only one location was studied, excluding
any possible variation in local conditions such as solar radiation,
water availability or length of the growing season which have
been found to affect shoot growth in other studies (Kishchenko
and Vantenkova, 2007; Ford et al., 1987; Perala, 1983; Pinto
et al., 2011). Importantly, as noted already, the SMEAR II site
has rarely suffered from notable drought and, moreover, any
drought episodes have tended to occur towards the end of the
growing season when shoot growth has already been completed
(Duursma et al., 2008; Peltoniemi et al., 2012). This situation
may change inthe future, however, as climate change is expected
to increase the summertime evaporative demand relative to pre-
cipitation (Jylha et al., 2004). The model structure would readily
allowfor incorporating other driving variables in the model, e.g.
solar radiation, air humidityand water availability, but this could
further emphasize the need to separate the functions governing
400
300
200
F
i
n
a
l

l
e
n
g
t
h

(
m
m
)
100
0
0 200
ETS at growth completion (Cd)
400 600
FI G. 6. Final length of shoots plotted against effective temperature sum (ETS,
S
c
) at growth completion determined by parameter s
c
.
15
10
05
R
a
n
d
o
m

e
f
f
e
c
t
,

b
j
05
10
15
20
13 14 15
Previous JulyAugust temperature (C)
16 17 18
0
FI G. 5. Values of random effect b
j
(regression 1) for each year as a function of
previous-year JulyAugust temperatures. R 0
.
820. If the outlier (year 2007) is
removed, R 0
.
984.
TABLE 10. Correlations (Pearson) between the accumulated
effective temperature at growth completion (s
c
), effective
temperature sum at growth completion (S
c
, 5 8C threshold), nal
shoot length (H
f
) and maximum shoot growth rate (L)
s
c
S
c
H
f
L
s
c
1
S
c
0
.
971321 1
H
f
0
.
724418 0
.
738974 1
L 0
.
642070 0
.
664761 0
.
974581 1
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growth and development. The Lockhard function provides a
good conceptual framework that considers both metabolic
(carbon supply) and hydromechanical inuences on growth
and how these are changed during ontological development
and are inuenced by the xylem and phloem transport network
(Pantin et al., 2012).
In this study, we considered the growth of shoots as a demand-
driven process, where the demand was explained by temperature
effects at different time scales. As already discussed above and
highlighted by the Lockhard function (Pantin et al., 2012), al-
though temperature provided a fair explanation of both
day-to-day growth, phenology and some year-to-year effects, it
seems important to extend the model to include other driving
variables, especially the availability of water, in future studies.
Secondly, it would be interesting to link the demand-driven ap-
proach to the supply of carbohydrates through photosynthetic
production. This becomes essential, especially, for predicting
climate change impacts. According to the present study as well
as other demand-driven models (e.g. Chuine et al., 2006;
Salminen and Jalkanen, 2007), consecutive warm years would
lead to increased growth of shoots through the impact of
previous-year temperature on nal shoot length. This would ob-
viously only be possible if the supply of carbohydrates and other
vital elements also increased as a result of climate change.
Furthermore, changes in the relative timing of photosynthesis
and growth may also play a role, as photosynthesis and growth
are limited by different environmental factors (Bansal and
Germino, 2009). Comparing the interactions and timing of
carbon sources and sinks in terms of phenological models
remains a future research topic.
ACKNOWLEDGEMENTS
We thank Minna Pulkkinen for help with statistical analysis and
Janne Korhonen and Liisa Kulmala for help with the measure-
ments. This work was supported by the Academy of Finland
(Grant no. 124531) and the FCoE Physics, Chemistry,
Biology and Meteorology of Atmospheric Composition and
Climate Change.
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APPENDI X
Derivation of eqn 7
Substituting f (s) from eqn (6) we have
L
_
s
c
0
f s ( ) ds = L
_
s
c
0
1
2
sin
p 4s s
c
( )
2s
c
+1
_ _
ds
=
1
2
L
_
s
c
0
sin
p 4s s
c
( )
2s
c
ds +
1
2
L
_
s
c
0
ds (A1)
The rst integral on the right-hand side can be integrated as
follows:
_
s
c
0
sin
p 4s s
c
( )
2s
c
ds =
s
c
2p
cos
p 4s
c
s
c
( )
2s
c
cos
p 0 s
c
( )
2s
c
_ _
=
s
c
2p
cos
3p
2
cos
p
2
_ _
_ _
= 0
(A2)
The second integral in (A1) has the value s
c
, hence
_
s
c
0
f s ( ) ds =
1
2
Ls
c
(A3)
which conrms the proposition of eqn (7).
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