1. Art and Diseño

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Timing of growth reductions in black spruce stem
and branches during the 1970s spruce budworm
outbreak1
Cornelia Krause, Boris Luszczynski, Hubert Morin, Sergio Rossi, and
Pierre-Y. Plourde
Abstract: Spruce budworm (Choristoneura fumiferana (Clemens)) defoliation is known to regularly produce radial growth
decrease in black spruce (Picea mariana (Mill.) Britton, Sterns & Poggenb.) in the boreal forest of Quebec. Some studies
have already shown that the first year of defoliation does not induce growth losses in the stem but could occur in other tree
parts. We therefore examined the timing and duration of the growth reduction caused by the last outbreak in black spruce
by also considering the branches. More than 79% of branches and 65% of stems exhibited a >40% growth decrease.The reduction was first registered in the upper part of the stem before being detected lower in the stem in 87% of the trees. Probabilities of growth reduction in the upper part of the stem were highest in 1976 and 1977. In the lower stem, the
probabilities were highest in 1978. An interesting finding was that in 69% of the studied stands, the probability of growth
reduction started earlier (1–2 years) in the branches than in the stem at 1.3 m. Branch analysis should be considered whenever questions arise in regard to the evolution of spruce budworm defoliation as well as the timing of observed growth reduction in black spruce.
Résumé : On sait que la défoliation par la tordeuse des bourgeons de l’épinette (Choristoneura fumiferana (Clemens)) entraîne régulièrement une baisse de la croissance radiale chez l’épinette noire (Picea mariana (Mill.) Britton, Sterns & Poggenb.) dans la forêt boréale du Québec. Des recherches ont déjà démontré que la première année de défoliation n’induisait
pas de pertes de croissance dans la tige, mais pouvait en causer ailleurs dans l’arbre. Nous avons par conséquent étudié le
déroulement et la durée de la réduction de croissance chez l’épinette noire causée par la dernière épidémie en tenant compte
aussi des branches. Plus de 79 % des branches et 65 % des tiges ont connu une réduction de croissance supérieure à 40 %.
Chez 87 % des arbres, la diminution de croissance a d’abord été observée dans la partie supérieure de la tige avant d’être
détectée plus bas dans le tronc. Les probabilités d’une réduction de croissance dans la partie supérieure de la tige ont été les
plus élevées en 1976 et 1977. Dans la partie inférieure de la tige, les probabilités ont été les plus élevées en 1978. Il est intéressant de noter que, dans 69 % des peuplements analysés, la probabilité d’observer une réduction de croissance a débuté
plus tôt dans les branches (1 à 2 ans) qu’à 1,3 m dans la tige. L’analyse des branches devrait être envisagée chaque fois que
des questions surgissent au sujet de l’évolution de la défoliation par la tordeuse des bourgeons de l’épinette et du moment
où apparaît la réduction de croissance chez l’épinette noire.
[Traduit par la Rédaction]
Introduction
Black spruce (Picea mariana (Mill.) Britton, Sterns &
Poggenb.) is the most abundant tree species in eastern North
America, with a distribution area between 49 and 51°N and
70 and 73°W (Viereck and Johnston 1990). Pure stands cover
almost 70% of the boreal forest of Quebec, Canada (Viereck
and Johnston 1990). Survival and renewal of this huge ecosystem are strictly related to two main disturbances, fire and
insect outbreaks (MacLean 1984; Morin 1994). In the eastern
part of Canada, periodic spruce budworm (Choristoneura fumiferana (Clemens)) defoliations have occurred and have
been recorded for the last three centuries with approximately
30-year frequency (Morin and Laprise 1990; Krause 1997;
Jardon et al. 2003; Boulanger and Arseneault 2004). During
the last outbreak in the 1970s, more than 55 million ha of
forest were affected (Boulet 1994). Severe defoliations induce
drastic growth losses in the stem and cause tree mortality
over wide areas. The ecological and physiological role of
spruce budworm outbreaks has been well documented in balsam fir (Abies balsamea (L.) Mill.), which is the main host
species (Blais 1965; Morin and Laprise 1990; Krause et al.
2003), but was disregarded for a long time in black spruce.
In the last two decades, few authors have investigated growth
reductions in black spruce during past periods of spruce budworm defoliation (Krause and Morin 1995; Morin 1998;
Received 22 November 2011. Accepted 21 March 2012. Published at www.nrcresearchpress.com/cjfr on xx May 2012.
C. Krause, B. Luszczynski, H. Morin, S. Rossi, and P.-Y. Plourde. Département des Sciences Fondamentales, Université du Québec à
Chicoutimi, 555 boulevard de l’Université, Chicoutimi, QC G7H 2B1, Canada.
Corresponding author: Cornelia Krause (e-mail: [email protected]).
1This
article is one of a selection of papers from the 7th International Conference on Disturbance Dynamics in Boreal Forests.
Can. J. For. Res. 42: 1220–1227 (2012)
doi:10.1139/X2012-048
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Krause et al.
Tremblay et al. 2011); thus, the consequences of this disturbance on growth and productivity of this most important tree
species in northeastern North America still remain unknown.
Black spruce death caused by spruce budworm is mostly
rare, but a reduction of more than 14% of the volume has
been reported (Morin et al. 2009). To protect this species
against severe defoliation periods, insecticides are generally
applied over large forest regions. The timing and location of
spraying should be well planned to optimize the effect on the
insect population. In this regard, the defoliation pattern
within a tree represents a helpful tool for the protection of
spruce stands.
Several studies tried to relate defoliation intensity to
growth losses in the stem by producing artificial defoliation
in balsam fir (Piene 1980; Erdle and MacLean 1999; D.A.
MacLean, personal communication, 1993). However, a recent
study showed that the impact of artificial defoliation on tree
rings of young individuals is modest and noticeable growth
reductions could only be observed after repeated severe defoliations over four growing seasons (Rossi et al. 2009a). Other
studies investigated defoliation from a physiological point of
view. Works by Lavigne et al. (2001) and Little et al. (2003)
demonstrated the occurrence of a compensatory mechanism,
with the remaining needles increasing their photosynthetic
rate to maintain a suitable level of production. All things
considered, links still have to be established between photosynthetic biomass losses and growth reductions during spruce
budworm outbreaks. Honkanen and Haukioja (1994) produced an exhaustive analysis of the carbon/nutrient balance
in response to single-branch defoliation in comparison with
that of the entire living crown. Moreover, young branches
were compared with older ones as well as the duration of
the defoliation over a range of 1–5 years. They discovered
that needle production in Scots pine (Pinus sylvestris L.) was
most severely affected in a young single branch defoliated in
just 1 year. Older and slower growing branches compensated
for defoliation losses better, even over several consecutive defoliation years. Based on their results, the authors concluded
that the sink/source hypothesis adequately explains the
changes in branch growth activities after defoliation. The authors suggested that the carbon storage in the stem and roots
is sufficient to rebuild needle mass.
In mature trees, the growth reductions do not necessarily
occur during the first year of a moderate to severe defoliation. Some authors pointed out that the effects of defoliation
could be registered earlier in the upper part of the tree of balsam fir and only afterwards in the lower stem (Mott et al.
1957; Blais 1958; MacLean 1985; Krause et al. 2003). This
delay seems to depend on tree height because growth reductions in taller trees appear 1–2 years later than in smaller
trees (Krause et al. 2003). On the whole, the information
available on time elapsed between insect defoliation and the
appearance of its effects on tree growth is scarce in mature
trees. Tree-ring chronology represents one of the most suitable and best-documented procedures to infer details of past
outbreaks and changes in insect populations. However, the
accuracy of the reconstructions depends on our knowledge
about the response of trees to these kinds of disturbances.
Questions arise on the level of sensitivity and dynamics of
growth reduction within a tree. In particular, how and when
do the different organs respond to an insect defoliation? The
1221
aim of this paper was to answer these questions by examining the dynamics of growth reduction induced by the 1970s
spruce budworm outbreak in stem and branches of black
spruce in the boreal forest of Quebec, Canada. The hypothesis was proposed that the wave of growth reduction moves
basipetally from the upper part of the tree towards the subjacent stem. Accordingly, we expected to observe (i) earlier
growth reductions in branches than in stem and (ii) earlier
growth reductions in the upper part than at the base of the
stem.
Material and methods
The study was conducted in the boreal forest of Quebec,
Canada, where 16 black spruce stands located between the
47th and 49th parallels were selected (Table 1). The choice
of these sites was based on defoliation survey maps with the
intention of covering a large region with mature black spruce
stands affected by the 1970s spruce budworm outbreak (Ministère des ressources naturelles et de la faune 2006). Stands
were composed of trees with an average age of 83 years,
17 cm diameter at breast height, and 14 m height (Table 1).
The basal area ranged from 17.5 to 32.0 m2·ha–1. The region
is characterized by cold winters and short vegetation periods
(Rossi et al. 2011). Over the past 30 years, the average minimum and maximum temperatures for this region were
–13.4 °C during the coldest months and 17.9 °C during the
warmest months. At the nearest weather stations to the
stands (48°53′N, 72°27′W), recorded annual mean temperature was 1.7 °C and annual precipitation ranged from 920
to 1187 mm (Environment Canada 2008). All stands were
monospecific and deriving from natural regeneration. A partial cutting in 10 of the stands was done more than 20 years
after the spruce budworm outbreak and is the only known
human activity in the stands.
Data collection
In each stand, three or six black spruce trees without visible injuries were randomly selected inside a 400 m2 plot and
felled for a total of 78 trees collected for the analysis (Table 1). Radial discs were sampled along the stem every
metre, starting at ground level. From each tree, discs were
also collected at the base of two living branches from the
lower living crown. All discs were air-dried, sanded with progressively finer grade sandpaper, and their tree-ring widths
measured along two perpendicular diameters for stem using
Mac Henson and WinDendro software (Guay et al. 1992).
To reduce the growth variability of the branches, a single radius was measured towards the soil surface to avoid compression wood. Radial growth was measured at 90° to the
direction of compression wood. Sections were then crossdated on a light table and checked with the Cofecha program
(Holmes 1983). Given the short series for the branches,
cross-dating was made with the light table only.
Tree-ring widths were transformed into a growth index
with the ARSTAN program using a double detrending with
a horizontal line and a spline function of 50 years (Cook
and Holmes 1986). No autoregression was removed from the
chronologies. Index chronologies were produced separately
for each stem height and for branches. During analysis, four
trees from stands 6, 11, and 15 were excluded because of a
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Table 1. Location and characteristics of the black spruce (Picea mariana) stands.
Site
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
Latitude
(°N)
47.51
47.51
47.88
48.03
48.03
48.08
48.08
48.14
48.14
48.46
48.46
48.47
48.47
48.87
48.98
48.98
Longitude
(°W)
71.18
71.19
71.46
72.33
72.33
71.52
71.52
71.87
71.87
70.33
70.32
70.21
70.21
71.74
72.73
72.74
Altitude (m
above sea
level)
753
369
731
404
388
347
342
326
376
683
657
631
603
170
216
210
Sampled
trees
6
3
6
6
3
3
6
6
6
6
3
6
3
3
6
3
Basal area
(m2·ha–1)
17.5
55.9
24.6
29.0
18.6
28.0
32.0
27.5
36.3
25.5
37.1
29.2
48.8
27.0
22.5
32.8
rotten heartwood and a lack of correlation with the site chronologies. The transformation of the tree-ring widths to specific volume increment, often used in papers on defoliation
outbreaks, was excluded because only one radius was measured for each branch. Another reason for the exclusion is the
eccentric growth where compression wood is produced in
branches.
Based on Morin’s (1998) study, the growth reductions at
1.3 m in balsam fir and black spruce stems induced by the
1970s spruce budworm outbreak occurred in the studied
stands during the period 1975–1980. Aerial defoliation survey maps, produced by real-time observers, revealed that one
stand registered a light defoliation in 1973 (Ministère des ressources naturelles et de la faune 2006). In 1974, the classes
light to moderately defoliated and severely defoliated were
found in 50% of the stands. All stands were severely defoliated in 1975 according to aerial photograph maps. Considering this fact, we selected a calibration period of 5 years prior
to 1975 (1970–1974). The growth reduction index, expressed
as a percentage, was estimated for each year starting from
1975 by subtracting each annual index from the mean index
of the calibration period (Krause and Morin 1995) according
to
GRx ¼
ðGRIx Þ À ðGRIð1970À1974Þ Þ
100
where GRx is the growth reduction (percent) in year x, GRIx
is the growth reduction index in year x, GRI(1970–1974) is the
mean growth reduction index for the calibration period, and
x is the year after the outbreak starting from 1975 to 1980.
GR ≥ 40% was considered to be an abrupt and significant
change in the growth of conifers (Schweingruber 1986).
Statistical analysis
For each year of the index chronologies along the stem and
in branches, binary responses were coded as presence (value
1) or absence (value 0) of growth reduction and discriminant
analysis was performed using PROC DISCRIM in SAS 9.2
(SAS Institute Inc., Cary, North Carolina) to classify each ob-
Age
(years)
61.6
163.7
71.8
137.6
118.0
79.5
80.6
78.3
75.3
84.6
80.7
84.8
85.0
77.8
70.3
73.3
Diameter at
breast height
(cm)
14.7
15.9
16.3
17.5
15.2
15.8
19.1
17.8
21.0
17.8
16.9
16.8
12.0
19.7
13.8
12.7
Height
(m)
10.4
13.2
11.3
16.1
10.2
15.3
17.9
15.5
16.6
13.5
13.5
12.9
13.0
16.9
12.7
13.4
Drainage
Good
Bad
Good to very good
Moderate
Good
Good
Bad
Moderate to good
Good
Good
Good
Good
Good
Good to very good
Good
Moderate
servation into one of the two groups. The resulting groupspecific densities were used to calculate univariate and bivariate posterior probability distributions of within-group
membership (Hora and Wilcox 1982). The classification criterion adopted parametric methods based on multivariate normal distributions within each class to derive discriminant
quadratic functions and assumed unequal variance between
classes using the observed within-group covariance matrices
(Rossi et al. 2009b). Final estimates were calculated only for
values within the ranges of variation of the measured variables and between 1970 and 1985.
Results
A total of 74 dated black spruce stems were analysed
(Table 2), but only 65 branches covered the period starting
from the beginning of the calibration period in 1970.
Branches were rarely aged more than 40 years, even the
lower ones.
Index chronologies
The index chronologies at 1 m height on the stem revealed
40% growth reductions for most stands in 1978 (Fig. 1),
which is related to the 1970s spruce budworm outbreak.
This decrease in growth lasted several years and reached minimum values in 1978–1979 in 70% of stands. Tree recovery
was not uniform among stands and was observed between
1980 and 1988. Timings and intensity of growth reductions
differed among trees in the same stand and also between
stands. After the outbreak, the growth pattern attained similar
values to those observed before 1975, but the variability
among trees remained high until 1995. Forty-six percent of
trees exhibited at least 3 years of consecutive growth reductions ≥40% (Table 2). All trees showed growth reductions
≥40% in stands 1, 2, 3, 6, and 11, whereas trees in stand 5
registered no radial growth decrease.
Growth reductions of 23% also occurred at the base of
branches in 1978 (Fig. 1). Despite the high differences
among stands, the variations were reduced during the outPublished by NRC Research Press
Krause et al.
1223
Table 2. Number of black spruce (Picea mariana) stems and branches registering a >40% growth reduction.
Total
6
3
6
6
3
2
6
6
6
6
2
6
3
6
4
3
Branches affected
1–2 years
1
1
3 years or more
5
2
6
1
1
1
4
3
4
4
1
2
1
1
1
4
1
3
1
1
Total
1
3
3
4
2
2
2
3
2
5
1
6
0
5
0
0
1–2 years
2
1
1
1
1
1
1
1
Stem
Fig. 1. Index chronologies within the 16 studied black spruce (Picea mariana) stands for stem at 1 m height and branches. The shaded background refers to the 1970s spruce budworm (Choristoneura fumiferana) outbreak.
1
Branches
Index chronologies (at 1 m stem height)
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Stems affected
Site
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
1
1950
1960
1970
break period. On average, the growth reductions started in
1973 and lasted for a longer period than in the stem, with
minimum values of ring width registered in 1987.
Along the stem
Although intensity and timing of growth reduction were
variable in the response to the outbreak among trees and
stands, the decreases along the stem did not start in the same
year in 13 out of 16 stands (Fig. 2). In 94% of trees, the
growth reductions first occurred in the higher part of the
1980
Year
1990
2000
2010
stem and then spread basipetally into the subjacent stem.
Probabilities of growth reduction in the upper part of the
stem were the highest in 1976 and 1977. In the lower stem,
the probabilities were the highest in 1978. The time delay between the first occurrence of growth reduction in the upper
and lower part of the stem was highly variable between
stands: seven stands showed a delay of <1 year, while in
two stands, the delay was 3 years. The average delay has
been estimated at 1.5 years. In half of the stands, growth reductions were more severe at the highest part of the stem.
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Fig. 2. Probability of growth reduction along the stem within the 16 studied black spruce (Picea mariana) stands.
Comparing stem and branches
Only 65 of the 144 branches covered the calibration period. The following results come from this data subset. The
impact of the outbreak was registered in 79% of the 65
branches (Table 2). The percentage of affected branches varied highly within stands, but in five stands, all branches exhibited a growth reduction. There was no relationship
between the proportion of affected stems and branches within
a stand. For example, in stand 5, stems did not show a
growth reduction over 40%, whereas the five branches did.
In three stands (13, 15, and 16), the absence of comparison between stem and branches can be explained by the lack
of branch samples within the calibration period (1970–1974).
In two additional stands (5 and 6), the probabilities of growth
reduction in the stem were not performed in the case of a 1
year decrease or with none. In branches and the stem at
1.3 m height, the probability of growth reduction culminated
between 60% and 90% (Fig. 3). In several stands, the probabilities of registering a growth reduction were higher in the
branches than in the stem. In 64% of the stands where both
probabilities were calculated, the growth reductions were
more likely to be observed earlier in branches with a delay
of 1–2 years (Fig. 3).
Discussion
Growth reductions in stem
In all stands with the exception of stand 5, at least one
stem registered a 40% radial growth reduction during the last
known spruce budworm outbreak. A delay of 1–3 years was
registered in growth reduction, which started first in the
upper part of the stem in 13 out of 16 stands.
Two main hypotheses are proposed for this delay. The first
refers to the larvae feeding on needles, which reduces the
photosynthetic surface and consequently decreases the production of sugar and starch (Mott et al. 1957; Piene 1980;
Piene et al. 1981; Archambault 1984). The higher the intensity of defoliation, the greater the reduction in assimilates
produced by trees (Webb and Karchesy 1977). Moreover, the
younger needles that are more effective in photosynthesis are
localized in the upper and outer part of the crown where
growth reduction occurs first (Honkanen and Haukioja
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1225
Fig. 3. Posterior probability of growth reduction in stem at 1 m height and branches within the 16 studied black spruce (Picea mariana)
stands.
0.9
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
0.6
Probability of growth reduction (%)
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0.3
0.9
0.6
0.3
0.9
0.6
0.3
0.9
Branches
0.6
Stem
0.3
1970
1975
1980
1970
1975
1980
1994). Cambium is an important sink for non-structural carbohydrates. Cell production is only possible when carbohydrates are extracted from the storage tissues or produced by
photosynthesis (Oribe et al. 2003; Deslauriers et al. 2009).
Parker and Houston (1971) found a relationship between production of assimilates and growth reduction in the crown. In
endemic periods, carbohydrate production should be high and
translocated to the storage parenchyma cells in the lower
stem and main roots. On the contrary, during defoliation periods, carbohydrates are reduced and the access to storage is
much more difficult given the distance required. A 1- to 2years delay in the occurrence of growth reduction between
crown and stem might also be attributed to the gradual depletion of carbon stocks in the form of starch in the lower stem
and root system. Roots play a key role in the carbon reserves
of trees and contribute as a flywheel to supply energy for the
radial growth of the inner stem during unfavourable periods
(Ericsson et al. 1980; Waring and Schlesinger 1985; Krause
and Morin 1995). This might also explain why no delay was
observed in smaller trees (Krause et al. 2003).
According to the source/sink theory, the lowest priority for
allocating carbohydrates within a plant is given to the xylem
(Polák et al. 2006). Consequently, a second hypothesis suggests that after a defoliation, trees give higher priority to
maintaining efficiency and functionality of the photosynthetic
structures than to sustaining secondary growth, allowing the
correct balance between photosynthesis and respiration to be
maintained (Ericsson et al. 1980; Waring and Schlesinger
1985; Piene 1989). Whenever the assimilates become insufficient for all metabolisms of the tree, the production of new
foliage from dormant and latent buds is more important than
1970
Year
1975
1980
1970
1975
1980
1985
the formation of wide tree rings. On the contrary, in the
lower stem, the absence of branches could allow a major proportion of assimilates to be provided for cambial activity and
secondary growth.
Growth reductions in branches
Growth reductions following the outbreak started 1–2
years earlier in branches than in the stem. Régnière and
Fletcher (1983) found a negative impact of defoliation on
newly formed foliage along the branches of host trees (white
spruce (Picea glauca (Moench) Voss)). During outbreaks,
spruce budworm affects most or all developing needles (Carisey and Bauce 1997), which forces trees to use the assimilates formed by the needles of the previous years to rebuild
the crown (Ericsson et al. 1980). Given that the assimilates
are essential for cell production and differentiation, their production after defoliation negatively affects the radial growth
of the different parts of the tree. Ericsson et al. (1980) suggested that during a defoliation, new branches are produced
on the existing ones from dormant or latent buds to calibrate
the proportion between sources and sinks. Simard and Payette (2003) tested this idea by analysing tree growth anomalies to date spruce budworm infestations and observed
terminal bud mortality and replica replacing of damaged
axes. They found that dating of tree growth anomalies (terminal bud mortality) has better resolution in time and space
than tree-ring patterns to determine the first year of insect defoliation. There is also evidence that starch reductions caused
by defoliation in pine species induce a radial growth reduction in the stem (Webb and Karchesy 1977; Webb 1981;
Långström et al. 1990; Honkanen et al. 1999). Honkanen
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1226
and Haukioja (1994) also observed a substantial growth reduction in younger defoliated branches in comparison with
the older ones for artificial defoliation. On the other hand,
needle production was less reduced when several synchronously defoliated branches on a tree were analysed simultaneously (Honkanen and Haukioja 1994).
More than 65% of stems registered >40% reductions in radial growth compared with 79% of branches. It is likely that
the branches were defoliated neither with the same intensity
nor at the same time. The growth reduction in branches
should be the result of their biomass losses by defoliation,
whereas the stem would represent the global loss of photosynthetic biomass in the whole crown. Our results demonstrated that the effects of defoliation are registered close to
the affected organs and successively spread to the other parts
of the tree, inducing marked reductions in secondary growth
and tree-ring width. Furthermore, given that the most productive photosynthetic biomass is located in the outer canopy,
the growth reduction occurred first in the branches and upper
stem. The fact that branches have been shown to generally
register the outbreaks 1–2 years earlier suggests that branch
radial increment might be a suitable proxy for changes in the
spruce budworm population.
Moreover, the wave of radial growth reduction moves basipetally from the upper to the lower stem. Given that the photosynthetic biomass is located in branches, this part of the
tree is more liable to register the effects of defoliation earlier
due to increases in the insect population.
Future study
Considering that many branches did not cover the calibration period, it would be useful to describe their growth pattern during the actual spruce budworm outbreak.
Furthermore, a higher number of branches distributed over
the entire crown should improve the pattern of growth loss
in black spruce trees. It would also be interesting to validate
this model with investigations on the root system to obtain a
more complete representation of the overall reaction of trees
to spruce budworm outbreaks.
Acknowledgements
This work was funded by the Consortium de Recherche
sur la Forêt Boréale Commerciale and Fonds de Recherche
sur la Nature et les Technologies du Québec. The authors
would like to thank M. Vincent, E. Pamerleau-Couture, A.
Lemay, M. Boulianne, E. Bouchard, M. Blackburn, P.
Émond, G. Savard, and C.A. Déry-Bouchard for technical
support, A. Garside for reviewing the English text, and the
Ministère des ressources naturelles et de la faune (Québec)
to give us access to the defoliation surveys.
References
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