Annals of Botany 85 : 137–142, 2000
Article No. anbo.1999.1007, available online at http:\\www.idealibrary.com on
Fire Tolerance and the Fire-related Sprouting Characteristics of
Two Cool-temperate Broad-leaved Tree Species
K A Z U H I K O M A S A KA*†, Y A S U Y U K I O H N O‡ and K E N J I Y A M A DA‡
* Hokkaido Forestry Research Institute, Dohoku Branch Station, Homare 300, Nakagawa, Hokkaido 098-2805,
Japan and ‡ Hokkaido Forestry Research Institute, Dohoku Branch Station, Otoineppu Sub-Station, Otoineppu,
Hokkaido 098-2501, Japan
Received : 13 August 1999
Returned for revision : 3 September 1999
Accepted : 28 September 1999
This study was conducted in a secondary broad-leaved forest in northern Hokkaido, Japan, which burned on 20–21
April 1998. The study plot, set up on 13 July 1998, contained Quercus mongolica var. grosseserrata and Betula
platyphylla var. japonica trees. The latter were more severely damaged by the fire. Size-dependent survivorship was
observed in both species with larger trees being more likely to survive the fire. However, many large Betula trees were
completely destroyed. Both species developed abundant root collar sprouts immediately after the fire. The number
of sprouts ranged from 0 to 296 in Betula and from 0 to 34 in Quercus. Trees with no sprouts were not necessarily
dead. The frequency distribution of the sprouting pattern in Betula was bimodal. This was related to damage severity,
with the most abundant sprouting manifest in the most severely damaged trees. This pattern was not observed in
Quercus. Stem diameter also appeared to influence the extent of sprouting in Betula, while in Quercus there was no
distinct correlation between basal area and the number of sprouts. In Betula, the relationship between the number
of sprouts and the damage severity suggests a trade-off in resource allocation for sprouting Šs. shoot flushing in
the crown.
# 2000 Annals of Botany Company
Key words : Betula platyphylla var. japonica, fire, fire tolerance, Quercus mongolica var. grosseserrata, resource
allocation, root collar sprouting, stem diameter size.
INTRODUCTION
Fire commonly disturbs forests worldwide and many tree
species respond by sprouting, even after most of their
foliage has been destroyed (Kozlowski et al., 1991). It is well
known that trees in semi-arid regions are particularly well
adapted to fire and have a vigorous sprouting ability that
enables them to survive recurring fire (Trabaud and Lepart,
1980 ; Uemura et al., 1990 ; Lo! pez-Soria and Castell, 1992).
On the other hand, trees of tropical rainforests, in which
naturally-occurring fires are rare and where trees are believed
to show very few adaptations related specifically to post-fire
survival, can also sprout and survive after an intense fire
(Kauffman, 1991). However, there is very little documentation of the sprouting response of trees following fire
in moist temperate forests, where fire is often caused by
human activity.
The loss of leaves in a fire generally releases the dormancy
of specialized ‘ epicormic ’ buds that survive under the bark
(Kozlowski et al., 1991). The ability of trees to sprout from
the root collar and stem is a species-specific characteristic
(Kauffman, 1991 ; Bellingham et al., 1994, 1996 ; Sonoyama
et al., 1997) that is closely connected to patterns of resource
deployment (Sakai and Sakai, 1998). Bellingham et al.
(1994) reported sprouting of trees in Jamaican montane
forests in response to severe physical damage caused by
strong wind, and showed that broken trunks produced more
sprouts than intact trunks, despite the fact that there was no
† For correspondence. E-mail masaka!hfri.bibai.hokkaido.jp
0305-7364\00\010137j06 $35.00\0
difference between uprooted and upright trunks. Although
the branches of a tree are likely to still be alive after the
foliage is stripped by a strong wind, almost all the minor
branches are likely to succumb to a crown fire. That is, the
severity of fire damage to the crown should have a much
greater effect than wind damage on sprouting ability.
Furthermore, the greater the severity of the crown damage,
the more seriously species- and size-specific sprouting ability
is affected, since fire tolerance and resource storage strategies
vary with species and individual size. Sakai and Sakai (1998)
cut the trunks of several tree species at various heights, and
demonstrated that the resource storage strategy and resource
deployment patterns were strongly related to sprouting
ability. However, there are few studies of the relationships
between fire tolerance, severity of damage, and sprouting
ability of species and individual trees.
In Hokkaido, northern Japan, large-scale fires were
frequent following settlement in the Meiji Era (late 19th
century) until early in the Showa Era (early 20th century)
(e.g. Takaoka and Sasa, 1996). Many of the forests in the
region have never recovered sufficiently to resume the normal
process of succession (e.g. Takaoka and Sasa, 1996). Small
fires still occur sporadically and continue to influence forests
in the region. A fire at Nishiokoppe in northern Hokkaido
in 1998 presented an opportunity to document the immediate
effects of fire and to consider their long-term implications
on forest composition. In this study, we addressed the
following questions. (1) Were there differences in the ways
in which trees of different size and species were affected
during the fire ? (2) To what extent does sprouting ability
# 2000 Annals of Botany Company
Masaka et al.—Fire Tolerance and Subsequent Sprouting in Broad-leaŠed Trees
differ with size and species ? (3) To what extent does the
severity of damage affect the sprouting ability of individual
trees ? The answers to these questions should allow us to
consider the implications of fire damage on the dynamics of
cool-temperate broad-leaved forests, such as those in
northern Hokkaido, Japan.
MATERIALS AND METHODS
Study site
The study was carried out in a secondary cool-temperate
broad-leaved forest in Nishiokoppe, northern Hokkaido,
Japan (43m 30h N, 142m 55h E, 220 m a.s.l). Betula platyphylla
var. japonica Hara and Quercus mongolica var. grosseserrata
Rehd et Wils. are the dominant species. Other species, such
as Populus tremula var. daŠidiana Schnneid, Acer mono
Maxim, Magnolia oboŠata Thunb., Sorbus alnifolia C.
Koch, and Kalopanax pictus Nakai, are sometimes mixed in
the forest. The soil is locally referred to as brown forest soil,
and the forest floor is mainly covered with dwarf bamboo,
Sasa senanensis Rehder. Precipitation in the region is
approx. 1100 mm per year. The mean monthly temperatures
during the warmest (August) and coldest (January) months
are 18n5 and k7n2 mC, respectively. A warmth index of
52n0 mC month indicates that the region is located between
the cool-temperate and sub-boreal zones (Kira, 1977). The
forest floor is usually snow-covered from December until
the following April. Nishiokoppe belongs to the Okhotsk
climatic zone. The foehn (l fo$ hn) phenomenon in early
spring, just after the snow cover disappears, is a climatic
characteristic of the region (O# kawa, 1992). The foehn
phenomenon involves warm dry winds that blow down
from the mountains.
The study area burned on 21–22 April 1998, when the air
temperature reached a maximum of 27n9 mC with the foehn
phenomenon. Almost all of the vegetation on the forest
floor was burned and when we surveyed the forest on 22
June 1998, there were abundant sprouts from the root
collars of injured deciduous broad-leaved trees.
An 80 mi10 m study plot was established in the burned
forest on the gentle sloping ridge of a hill on 13 July 1998.
Trees in the study plot were tagged ; their stem diameter at
breast height (dbh) was measured and the number of new
sprouts counted. The species composition in the study plot
is shown in Figure 1. The principal species studied were B.
platyphylla var. japonica and Q. mongolica var. grosseserrata,
the dominant species in the study plot. Hereafter, we will
refer to these two species as Betula and Quercus, respectively.
There were no sprouts from the upper trunks, so in this
paper, the term ‘ sprout ’ is restricted to ‘ root collar sprout ’.
There were a few sprouts that had been damaged by
herbivores, such as rodents, and these were counted together
with the current undamaged sprouts.
Damage severity was divided into the following categories,
scoring crown survival score by eye measurement : 0, no
foliage in the crown, only a standing trunk remained, which
was considered to be dead ; 1, less than 25 % of the foliage
survived and the majority of the crown was lost ; 2, partially
damaged, 25–75 % of the foliage survived ; 3, damaged, but
25
20
Frequency (no.)
138
15
10
5
0
10
20
dbh class (cm)
30
F. 1. Size-class frequency histograms in the study plot. () Betula
platyphylla var. japonica ; (9), Quercus mongolica var. grosseserrata ;
( ) Acer japonica and A. mono ; (8) Kalopanax pictus ; (
) Magnolia
oboŠata, Prunus sargentii and Tilia japonica.
more than 75 % of the foliage survived ; 4, intact, unscathed
crown.
Large trees are expected to tolerate fire better than small
trees, because their crown is more elevated and their bark is
thicker. One-way ANOVA was conducted to test the
differences in stem size (dbh) and survival score. The
mortality of each dbh class was defined as the proportion of
trees with a survival score l 0 compared to the number of
trees in the dbh class. The resource potential of the surviving
body of the tree was therefore assessed largely in relation to
the size of tree. A regression analysis was also conducted to
evaluate the relationship between trunk size expressed as the
log-transformed basal area (BA l π[dbh\2]#) to the logtransformed (number of sproutsj1) for different survival
scores. These analyses were applied to both Betula and
Quercus.
RESULTS
SurŠiŠal mode during fire
The relationship between survival score and tree size was
positive in both species (Fig. 2 A and B ; one-way ANOVA
and Tukey’s HSD test, P 0n05). As expected, these results
indicated that fire damaged small trees more intensively
than large trees. The mortality of Betula was higher than
that of Quercus in all size-classes (Fig. 3). Many large Betula
trees were dead, while few large Quercus trees died, making
the mortality of the large Betula much higher than that of
Quercus (Fig. 3). The crown position of each species seemed
to have no effect on the damage severity, since the bark of
branches in the crown was not charred.
Sprouting characteristics
We observed vigorous sprouting in both species. The
maximum number of sprouts in Betula was 296, while in
Quercus it was 34. The sprouting frequency distribution was
bimodal in Betula, and L-shaped in Quercus (Fig. 4 A and
Masaka et al.—Fire Tolerance and Subsequent Sprouting in Broad-leaŠed Trees
30
139
A
A
20
b
a
ab
20
ab
15
10
Number of trees
a
dbh (cm)
10
0
30
0
1
2
3
4
b
21 < 22 < 23 < 24 < 25 < 26 < 27 < 28 < 29
0
20
21 < 22 < 23 < 24 < 25 < 26 < 27 < 28 < 29
B
20
5
0
Number of sprouts
a
F. 4. Log-scaled number-class frequency histogram of sprouts per
tree for B. platyphylla var. japonica (A) and Q. mongolica var.
grosseserrata (B). Survival scores : (
) 0 ; (8) 1 ; ( ) 2 ; (9) 3 ; () 4.
0
1
2
3
Survival score
4
F. 2. Boxplots of the dbh of B. platyphylla var. japonica (A) and Q.
mongolica var. grosseserrata (B) for different survival scores. The
sample is represented as a box whose top and bottom are drawn at the
upper and lower quartiles, respectively. The box is divided at the
median. Vertical lines are drawn from the top and bottom of the box
to the 90th and 10th percentiles, respectively. The closed square indicates
the mean dbh. Means that share the same letter do not differ
significantly within species (P 0n05).
100
Tolerance to fire
60
40
20
10
20
not observed in Quercus (Fig. 4 B). The stem diameter
appeared to influence sprouting in Betula (Fig. 5 A ; R# l
0n181, F , l 11n928, P 0n002, n l 56), especially in the
" &%
dead trees (survival score l 0) (R# l 0n755, F , l 40n107,
" "$
P 0n001, n l 15). However, there was no significant correlation between basal area and the number of sprouts when
the trees without sprouts were excluded from the analysis.
In Quercus, there was no correlation between basal area and
the number of sprouts (Fig. 5 B ; R# l 0n049, F , l 1n704,
" $$
P 0n20, n l 35). In Quercus, the maximum number of
sprouts was seen in slightly larger and partially surviving
trees.
DISCUSSION
Betula
Quercus
80
Mortality (%)
20
10
a
0
25
0
b
20
0
0
15
B
b
10
5
30
dbh size-class (cm)
F. 3. Mortality of trees in each size class.
B). In Betula, the two peaks suggest alternative responses of
sprouting or not sprouting. The mean number of sprouts is
likely to increase with damage severity. These features were
In the study plot, the fire tolerance and sprouting ability of
Betula differed markedly from that of Quercus. The fire only
slightly damaged large Quercus trees (Fig. 2 B), which
suggests that the bark of these trees was thick enough to
resist the fire. The bark of oaks contains abundant
sclerenchyma tissue, especially interlocking fibres. Consequently, cells outside the periderm remain coherent, resulting
in a very thick bark and, hence, a high tolerance to fire
(Kramer and Kozlowski, 1979). On the other hand, although
size-dependent tolerance also applied in Betula, many large
trees were completely burned (Fig. 2 A). The bark of birch
species is thin and contains large amounts of terpene,
contributing to its low critical temperature for ignition. The
relatively inflammable Betula bark probably contributes to
the bimodal distribution of damage severity (Fig. 2 A). A
difference in fire tolerance related to bark thickness is also
recognized in fire–prone ecosystems such as Siberian taiga
Masaka et al.—Fire Tolerance and Subsequent Sprouting in Broad-leaŠed Trees
500
500
A
Number of sprouts + 1
140
100
Number of sprouts + 1
10
1
10
500
100
100
10
break point = 2·135
1
10
1000
0
1
2
3
4
100
1000
Basal area (cm2)
B
F. 6. Simulation of tree-size–sprouting relationship for different
survival scores in B. platyphylla var. japonica. The survival score is
shown in the inset box.
100
area (ln B) and the survival score (S ) by piecewise regression
analysis in order to consider the alternatives. The following
significant relationships were derived :
10
ln NS lk1n889j0n497 ln Bk0n041 S
for NS
2n135
and
1
10
ln NS l0n054j0n799 ln Bk0n270 S
100
1000
Basal area (cm–2)
F. 5. Relationship of basal area to sprouts per tree for different
survival scores in B. platyphylla var. japonica (A) and Q. mongolica var.
grosseserrata (B). A regression line could only be fitted for the trees
with survival score l 0 in B. platyphylla var. japonica (R# l 0n755,
F , l 40n107, P 0n001, n l 15). Survival scores : ($) 0 ; (>) 1 ;
" "$
(=) 2 ; () 3 ; (#) 4.
(Chugnova, 1979 ; Uemura et al., 1990) and Australian
eucalyptus (Gill and Ashton, 1968).
Sprouting ability and resource allocation
All the sprouts observed in the study plot were clearly
disturbance-induced. Heating per se, rather than charring,
was likely to be responsible for causing dormant buds to
germinate, since many sprouts were observed on intact,
uncharred Betula trees (Fig. 4 A). Whether sprouting occurs
in Betula (Fig. 4 A) should largely reflect the amount of
resources available in the tree. These characteristics of
sprouting led us to expect there to be a critical size for
sprouting ability, since there is a positive correlation between
basal area and number of sprouts. In addition, the mean
number of sprouts in Betula is likely to increase with
damage severity, since the most abundant sprouting was
observed in the most severely damaged trees (Fig. 4 A). Such
obvious differences in sprouting strategy suggest the
presence of a ‘ switch ’ in the allocation of resources to
sprouting and away from shoot flushing in the crown.
Therefore, we compared the log-transformed (number of
sproutsj1) (ln NS) with both the log-transformed basal
for NS 2n135
(R# l 0n841, F , l 67n420, P 0n001, n l 56 ; Fig. 6).
% &"
Tree size and damage severity explained at least 84 % of the
variation in the sprouting ability of Betula. This shows that
sprouting occurs above a critical size. Although a positive
correlation between individual tree size and the number of
sprouts has been recognized in several tree species (Jones
and Raynal, 1987 ; Giovannini et al., 1992), little has been
reported on a critical size for sprouting. The dormant basal
buds of birch species are likely to form clusters (Kauppi et
al., 1987), and the number of clusters is positively correlated
with tree size (Kauppi et al., 1988). The relationship
between the number of clusters of dormant buds and tree
size would be one of the causes of a critical size for sprouting
ability.
In addition, we showed that the greater the damage a tree
sustained, the more sprouts that subsequently emerged.
This suggests that trees without living branches in the crown
are still able to allocate resources to initiate sprouting, while
trees with some surviving branches are able to allocate
resources to both new sprouts and shoot flushing in the
crown. Kauffman (1991) investigated survival by sprouting
of tropical rain forest trees following fire, and reported that
the more severe the fire, the greater the proportion of trees
which produced sprouts. On the other hand, sprouts from
broken stems must reach a certain minimum size to display
sufficient photosynthetic surface to support the root system
(Peterson and Pickett, 1991). Therefore, there are thought
to be trade-offs in resource allocation between sprouting
and shoot flushing in the crown.
By contrast, alternative sprouting strategies were not
observed in Quercus, and there was no relationship between
ln Ns and ln B or S as observed with Betula. In general, oak
Masaka et al.—Fire Tolerance and Subsequent Sprouting in Broad-leaŠed Trees
species have a well-developed tap root containing abundant
carbohydrates (Sakai et al., 1997), and it has been assumed
that there is a tap root storage strategy for surviving fires
(Crow, 1988). The weak trend in sprouting ability of
Quercus in the study site is probably due to tap root
development ; Betula develops rootlets rather than a tap
root (Kozlowski, 1971). The resource storage strategy of the
root should therefore affect the sprouting ability of trees
(Sakai and Sakai, 1998) ; however, we have no information
on the extent of starch reserves in these species and whether
this might explain the greater sprouting of Betula. The
mortality and recruitment rate of sprouts must be studied
for further discussion. In addition, the oak involved in our
study is considered to be well adapted to fire, since large
trees are well protected by virtue of their thick bark. Indeed,
in this species, mild fires might be insufficient to stimulate
the sprouting of dormant buds.
With regard to resource allocation, the impact of a fire on
the plant community is also likely to be determined by the
season in which the fire occurs. For example, it is well
documented that sprouting is least abundant in stumps
when a newly fully-leafed-out tree is sawn down in spring,
when carbohydrate reserves are likely to be at lowest level,
whereas there is abundant sprouting from stumps of trees
which have been cut during the dormant season (Crawley,
1986 ; Malanson and Trabaud, 1988). In the study plot, the
fire occurred before the trees leafed out, and the prolific
sprouting that followed the fire must have been related to
the season in which it occurred (Clark and Liming, 1953 ;
Malanson and Trabaud, 1988 ; Babeux and Mauffette,
1994 ).
In conclusion, we suggest that the relatively high tolerance
to fire shown by Quercus will allow it to become progressively
dominant in areas where there are frequent fires. Conversely,
the mortality of large Betula trees in the study area suggests
that its abundance will decline under similar fire regimes
(Fig. 2 A and B). In a similar manner in the eastern United
States, fire is considered to have played a vital role in
maintaining oak dominance before European settlement
(Abrams, 1992). Fire should favour oaks because of their
thick bark, sprouting ability, resistance to rotting after fire
scarring, and the suitability of fire-created seedbeds for
acorn germination (Lorimer, 1985). In our study site,
however, the sprouting ability of Betula was much higher
than that of Quercus (Fig. 3). The surviving Quercus canopy
trees appeared to be shading their own sprouts, whereas the
sprouts of Betula were not shaded by mother trees which
had lost their crowns. Therefore Betula, in contrast, seems
to have a greater advantage for regeneration by sprouting
than Quercus, unless fires occur at high frequency. These
differences might be related to post-fire seed establishment.
The dynamics of sprout populations under heterogeneous
light regimes on the forest floor would be an interesting
aspect for further study.
A C K N O W L E D G E M E N TS
We are grateful to Drs M. D. Abrams, J. S. Pate, and an
anonymous referee for their invaluable comments and
suggestions on the manuscript, and for correcting the
141
English. We are also grateful to Dr K. Umeki, T.
Egawa, M. Honda and Y. Takahashi for their help in the
field survey ; Y. Kawai for translating the Russian text ; and
Hokkairyokka Inc. for permission to conduct our survey in
the company-owned forest.
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