Susceptibility of northern British Columbia forests to spruce budworm defoliation

Susceptibility of northern British Columbia forests tospruce budworm defoliation

Rene I. Alfaroa,*, S. Taylorb, R.G. Browna, J.S. Clowaterc

aCanadian Forest Service, Paci®c Forestry Centre, Victoria, BC, Canada, V8Z 1M5bBC Ministry of Forests, Prince George Region, 1011-4th Ave., Prince George, BC, Canada, V2L 3H9

cDepartment of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada, V5A 1S6

Received 22 October 1999; accepted 21 March 2000

Abstract

Stand susceptibility to defoliation by spruce budworm, Choristoneura fumiferana (Clem.), was examined in the Fort Nelson

area of the Prince George Forest Region of British Columbia. In a retrospective study, defoliation maps of the study area were

overlaid onto British Columbia Ministry of Forests cover type maps using a geographic information system. Analysis of the

combined data identi®ed forest characteristics associated with increased susceptibility to defoliation by spruce budworm.

These were stands where the leading species was white spruce (Picea glauca (Moench) Voss), or where spruce was associated

with aspen (Populus tremuloides Michx. and P. balsamifera L.) in mixed stands. Susceptibility to defoliation also was related

to site quality, level of crown closure and stand age. Spruce stands on medium quality sites (site index 15 to 25 m, at reference

breast height age 50 years) were more susceptible than stands on both poor- and high-quality sites. When spruce was mixed

with aspen, stands on higher quality sites were more susceptible to budworm attack than poor sites. Open stands, where crown

closure was <50%, were more susceptible to attack by spruce budworm than closed canopy stands. Older stands (120±199

years) were more susceptible to budworm attack than younger stands (40±110 years). In defoliated plots monitored for 6 years,

tree mortality and top-kill reached a maximum of 30.4 and 47.2%, respectively. The losses varied with level of defoliation and

were reduced by applications of the biological pesticide Bacillus thuringiensis. Crown Copyright # 2001 Published by

Elsevier Science B.V. All rights reserved.

Keywords: Choristoneura fumiferana; Picea; Insect damage; Landscape level analysis

1. Introduction

Defoliation by spruce budworm, Choristoneura

fumiferana (Clem.), has caused substantial loss to

merchantable timber in eastern Canada and the United

States (MacLean, 1985), and is considered the most

widely distributed and destructive defoliator of

spruce±®r (Picea spp.±Abies spp.) forests in North

America. The spruce budworm is associated primarily

with the boreal forest, with a range extending from the

Atlantic coast to north-central British Columbia (BC)

and north into the Yukon (Harvey, 1985). The main

host defoliated in BC is white spruce (Picea glauca

(Moench) Voss).

The life cycle of the spruce budworm (Miller, 1963)

is similar across Canada. Adult moths emerge from

mid-July to early August, and then they mate and

oviposit on the foliage. Eggs hatch in about 12 days,

and then the ®rst-instar larvae disperse and build

hibernaculae in which they overwinter. In early

Forest Ecology and Management 145 (2001) 181±190

* Corresponding author.

0378-1127/01/$ ± see front matter Crown Copyright # 2001 Published by Elsevier Science B.V. All rights reserved.

PII: S 0 3 7 8 - 1 1 2 7 ( 0 0 ) 0 0 4 0 6 - 0

May, the second-instar larvae emerge and feed ®rst on

staminate ¯owers and last year's needles, and later on

the expanding vegetative buds (Johnson and Lyon,

1991). The majority of damage to the tree foliage is

through defoliation of the current year's needle crop.

The outbreak history of this budworm species is not

well known in BC. Defoliation in the Prince George

Forest Region of BC was ®rst recorded in 1957 near

Liard River (Erickson and Loranger, 1982), but there

is dendrochronological evidence suggesting that defo-

liation has occurred periodically ®ve times in this area

since 1869 (Shore and Alfaro, 1986). In 1962, new

infestations appeared in the Kledo Creek area near

Fort Nelson (Fig. 1), and in 1965 the Canadian Forest

Service recorded a peak defoliation of 194 000 ha

(Fig. 2). Defoliation then decreased and remained

low until reaching a maximum again in 1990

(398 155 ha).

Extensive mortality by spruce budworm creates the

need for prompt salvage before weathering and fungal

deterioration reduces the commercial value of the

timber (Baskerville and MacLean, 1979). These out-

breaks also disrupt planning for sustained yield since

the long-term wood supply is affected (MacLean,

1980).

Stand susceptibility refers to the probability that a

stand would be infested by spruce budworm, while

vulnerability has been de®ned as the probability of

Fig. 1. Geographic location of the study site, near Fort Nelson in the Prince George Forest Region, BC. The area studied included

�1 500 000 ha. Shaded area indicates the maximum extent of budworm defoliation obtained by overlay of defoliation maps from 1986 to

1991.

Fig. 2. Documented history of defoliation by spruce budworm in

the Prince George Forest Region (Source: Forest Insect and Disease

Survey, Natural Resources Canada).

182 R.I. Alfaro et al. / Forest Ecology and Management 145 (2001) 181±190

tree mortality when a stand has been infested by

budworm (Mott, 1963; MacLean, 1982). In eastern

Canada, several research projects have studied stand

vulnerability and susceptibility (MacLean, 1980,

1982; Blais, 1983; Blum and MacLean, 1984; Gagnon

and Chabot, 1989), but no studies have been con-

ducted in the west. In this paper, we studied the

characteristics of stands defoliated by spruce bud-

worm to identify factors associated with susceptibility

to spruce budworm defoliation. In particular, we

related susceptibility to defoliation, to forest charac-

teristics, such as species composition, site index, stand

age, and crown closure. In addition, we measured the

levels of tree mortality and top-kill in research plots

monitored for 6 years (1992±1997) in spruce stands,

which sustained different budworm feeding pressure

and duration.

2. Materials and methods

The study consisted of two parts: ®rst, an analysis of

defoliation and inventory maps conducted in 1992 to

determine the stand characteristics associated with

susceptibility to budworm defoliation; second, tree

mortality and top-kill was monitored in a series of

plots established in 1992 and followed annually until

1997.

2.1. Stand susceptibility to budworm defoliation

In order to study stand characteristics in relation to

susceptibility relative to defoliation, in 1992 we

selected a square area, �1 500 000 ha in size, which

included a large portion of the infestation as well as

many undefoliated areas (Fig. 1). The study site was

located within the Prince George Forest Region of BC,

near the town of Fort Nelson. The area is within the

Boreal White and Black Spruce Biogeoclimatic Zone

(Meidinger and Lewis, 1983), and is de®ned geogra-

phically between 12280000000W and 12480000000Wlongitude and between 5882400000N and 5983600000Nlatitude. Summary characteristics for the study area

are presented in Table 1.

Annual aerial survey maps of defoliation in the Fort

Nelson area were obtained from the Canadian Forest

Service for the years 1986 to 1991, a period which

contained the years of maximum extent of defoliation,

considering all defoliation years in the current out-

break (Fig. 2). Using a PAMAP (PCI Geomatics)

geographic information system, the summary map

of defoliation in the study area was overlaid with

BC Ministry of Forests, Inventory Graphic and Attri-

bute ®les (BC Ministry of Forests, 1999) which con-

tained the forest cover characteristics. The data ®le

resulting from the overlay process contained 53 066

records representing stand attributes and was entered

into DBASE IV for further analysis. All non-forest areas

and non-productive forest lands were excluded from

the analysis.

Maximum extent of defoliation was determined by

overlay of all defoliation maps and was tabulated in

relation to each of the following stand attributes,

which are available from the inventory maps: leading

tree species; secondary species; spruce age class (20-

year intervals); white spruce site index; and crown

closure. Leading species was de®ned as the species of

greatest volume in the stand. Depending on the last

update of the inventory map, stand ages were pro-

jected forward to 1992. The site index used for white

Table 1

Area of stands and percentage area defoliated by spruce budworm in northern British Columbia forests as of 1992, at the start of the study

Leading tree speciesa Total area (ha) Defoliated area (%)

Aspen: Populus tremuloides Michx. and P. balsamifera L. 359 409 5.3

White spruce: Picea glauca (Moench) Voss 204 185 30.6

Black spruce: Picea mariana (Mill.) B.S.P. 140 013 18.1

Lodgepole pine: Pinus contorta Dougl. Ex Loud 62 181 3.3

Birch: Betula papyrifera Marsh. and Betula spp. 56 694 4.7

Larch: Larix laricina (Du Roi) K. Koch 552 18.0

Balsam: Abies lasiocarpa (Hook.) Nutt. 245 9.0

aLeading species is defined as the tree species of greatest volume in the stand.

R.I. Alfaro et al. / Forest Ecology and Management 145 (2001) 181±190 183

spruce was that of Goudie (1984) and was based on a

breast height age of 50 years. Crown closure is the

percent of ground area covered by the vertical projec-

tion of tree crowns and was assumed constant between

the date of the last inventory and 1992.

Statistical analysis was based on total number of

hectares with or without defoliation, and an index of

susceptibility to budworm defoliation (Sui) was cal-

culated for each inventory attribute, as follows:

Sui � 100� �Expÿ Actual�Exp

where: Exp is the expected defoliation (the area of

defoliation which would occur if budworm affected

all stands equally, i.e. the characteristic studied did

not influence susceptibility to budworm), and Actual

represents the actual defoliation. Expected defolia-

tion and significance of differences between actual

and expected defoliation areas were computed using

the procedures for the w2-test (Sokal and Rohlf,

1969).

2.2. Measurement of the tree mortality and top-kill

caused by budworm defoliation

In order to measure the level and progression of tree

mortality and top-kill (dieback of crown as a result of

defoliation) caused by spruce budworm, ®ve plots

were established in 1992 in each of 18 stands that

had sustained different outbreak duration between

1986 and 1991 (Table 2). The selected stands were

divided into ®ve classes according to the number of

years of consecutive defoliation each stand had sus-

tained in the period. Stands that had sustained pro-

tective sprays (2 or 4 years of protection) with the

biological pesticide Bacillus thuringiensis Berliner

(Bt) (Hodgkinson et al., 1979) were placed in different

classes (Table 2).

All stands contained white spruce (Picea glauca

(Moench) Voss) as the leading species, were relatively

open grown (46±75% crown cover) and were located

mostly on medium sites (Site index 12±18 m at breast

height age 50 years, one stand had a site index of

10 m). The research plots in one stand were subse-

quently lost to logging.

In February 1992, ®ve linear plots, each �50 m

long by 2 m wide, were established in each stand. The

start of each line was located at least 50 m inside the

stand. The linear plots were established in a polygon

arrangement (often a pentagon) with 50 m interval

between lines. However, topographic and access lim-

itations sometimes required this plot layout to be

slightly modi®ed. Trees within 1 m of the transect

line, dead or alive, were recorded. A border tree was

counted in, if at least 50% of its diameter was within

1 m of the transect line. Data recorded for each tree

included species, status (alive or dead), level of defo-

liation and, if top-kill was present, the length of the

dieback. A tree was counted as dead if it had 100%

defoliation for two consecutive years. Death was

assumed to have occurred in the ®rst year. A trained

observer assessed defoliation using binoculars to ®rst

divide the living crown into thirds, and then to esti-

mate the amount of total foliage missing from the

crown. Except for 1993, mortality, defoliation and top-

kill were re-measured in annual visits from 1992 until

1997. Defoliation level per tree was not recorded in the

1993 season because of budget constraints.

Mean tree defoliation was calculated for each white

spruce for each year. Then, analysis of variance,

nesting stand into stand class, was used to determine

if there was signi®cant variation by stand class in

Table 2

Stand classes used to determine the impacts of spruce budworm on white spruce

Stand class No.

stands

No. years defoliation

prior to 1992

Spray

years

Mortality prior

to 1992 (%)

Mortality

1992±1997 (%)

Top-killa

1992±1997 (%)

I 2 0 None 17.2 0 0

II 6 3±4 (1988±1991) None 4.2 7.8 47.2

III 6 5±6 (1986±1991) None 28.2 30.4 24.8

IV 2 3±4 1991±1992 7.4 10.9 13.6

V 2 3±4 1989±1992 6.1 7.0 3.2

aTop-kill on surviving spruce (i.e. alive in 1997).


percentages of defoliation, tree mortality, and top-kill.

Percentages were transformed to the arcsine.

3. Results

3.1. Species composition of defoliated stands

Leading species of stands defoliated by the spruce

budworm in the Fort Nelson study area were, in decreas-

ing order of area affected, white spruce (Picea glauca

(Moench) Voss), black spruce (Picea mariana (Mill.)

B.S.P.), aspen (Populus tremuloides Michx. and P. bal-

samifera L.), Birch (Betula papyrifera Marsh. and

Betula spp.), and lodgepole pine (Pinus contorta Dougl.

Ex Loud.) (Table 1). Aspen, birch or pine stands are de-

foliated when the secondary species is a budworm host,

i.e. spruce, balsam (Abies lasiocarpa (Hook.) Nutt.), or

larch (Larix laricina (Du Roi) K. Koch) (Table 1).

Greater than expected defoliation occurred in stands

where the leading species was white spruce or aspen;

lower than expected defoliation of white spruce

occurred if the leading tree species was birch, black

spruce or pine (w2-test, p<0.001) (Fig. 3a). Stands

Fig. 3. Budworm susceptibility of stands defoliated by spruce budworm tabulated by (a) leading species, (b) secondary species, (c) percent

crown closure, and (d) stand age.


where aspen is the leading species and spruce is a

secondary species are the most abundant in the region;

however, only 5.3 % of the area covered by them

sustained defoliation compared to 30.6% of the area in

white spruce leading stands (Table 1).

Among stands with leading white spruce there was a

signi®cant difference in amount of defoliation depend-

ing on which was the associated secondary species

(w2-test, p<0.001) (Fig. 3b). Stands of white spruce

and aspen, white spruce and larch and those of pure

white spruce showed greater than expected defoliation

than mixtures of white spruce with other species.

3.2. Crown closure

Mean crown closure of spruce stands in the Fort

Nelson region was 51.5%, with a minimum of 1%, and

a maximum of 90%. Observed defoliation of spruce

stands with respect to crown closure was signi®cantly

different from expected (w2-test p<0.001) (Fig. 3c).

Open canopy stands with crown closures of 10±50%

sustained signi®cantly more defoliation than stands

with closed canopies.

3.3. Stand age

The age of white spruce stands in the Fort Nelson

study area ranged from 4 to 624 years with a mean of

123 years. However, very few stands were younger

than 30 years or older than 239 years, so these were

excluded from analysis. Observed defoliated area with

respect to age was signi®cantly different from

expected (w2-test, p<0.001) (Fig. 3d). Stands in age

classes 50 to 110 years were defoliated less than

expected, as were the few stands 210 years and older.

Stands in age classes 130 to 190 years, as well as

regeneration stands (age class 30 years) were defo-

liated more than expected.

3.4. Site index

In stands where the leading species was white

spruce, the mean site index was 15.7 m (at breast

height age 50 years), but ranged from 5.0 to

30.0 m. Observed defoliation of stands with respect

to site index was signi®cantly different from expected

defoliation (w2-test p<0.001). Stands on sites with

mid-range indices of 15±25 m were defoliated more

than stands at the extremes of the site index distribu-

tion.

3.5. Tree mortality and top-kill caused by defoliation

With the exception of the no-defoliation plots, bud-

worm continued to defoliate white spruce in all stands

until the termination of the study in 1997 (Fig. 4).

However, a clear difference in defoliation level

occurred by stand class (i.e. prior outbreak duration

or Bt treatment). Stands that were left without aerial

control sustained signi®cantly higher defoliation than

Fig. 4. Percent defoliation of white spruce by spruce budworm, 1992±1997, in areas sustaining different levels of defoliation and protection

prior to 1992. Roman numerals refer to stand classes in Table 2.


stands with Bacillus thuringiensis protection. Defolia-

tion in the stands without control peaked in 1994 at

53±57%, whereas defoliation in the protected stands

remained below 15% throughout the observation per-

iod (Fig. 4). Analysis of variance of the defoliation

data for the year 1994, the year of peak defoliation,

indicated a signi®cant effect of stand class (F�79.8,

p<0.001). However, post-hoc comparisons indicate

that in the year of peak defoliation there were no

differences in defoliation between the two spray treat-

ments, i.e. two Bt sprays provided equal protection to

four sprays (Tukey HSD test, p>0.05). Similarly, by

1994 there were no signi®cant differences in tree

defoliation between unsprayed plots that had sustained

different outbreak lengths before 1992 (stand classes

II and III) (Fig. 4). By 1997, defoliation remained at

levels similar to those of 1994, except in Class III

(defoliated 5±6 years prior to 1992 and not protected)

where defoliation declined to 20%. By 1997, defolia-

tion was most severe in stands in Class II, i.e.

unsprayed plots that had sustained 3±4 years of defo-

liation by 1992. In 1997, defoliation in the sprayed

plots was not signi®cantly different from the undefo-

liated controls (Tukey HSD, p<0.001).

3.6. Tree mortality in the plots before 1992

At the start of the study in 1992, an average 14.8%

of the spruce in the 18 stands were dead. However, not

all mortality could be attributed to budworm defolia-

tion. In fact, undefoliated stands contained an above-

average amount of mortality (17.2%). Other agents of

spruce mortality in this area include spruce beetle and

root rot. Analysis of variance indicated a signi®cant

effect of stand class (F�30.7, p<0.001) on mortality

by 1992. However, because of high plot variability,

only the Class III stands that had sustained the longest

defoliation (5±6 years) had mortality levels (28.2%)

signi®cantly higher than the undefoliated stands by

1992 (Tukey HSD test, p<0.01).

3.7. Tree mortality in the plots between 1992 and

1997

The undefoliated plots sustained no tree mortality

between 1992 and 1997. The annual rate of spruce

mortality remained below 5% in all stands, with the

exception of stands in Class III, which sustained the

longest outbreak duration before 1992 (5±6 years of

defoliation, not protected) and sustained maximum

defoliation during the monitoring period (Fig. 5).

Spruce in this stand class sustained maximum annual

mortality in the year 1995 (12.9%), one year after peak

defoliation. By 1997, mortality in these most severely

defoliated stands (Class III) accumulated to 30.4% of

the spruce that were alive at the start of the observation

period in 1992 (the six stands in this class lost an

average of 338 trees per ha in the period) (Fig. 6).

Mortality in stand classes II, IV and V averaged only

8.7% of the spruce (66 trees/ha) in the period. Since

Fig. 5. Annual rate (%) of spruce mortality in stands sustaining different levels of defoliation by spruce budworm and that were sprayed or not

sprayed with Bacillus thuringiensis. Roman numerals refer to stand classes in Table 2.


undefoliated stands sustained no mortality in this

period, all this mortality is probably attributable to

budworm defoliation.

Adding the existing mortality by 1992 to the mor-

tality accumulated during the observation period, we

arrive at total spruce mortality, as of 1997, of 17.2,

12.0, 58.6, 18.3 and 13.1% in stand classes I to V,

respectively. However, as explained earlier, the high

level of mortality in the undefoliated stands indicates

that other mortality agents are also active in these

boreal stands.

3.8. Top-kill

On average, 27.9% of surviving spruce in defoliated

stands sustained top-kill, with a length of crown die-

back averaging 1.6 m. The proportion of surviving

spruce which sustained top-kill varied signi®cantly by

stand class ((w2-test�139, p<0.001) (Table 2). No top-

kill occurred in undefoliated stands and maximum

top-kill (47.2%) occurred in stands in Class II, defo-

liated 3±4 years before 1992 and not sprayed. A lower

percentage of top-kill (24.8%) was registered in the

stands in Class III, which sustained a longer outbreak

duration prior to 1992, and more severe defoliation

thereafter, than stands in Class II, due to increased

mortality among trees in this class. Stands protected

for only two years sustained 10.4% more top-kill than

stands that had been protected for four years (13.6%

vs. 3.2%).

4. Discussion

Of the species known to be attacked by the spruce

budworm in eastern Canada, Abies balsamea (L.)

Mill., is generally considered the most susceptible,

followed by white spruce, red spruce, and black spruce

(Greenbank, 1963; Kucera and Orr, 1981; Blum and

MacLean, 1984; Blais, 1985; Harvey, 1985). However,

in BC, stands where the closely related Abies lasio-

carpa was the leading species formed only 0.03%

(245 ha) of the total productive forest (823 279 ha) in

the Fort Nelson study area (Table 1). Of these, only

21.7 ha (of 245 ha) were defoliated. Most defoliation

occurred in stands where the leading species was

white spruce, black spruce or aspen. However, only

stands where the leading species was white spruce or

aspen sustained more defoliation than expected

(Fig. 3a). White spruce stands, where the secondary

species was aspen or larch, also were defoliated more

than expected (Fig. 3b). Stands with leading species of

black spruce, pine, or birch all were defoliated less

than was expected (Fig. 3a). Studies in eastern Canada

(Greenbank, 1963; Carlson, 1987), indicate that host

selection during oviposition favours balsam ®r and

white spruce over black spruce. Synchronization of

spring larval emergence and budburst is important for

spruce budworm survival (Shepherd, 1985; Carlson,

1987; Lawrence et al., 1997) and other defoliators

(Carroll, 1999), and may account for host preferences

in BC. Optimal survival occurs when larval emergence

Fig. 6. Cumulative mortality (%), 1992±1997, in stands sustaining different levels of defoliation by spruce budworm and that were sprayed or

not sprayed with Bacillus thuringiensis.


from overwintering precedes budburst by about 2

weeks (Lawrence et al., 1997). Trees on which bud-

burst occurs before larval emergence are less suscep-

tible to budworm attack.

Aspen±spruce stands sustained more defoliation

than stands of pure spruce. This may be due to the

fact that aspen creates more openings in the canopy, as

well as more variation in tree heights. In addition,

defoliation generally was higher than expected in

more open stands with crown closure <50%

(Fig. 3c). These characteristics allow increased expo-

sure of crowns, thereby increasing egg deposition sites

(Morris and Mott, 1963), while also improving the

microclimate for feeding larvae by increasing heat

accumulation (Shepherd, 1959; Mott, 1963).

Our results indicate that young stands of mean age

39±119 years were defoliated less than expected

(Fig. 3d) and older stands, 120±199 years old, were

defoliated more than expected. These results agree with

those of Balch (1946) who found that in balsam ®r

forests, older stands are more susceptible, as well as

large, more continuous stands, and stands with higher

stem densities. Maturity is often accompanied by

increasing crown exposure and may be the important

factor associated with age (Mott, 1963). At each end of

the age spectrum the trend was reversed, very young

stands were defoliated more than expected and very old

stands were defoliated less than expected. However,

these observations may be in¯uenced by the low num-

ber of samples at the extremes of the age distribution.

Susceptibility to budworm attack was more than

expected in sites with mid-range site indexes than on

very poor or very good sites. We hypothesize that

stands on poor or above-average sites may be defo-

liated less than expected because trees on these sites

may have foliage qualities that are less favorable to the

female moths or larvae. Variation in soil fertility may

affect the carbon/nutrient balance of spruce, thereby

affecting the amount of carbohydrates available for

synthesis of secondary metabolites involved in plant

defense against herbivores (Mattson et al., 1991;

Lawrence et al., 1997). Trees growing on poor soils

may have the bene®t of higher accumulation of sec-

ondary metabolites available for defense than medium

or fast growing trees (Bryant et al., 1983; Reichardt

et al., 1991).

Periodic monitoring of plots indicated that spruce

budworm is a signi®cant disturbance agent in these

northern ecosystems. During the observation period

(1992±1997), tree mortality exceeded 30% in unpro-

tected stands with 5±6 years of defoliation before

1992. Areas susceptible to these loss levels were

mature stands (age 120 years or older), open grown,

with white spruce or aspen/white spruce as the leading

species. Management of these northern ecosystems

will require the identi®cation of these stands as

high hazard so that they are targeted for periodic

monitoring.

Acknowledgements

We acknowledge the superb technical assistance

provided by retired technician Emil Wegwitz who

battled extreme weather conditions and mosquitoes

to obtain the ®eld data. Robert Hodgkinson, BC

Ministry of Forests, Prince George, conducted the

aerial sprays with Bacillus thuringiensis. The work

was conducted with funding from the Federal Govern-

ment Green Plan and from the BC Ministry of Forests,

Prince George Region. GIS overlay was conducted by

Forgis Resource Consultants Ltd. The Forest Insect

and Disease Survey of the Canadian Forest Service

produced the defoliation maps.

References

Balch, R.E., 1946. The Spruce Budworm and Forest Management

in the Maritime Provinces. Can. Dept. Agr., Entomol. Div.,

Proc. Publ. No. 60.

Baskerville, G.L., MacLean, D.A., 1979. Budworm-caused mor-

tality and 20-year recovery in immature balsam fir stands.

Canadian Forestry Service, Maritimes Forest Research Centre,

Inf. Rep. M-X-102.

BC Ministry of Forests, 1999. Resources inventory digital data

maps. 722 Johnson St., Victoria, BC. V8W 3E7.

Blais, J.R., 1983. Predicting tree mortality induced by spruce

budworm: a discussion. For. Chron. 59, 294±297.

Blais, J.R., 1985. The ecology of the eastern spruce budworm: A

review and discussion. In: Sanders, C.J., Stark, R.W., Mullins,

E.J., Murphy, J. (Eds.), Recent Advances in Spruce Budworms

Research: Proceedings of the CANUSA Spruce Budworms

Research Symposium. Canadian Forestry Service, Ottawa,

pp. 49±49.

Blum, B.M., MacLean, D.A., 1984. Silviculture, forest manage-

ment, and the spruce budworm. In: Spruce Budworms hand-

book: Managing the spruce budworm in eastern North America.

USDA For. Serv., Agr. Handbook, No. 620, pp. 83±102.


Bryant, J.P., Chapin III, F.S., Klein, D.R., 1983. Carbon/nutrient

balance of boreal plants in relation to vertebrate herbivory.

Oikos 40, 357±368.

Carlson, C.E., 1987. Effects of site and stand conditions on

budworm outbreaks. In: Western spruce budworm and forest-

management planning, USDA Forest Service, Techn. Bull. No.

1696, pp. 5±7.

Carroll, Allan L., 1999. Physiological adaptation to temporal variation

in conifer foliage by a caterpillar. Can. Entomol. 131, 1±11.

Erickson, R.D., Loranger, J.F., 1982. History of population

fluctuations and infestations of important forest insects in the

Prince George Forest Region 1942±1982. Forest Insect and

Disease Survey, Canadian Forest Service, Victoria, Canada.

Gagnon, R.R., Chabot, M., 1989. A system to evaluate spruce

budworm stand vulnerability: principles and use. In: Woodl.

Sect., Can. Pulp and Paper Assoc., Proc. 70th Annual Meeting,

held at Montreal, PQ, 21±22 March, 1989. Canadian Pulp and

Paper Association, Montreal, pp. 127±134.

Goudie, J.W., 1984. Height growth and site index curves for

lodgepole pine and white spruce and interim managed stand

yield tables for lodgepole pine in British Columbia. Research

Branch, BC Ministry of Forests, Victoria.

Greenbank, D.O., 1963. Host species and the spruce budworm. In:

Morris, R.F. (Ed.), The Dynamics of Epidemic Spruce

Budworm Populations. Entomol. Soc. Can. Memoirs, No. 31,

pp. 219±222.

Harvey, G.T., 1985. The taxonomy of the coniferophagous

Choristoneura (Lepidoptera:Tortricidae): a review. In: Sanders,

C.J., Stark, R.W., Mullins, E.J., Murphy, J. (Eds.), Recent

Advances in Spruce Budworms Research: Proceedings of the

CANUSA Spruce Budworms Research Symposium. Canadian

Forestry Service, Ottawa, pp. 16±48.

Hodgkinson, R.S., Finnis, M., Shepherd, R.F., Cunningham, J.C.,

1979. Aerial applications of nuclear polyhedrosis virus and

Bacillus thuringiensis against western spruce budworm. Joint

report 10, BC Ministry of Forests and Canadian Forest Service,

Victoria.

Johnson, W.T., Lyon, H.H., 1991. Insects that feed on trees and

shrubs, 2nd Edition. Cornell University Press, Ithaca, NY.

Kucera, D.R., Orr, P.W., 1981. Spruce budworm in the eastern

United States. Forest Insect and Disease Leaflet 160, USDA

Forest Service.

Lawrence, R.K., Mattson, W.T., Haack, Robert, 1997. White spruce

and the spruce budworm: defining the phenological window of

susceptibility. Can. Entomol. 129, 291±318.

MacLean, D.A., 1980. Vulnerability of fir-spruce stands during

uncontrolled spruce budworm outbreaks: a review and discus-

sion. For. Chron. 56, 213±221.

MacLean, D.A., 1982. Vulnerability rating of forests in New

Brunswick and Nova Scotia to budworm attack. Can. For. Serv.,

Mar. For. Res. Cent., Inf. Rep. M-X-132.

MacLean, D.A., 1985. Effects of spruce budworm outbreak on

forest growth and yield. In: Sanders, C.J., Stark, R.W., Mullins,

E.J., Murphy, J. (Eds.), Recent Advances in Spruce Budworms

Research: Proceedings of the CANUSA Spruce Budworms

Research Symposium. Canadian Forestry Service, Ottawa,

pp. 148±175.

Mattson, W.J., Haack, R.A., Lawrence, R.K., Slocum, S.S., 1991.

Considering the nutritional ecology of the spruce budworm in

its management. For. Ecol. Manage. 39, 183±210.

Meidinger, D., Lewis, T., 1983. Biogeoclimatic zones and subzones

of the Fort Nelson Timber Supply Area, BC. Northern Fire

Ecology Project, BC Ministry of Forests Research Branch,

Victoria.

Miller, C.A., 1963. Life cycle of the spruce budworm. In:



pp. 12±19.

Morris, R.F., Mott, D.G., 1963. Dispersal and the spruce budworm.

In: Morris, R.F. (Ed.), The Dynamics of Epidemic Spruce


pp. 180±189.

Mott, D.G., 1963. The forest and the spruce budworm. In:


Budworm Populations. Entomol. Soc. Can. Memoirs No. 31,

pp. 189±202.

Reichardt, P.B., Chapin III, F.S., Bryant, J.P., Mattes, B.R.,

Clausen, T.P., 1991. Carbon/nutrient balance as a predictor of

plant defense in Alaskan balsam poplar: Potential importance

of metabolite turnover. Oecologia 88, 401±406.

Shepherd, R.F., 1959. Phytosociological and environmental

characteristics of outbreak and non-outbreak areas of the two-

year cycle budworm, Choristoneura fumiferana. Ecology 40

(4), 608±620.

Shepherd, R.F., 1985. A theory on the effects of diverse host-

climatic environments in British Columbia on the dynamics of

western spruce budworm. In: Sanders, C.J., Stark, R.W.,

Mullins, E.J., Murphy, J. (Eds.), Recent Advances in Spruce

Budworms Research: Proceedings of the CANUSA Spruce

Budworms Research Symposium. Canadian Forestry Service,

Ottawa, pp. 49±59.

Shore, T.L., Alfaro, R.I., 1986. The spruce budworm, Choristo-

neura fumiferana (Lepidoptera: Tortricidae), in British Colum-

bia. J. Entomol. Soc. BC 83, 31±38.

Sokal, R.R., Rohlf, F.J., 1969. Biometry. W.H. Freeman, San

Francisco, CA, 776 pp.


Susceptibility of northern British Columbia forests to spruce budworm defoliation

Documents

Transcript of Susceptibility of northern British Columbia forests to spruce budworm defoliation